WT1 Cancer Vaccine for the Treatment and Prevention
Main Article Content
Abstract
Wilms’ tumor gene 1 (WT1) overexpresses in almost all kinds of hematological malignancies and solid tumors (hereinafter referred to as cancer). Therefore, WT1 protein is a ubiquitous tumor-associated antigen (TAA). Many clinical studies of WT1-targeted cancer immunotherapies (hereinafter referred to as WT1 cancer vaccine), including WT1 peptide vaccine, WT1 peptide-pulsed dendritic cell (WT1-DC) vaccine, and WT1 mRNA-electroporated dendritic cell (WT1 mRNA-DC) vaccine had been conducted for the treatment of almost all kinds of cancer. The clinical effect was promising, whereas the major side effects were the temporary fever and skin reaction on the vaccine injection sites and not significant. The appropriate combination therapy of WT1 cancer vaccine and chemotherapy enhanced WT1 immune response against cancer. Gemcitabine (GEM), for example, increased WT1 immune response through the promotion of the expression of WT1 antigen protein and HLA class I/II molecules in cancer. Furthermore, WT1 cancer vaccine immediately after hematopoietic stem cell transplantation (HSCT) induced sufficient WT1 immune response regardless of severe immunocompromised conditions and exerted sufficient clinical effect, suggesting that the immune condition immediately after HSCT should be suitable for the priming of WT1 immune response. Moreover, the combination therapy of WT1 cancer vaccine and immune checkpoint inhibitors (ICIs) was promising. Compared to the other TAAs, WT1 is especially unique in that it expresses not only in cancer cells but also in their stem cells at the quiescent state of cell-cycle, which are resistant to chemo-and radio-therapies. This uniqueness of WT1 largely contributes to cure cancer through the complete eradication of WT1-expressing cancer stem cells by WT1 immune response against them. Since the complete eradication of cancer stem cells is essential to cure cancer, and since only immune cells against cancer are considered to be able to kill the cancer stem cells at the quiescent state of cell-cycle, the introduction of immunotherapy, especially of WT1 cancer vaccine with sufficient safety is essential in the cure-oriented treatments of cancer. Accumulated clinical results suggest that WT1 cancer vaccine should be useful for cancer prevention, and the development of WT1 cancer prevention vaccine is awaited.
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How to Cite
SUGIYAMA, Haruo.
WT1 Cancer Vaccine for the Treatment and Prevention.
Medical Research Archives, [S.l.], v. 10, n. 4, apr. 2022.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2762>. Date accessed: 22 dec. 2024.
doi: https://doi.org/10.18103/mra.v10i4.2762.
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The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
1. A, Cavenee W, Neve R L, Orkin S H, Bruns G A. Homozygous deletion in Wilms tumours of a zinc-finger gene identified by chromosome jumping. Nature. 1990; 343: 774-778.
2. Call K M, Glaser T, Ito C Y, Buckler A J, Pelletier J, Haber D A, Rose E A, Kral A, Yeger H, Lewis W H, Jones C, Housman D E. Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell. 1990; 60: 509-520.
3. Sugiyama H. WT1 (Wilms' tumor gene 1): biology and cancer immunotherapy. Jpn J Clin Oncol. 2010; 40: 377-387.
4. Hastie ND. Wilms' tumour 1 (WT1) in development, homeostasis and disease. Development. 2017; 144: 2862-2872.
5. Wagner KD, Cherfils-Vicini J, Hosen N, Hohenstein P, Gilson E, Hastie ND, Michiels JF, Wagner N. The Wilms' tumour suppressor Wt1 is a major regulator of tumour angiogenesis and progression. Nat Commun. 2014; 5: 5852.
6. Wagner K D, Maï M E, Ladomery M, Belali T, Leccia N, Michiels J F, Wagner N. Altered VEGF Splicing Isoform Balance in Tumor Endothelium Involves Activation of Splicing Factors Srpk1 and Srsf1 by the Wilms' Tumor Suppressor Wt1. Cells. 2019; 8: 41.
7. Miwa H, Beran M, Saunders GF. Expression of the Wilms' tumor gene (WT1) in human leukemias. Leukemia. 1992; 6: 405-409.
8. Inoue K, Sugiyama H, Ogawa H, Nakagawa M, Yamagami T, Miwa H, Kita K, Hiraoka A, Masaoka T, Nasu K, Kyo T, Dohy H, Nakauchi H, Ishidate T, Akiyama T, Kishimoto T. WT1 as a new prognostic factor and a new marker for the detection of minimal residual disease in acute leukemia. Blood. 1994; 84: 3071-3079.
9. Yamagami T, Sugiyama H, Inoue K, Ogawa H, Tatekawa T, Hirata M, Kudoh T, Akiyama T, Murakami A, Maekawa T, Kishimoto T. Growth inhibition of human leukemic cells by WT1 (Wilms tumor gene) antisense oligodeoxynucleotides: Implications for the involvement of WT1 in leukemogenesis. Blood. 1996; 87: 2878-2884.
10. Algar E M, Khromykh T, Smith S I, Blackburn D M, Bryson G J, Smith P J. A WT1 antisense oligonucleotide inhibits proliferation and induces apoptosis in myeloid leukaemia cell lines. Oncogene. 1996; 12: 1005-1014.
11. Oji Y, Ogawa H, Tamaki H, Oka Y, Tsuboi A, Kim EH, Soma T, Tatekawa T, Kawakami M, Asada M, Kishimoto T, Sugiyama H. Expression of the Wilms' tumor gene WT1 in solid tumors and its involvement in tumor cell growth. Jpn J Cancer Res. 1999; 90: 194-204.
12. Nakatsuka S, Oji Y, Horiuchi T, Kanda T, Kitagawa M, Takeuchi T, Kawano K, Kuwae Y, Yamauchi A, Okumura M, Kitamura Y, Oka Y, Kawase I, Sugiyama H, Aozasa K. Immunohistochemical detection of WT1 protein in a variety of cancer cells. Mod Pathol. 2006; 19: 804-814.
13. Qi XW, Zhang F, Wu H, Liu JL, Zong BG, Xu C, Jiang J. Wilms' tumor 1 (WT1) expression and prognosis in solid cancer patients: a systematic review and meta-analysis. Sci Rep. 2015; 5:8924.
14. Inoue K, Ogawa H, Yamagami T, Soma T, Tani Y, Tatekawa T, Oji Y, Tamaki H, Kyo T, Dohy H, Hiraoka A, Masaoka T, Kishimoto T, Sugiyama H. Long-term follow-up of minimal residual disease in leukemia patients by monitoring WT1 (Wilms tumor gene) expression levels. Blood. 1996; 88: 2267-2278.
15. Cilloni D, Saglio G.WT1 as a universal marker for minimal residual disease detection and quantification in myeloid leukemias and in myelodysplastic syndrome. Acta Haematol. 2004; 112: 79-84.
16. Cilloni D, Gottardi E, De Micheli D, Serra A, Volpe G, Messa F, Rege-Cambrin G, Guerrasio A, Divona M, Lo Coco F, Saglio G. Quantitative assessment of WT1 expression by real time quantitative PCR may be a useful tool for monitoring minimal residual disease in acute leukemia patients. Leukemia. 2002; 16(10): 2115-2121.
17. Hashii Y, Kosaka Y, Watanabe K, Kato K, Imaizumi M, Kaneko T, Sunami S, Watanabe A, Hiramatsu H, Koga Y, Hirayama M, Nakao T, Hata T, Uchida N, Ishiyama K, Mitani K, Hidaka M, Kitamura K, Tsunemine H, Ueda Y, Mugitani A, Usuki K, Kanda Y, Miyazaki Y, Imai K, Naoe T, Koh K, Sugiyama H, Horibe K. Clinical Significance of WT1 mRNA Levels in Japanese Acute Lymphoblastic Leukemia Patients. J Leuk. 2017; 5: 243. Doi: 10.4172/2329-6917.1000243
18. Tamaki H, Ogawa H, Ohyashiki K, Oyhashiki JH, Iwama H, Inoue K, Soma T, Oka Y, Tatekawa T, Oji Y, Tsuboi A, Kim EH, Kawakami M, Fuchigami K, Tomonaga M, Toyama K, Aozasa K, Kishimoto T, Sugiyama H. The Wilms' tumor gene WT1 is a good marker for diagnosis of disease progression of myelodysplastic syndromes. Leukemia. 1999; 13: 393-399.
19. Cilloni D, Gottardi E, Messa F, Fava M, Scaravaglio P, Bertini M, Girotto M, Marinone C, Ferrero D, Gallamini A, Levis A, Saglio G; Piedmont Study Group on Myleodysplastic Syndromes. Significant correlation between the degree of WT1 expression and the International Prognostic Scoring System Score in patients with myelodysplastic syndromes. J Clin Oncol. 2003; 21: 1988-1995.
20. Ueda Y, Mizutani C, Nannya Y, Kurokawa M, Kobayashi S, Takeuchi J, Tamura H, Ogata K, Dan K, Shibayama H, Kanakura Y, Niimi K, Sasaki K, Watanabe M, Emi N, Teramura M, Motoji T, Kida M, Usuki K, Takada S, Sakura T, Ito Y, Ohyashiki K, Ogawa H, Suzuki T, Ozawa K, Imai K, Kasai M, Hata T, Miyazaki Y, Morita Y, Kanamaru A, Matsuda A, Tohyama K, Koga D, Tamaki H, Mitani K, Naoe T, Sugiyama H, Takaku F. Clinical evaluation of WT1 mRNA expression levels in peripheral blood and bone marrow in patients with myelodysplastic syndromes. Leuk Lymphoma. 2013; 54: 1450-1458.
21. Oka Y, Udaka K, Tsuboi A, Elisseeva OA, Ogawa H, Aozasa K, Kishimoto T, Sugiyama H. Cancer Immunotherapy targeting Wilms’ tumor gene WT1 product. J Immunol. 2000; 164: 1873-1880.
22. Gaiger A, Reese V, Disis M L, Cheever M A. Immunity to WT1 in the animal model and in patients with acute myeloid leukemia. Blood. 2000; 96: 1480-1489.
23. Oka Y, Elisseeva OA, Tsuboi A, Ogawa H, Tamaki H, Li H, Oji Y, Kim EH, Soma T, Asada M, Ueda K, Sugiyama H. Human cytotoxic T lymphocyte responses specific for peptides of wild-type Wilms’ tumor gene WT1 product. Immunogenetics. 2000; 51: 99-107
24. Gao L, Bellantuono I, Elsässer A, Marley SB, Gordon MY, Goldman JM, Stauss HJ. Selective elimination of leukemic CD34(+) progenitor cells by cytotoxic T lymphocytes specific for WT1. Blood. 2000; 95: 2198-2203.
25. Ohminami H, Yasukawa M, Fujita S. HLA class I-restricted lysis of leukemia cells by a CD8(+) cytotoxic T-lymphocyte clone specific for WT1 peptide. Blood. 2000; 95: 286-293.
26. Cheever MA, Allison JP, Ferris AS, Finn OJ, Hastings BM, Hecht TT, Mellman I, Prindiville SA, Viner JL, Weiner LM, Matrisian LM. The Prioritization of Cancer Antigens: A National Cancer Institute Pilot Project for the Acceleration of Translational Research. Clin Cancer Res. 2009; 15: 5323-5337.
27. Fujiki F, Oka Y, Tsuboi A, Kawakami M, Kawakatsu M, Nakajima H, Elisseeva OA, Harada Y, Ito K, Li Z, Tatsumi N, Sakaguchi N, Fujioka T, Masuda T, Yasukawa M, Udaka K, Kawase I, Oji Y, Sugiyama H. Identification and characterization of a WT1 (Wilms Tumor Gene) protein-derived HLA-DRB1*0405-restricted 16-mer helper peptide that promotes the induction and activation of WT1-specific cytotoxic T lymphocytes. J Immunother. 2007; 30: 282-93.
28. Nakajima H, Nakata J, Imafuku K, Hayashibara H, Isokawa K, Udaka K, Fujiki F, Morimoto S, Hasegawa K, Hosen N, Hashii Y, Nishida S, Tsuboi A, Oka Y, Oji Y, Sogo S, Sugiyama H. Identification of mouse helper epitopes for WT1-specific CD4+ T cells. Cancer Immunol Immunother. 2021; 70: 3323-3335.
29. Oka, Y, Tsuboi A, Murakami M, Hirai M, Tominaga N, Nakajima H, Masuda T, Nakano A, Kawakami M, Oji Y, Ikegame K, Hosen N, Udaka K, Yasukawa M, Ogawa H, Kawase I, Sugiyama H. WT1 peptide-based immunotherapy for patients with overt leukemia from myelodysplastic syndome (MDS) or MDS with myelofibrosis. Int J Hematol. 2003; 78: 56-61.
30. Oka Y, Tsuboi A, Taguchi T, Osaki T, Kyo T, Nakajima, Elisseeva OA, Oji Y, Kawakami M, Ikegame K, Hosen, N, Yoshihara S, Wu F, Fujiki F, Murakami M, Masuda T, Nishida S, Shirakata T, Nakatsuka S, Sasaki A, Udaka K, Dohy H, Aozasa K, Noguchi S, Kawase I, Sugiyama H. Induction of WT1 (Wilms’ tumor gene)-specific cytotoxic T lymphocytes by WT1 peptide vaccine and the resultant cancer regression. Proc Natl Acad Sci U S A. 2004; 101:13885-13890.
31. Rezvani K, Yong A S, Mielke S, Savani B N, Musse L, Superata J, Jafarpour B, Boss C, Barrett A J. Leukemia-associated antigen-specific T-cell responses following combined PR1 and WT1 peptide vaccination in patients with myeloid malignancies. Blood, 2008; 111: 236-42.
32. Keilholz U, Letsch A, Busse A, Asemissen AM, Bauer S, Blau IW, Hofmann WK, Uharek L, Thiel E, Scheibenbogen C. A clinical and immunologic phase 2 trial of Wilms tumor gene product 1 (WT1) peptide vaccination in patients with AML and MDS. Blood. 2009; 113: 6541-8.
33. Yasukawa M, Fujiwara H, Ochi T, Suemori K, Narumi H, Azuma T, Kuzushima K. Clinical efficacy of WT1 peptide vaccination in patients with acute myelogenous leukemia and myelodysplastic syndrome. Am J Hematol. 2009; 84: 314-315.
34. Maslak PG, Dao T, Krug LM, Chanel S, Korontsvit T, Zakhaleva V, Zhang R, Wolchok JD, Yuan J, Pinilla-Ibarz J, Berman E, Weiss M, Jurcic J, Frattini MG, Scheinberg DA. Vaccination with synthetic analog peptides derived from WT1 oncoprotein induces T-cell responses in patients with complete remission from acute myeloid leukemia. Blood. 2010; 116: 171-179.
35. Koido S, Okamoto M, Kobayashi M, Shimodaira S, Sugiyama H. Significance of Wilms' tumor 1 antigen as a cancer vaccine for pancreatic cancer. Discov Med. 2017; 24: 41-49.
36. Koya T, Date I, Kawaguchi H, Watanabe A, Sakamoto T, Togi M, Kato T Jr, Yoshida K, Kojima S, Yanagisawa R, Koido S, Sugiyama H, Shimodaira S. Dendritic Cells Pre-Pulsed with Wilms' Tumor 1 in Optimized Culture for Cancer Vaccination. Pharmaceutics. 2020; 12: 305.
37. Van Driessche A, Van de Velde AL, Nijs G, Braeckman T, Stein B, De Vries JM, Berneman ZN, Van Tendeloo VF. Clinical-grade manufacturing of autologous mature mRNA-electroporated dendritic cells and safety testing in acute myeloid leukemia patients in a phase I dose-escalation clinical trial. Cytotherapy. 2009; 11:653-668.
38. Dagvadorj N, Deuretzbacher A, Weisenberger D, Baumeister E, Trebing J, Lang I, Köchel C, Kapp M, Kapp K, Beilhack A, Hünig T, Einsele H, Wajant H, Grigoleit GU. Targeting of the WT1 91-138 fragment to human dendritic cells improves leukemia-specific T-cell responses providing an alternative approach to WT1-based vaccination. Cancer Immunol Immunother. 2017; 66: 319-332.
39. Tsuboi A, Oka Y, Udaka K, Murakami M, Masuda T, Nakano A, Nakajima H, Yasukawa M, Hiraki A, Oji Y, Kawakami M, Hosen N, Fujioka T, Wu F, Taniguchi Y, Nishida S, Asada M, Ogawa H, Kawase I, Sugiyama H. Enhanced induction of human WT1-specific cytotoxic T lymphocytes with a 9-mer WT1 peptide modified at HLA-A*2402-binding residues. Cancer Immunol Immunother. 2002; 51: 614-620.
40. Tsuboi A, Oka Y, Kyo T, Katayama Y, Elisseeva OA, Kawakami M, Nishida S, Morimoto S, Murao A, Nakajima H, Hosen N, Oji Y, Sugiyama H. Long-term WT1 peptide vaccination for patients with acute myeloid leukemia with minimal residual disease. Leukemia. 2012; 26: 1410-1413.
41. Mailänder V, Scheibenbogen C, Thiel E, Letsch A, Blau IW, Keilholz U. Complete remission in a patient with recurrent acute myeloid leukemia induced by vaccination with WT1 peptide in the absence of hematological or renal toxicity. Leukemia. 2004; 18: 165-166.
42. Ochsenreither S, Fusi A, Geikowski A, Stather D, Busse A, Stroux A, Letsch A, Keilholz U. Wilms' tumor protein 1 (WT1) peptide vaccination in AML patients: predominant TCR CDR3β sequence associated with remission in one patient is detectable in other vaccinated patients. Cancer Immunol Immunother. 2012; 61: 313-322.
43. Uttenthal B, Martinez-Davila I, Ivey A, Craddock C, Chen F, Virchis A, Kottaridis P, Grimwade D, Khwaja A, Stauss H, Morris EC. Wilms' Tumour 1 (WT1) peptide vaccination in patients with acute myeloid leukaemia induces short-lived WT1-specific immune responses. Br J Haematol. 2014; 164: 366-375.
44. Brayer J, Lancet JE, Powers J, List A, Balducci L, Komrokji R, Pinilla-Ibarz J. WT1 vaccination in AML and MDS: A pilot trial with synthetic analog peptides. Am J Hematol. 2015; 90: 602-607.
45. Shah NN, Loeb DM, Khuu H, Stroncek D, Ariyo T, Raffeld M, Delbrook C, Mackall CL, Wayne AS, Fry TJ. Induction of Immune Response after Allogeneic Wilms' Tumor 1 Dendritic Cell Vaccination and Donor Lymphocyte Infusion in Patients with Hematologic Malignancies and Post-Transplantation Relapse. Biol Blood Marrow Transplant. 2016; 22: 2149-2154.
46. Nakata J, Nakae Y, Kawakami M, Morimoto S, Motooka D, Hosen N, Fujiki F, Nakajima H, Hasegawa K, Nishida S, Tsuboi A, Oji Y, Oka Y, Kumanogoh A, Sugiyama H. Wilms tumour 1 peptide vaccine as a cure-oriented post-chemotherapy strategy for patients with acute myeloid leukaemia at high risk of relapse. Br J Haematol. 2018; 182: 287-290.
47. Nakata J, Oji Y, Oka Y, Sugiyama H. What should we tackle next in acute myeloid leukemia? Wilms tumor gene 1 vaccine therapy would be a promising and versatile strategy for acute myeloid leukemia. Expert Rev Hematol. 2019; 12: 211-213.
48. Maslak PG, Dao T, Scheinberg DA, Bernal Y, Chanel SM, Zhang R, Frattini M, Rosenblat T, Jurcic JG, Brentjens RJ, Arcila ME, Rampal R, Park JH, Douer D, Katz L, Sarlis N, Tallman M, Scheinberg DA. Phase 2 trial of a multivalent WT1 peptide vaccine (galinpepimut-S) in acute myeloid leukemia. Blood Adv. 2018; 2(3): 224.
49. Anguille S, Van de Velde AL, Smits EL, Van Tendeloo VF, Juliusson G, Cools N, Nijs G, Stein B, Lion E, Van Driessche A, Vandenbosch I, Verlinden A, Gadisseur AP, Schroyens WA, Muylle L, Vermeulen K, Maes MB, Deiteren K, Malfait R, Gostick E, Lammens M, Couttenye MM, Jorens P, Goossens H, Price DA, Ladell K, Oka Y, Fujiki F, Oji Y, Sugiyama H, Berneman ZN. Dendritic cell vaccination as postremission treatment to prevent or delay relapse in acute myeloid leukemia. Blood. 2017; 130: 1713-1721.
50. Van Tendeloo VF, Van de Velde A, Van Driessche A, Cools N, Anguille S, Ladell K, Gostick E, Vermeulen K, Pieters K, Nijs G, Stein B, Smits EL, Schroyens WA, Gadisseur AP, Vrelust I, Jorens PG, Goossens H, de Vries IJ, Price DA, Oji Y, Oka Y, Sugiyama H, Berneman ZN. Induction of complete and molecular remissions in acute myeloid leukemia by Wilms' tumor 1 antigen-targeted dendritic cell vaccination. Proc Natl Acad Sci U S A. 2010; 107: 13824-13829.
51. Kobayashi Y, Sakura T, Miyawaki S, Toga K, Sogo S, Heike Y. A new peptide vaccine OCV-501: in vitro pharmacology and phase 1 study in patients with acute myeloid leukemia. Cancer Immunol Immunother. 2017; 66: 851-863.
52. Kiguchi T, Yamaguchi M, Takezako N, Miyawaki S, Masui K, Ihara Y, Hirota M, Shimofurutani N, Naoe T. Cancer Immunol Immunother. Efficacy and safety of Wilms' tumor 1 helper peptide OCV-501 in elderly patients with acute myeloid leukemia: a multicenter, randomized, double-blind, placebo-controlled phase 2 trial. Cancer Immunol Immunother. https://doi.org/10.1007/s00262-021-03074-4.
53. Oji Y, Oka Y, Nishida S, Tsuboi A, Kawakami M, Shirakata T, Takahashi K, Murao A, Nakajima H, Narita M, Takahashi M, Morita S, Sakamoto J, Tanaka T, Kawase I, Hosen N, Sugiyama H. WT1 peptide vaccine induces reduction in minimal residual disease in an Imatinib-treated CML patient. Eur J Haematol. 2010; 85: 358-360.
54. Narita M, Masuko M, Kurasaki T, Kitajima T, Takenouchi S, Saitoh A, Watanabe N, Furukawa T, Toba K, Fuse I, Aizawa Y, Kawakami M, Oka Y, Sugiyama H, Takahashi M. WT1 peptide vaccination in combination with imatinib therapy for a patient with CML in the chronic phase. Int J Med Sci. 2010; 7: 72-81.
55. Saitoh A, Narita M, Watanabe N, Tochiki N, Yamahira A, Nakamura T, Kaji M, Masuko M, Furukawa T, Toba K, Fuse I, Aizawa Y, Takahashi M. WT1 peptide vaccination in a CML patient: induction of effective cytotoxic T lymphocytes and significance of peptide administration interval. Med Oncol. 2011; 28: 219-230.
56. Hughes A, Clarson J, Tang C, Vidovic L, White DL, Hughes TP, Yong AS.CML patients with deep molecular responses to TKI have restored immune effectors and decreased PD-1 and immune suppressors. Blood. 2017; 129: 1166-1176.
57. Dong WZ, Dan L, jun HX. Graft-versus-leukemia effects of Wilms’ tumor 1 protein-specific cytotoxic T lymphocytes in patients with chronic myeloid leukemia after allogeneic hematopoietic stem cell transplantation. Chin Med J. 2010; 123: 912-916.
58. Ueda Y, Ogura M, Miyakoshi S, Suzuki T, Heike Y, Tagashira S, Tsuchiya S, Ohyashiki K, Miyazaki Y. Phase 1/2 study of the WT1 peptide cancer vaccine WT4869 in patients with myelodysplastic syndrome. Cancer Sci. 2017; 108: 2445-2453.
59. Miyakoshi S, Usuki K, Matsumura I, Ueda Y, Iwasaki H, Miyamoto T, Origuchi M, Tagashira S, Ichiro Naoi, Naoe T, Kizaki M, Heike Y, Akashi K, Miyazaki Y. Preliminary results from a phase 1/2 study of DSP-7888, a novel WT1 peptide-based vaccine, in patients with myelodysplastic syndrome (MDS). Blood. 2016; 128: 4335.
60. Usuki K, Ueda Y, Fujita J, Matsumura I, Aotsuka N, Sekiguchi N, Nakazato T, Iwasaki H, Watanabe A, Sugimoto S, Yamakawa EK, Naoe T, Kizaki M, Heike Y, Miyazaki Y, Akashi K. Phase 1/2 study of DSP-7888 in patients with higher-risk (HR) myelodysplastic syndromes (MDS) after failure of azacitidine (AZA) therapy. https://library.ehaweb.org/eha/2019/24th/266961/kensuke.usuki.phase.1.2.study.of.dsp-7888.in.patients.with.higher-risk.%28hr%29.html.
61. Spira A, Hansen AR, Harb WA, Curtis KK, Koga-Yamakawa E, Origuchi M, Li Z, Ertik B, Shaib WL. Multicenter, Open-Label, Phase I Study of DSP-7888 Dosing Emulsion in Patients with Advanced Malignancies. Target Oncol. 2021; 16: 461-469.
62. Ogasawara M, Miyashita M, Yamagishi Y, Ota S. Wilms’ tumor 1 peptide-loaded dendritic cell vaccination in patients with relapsed or refractory malignant lymphoma. Leuk Lymph. http://doi.org/10.1080/10428194.2022.2038371.
63. Israyelyan A, La Rosa C, Tsai W, Kaltcheva T, Srivastava T, Aquino L, Li J, Kim Y, Palmer J, Streja L, Senitzer D, Zaia JA, Rosenwald A, Forman SJ, Nakamura R, Diamond DJ. Detection and preliminary characterization of CD8+T lymphocytes specific for Wilms' tumor antigen in patients with non-Hodgkin lymphoma. Leuk Lymph. 2013; 54: 2490-2499.
64. Tsuboi A, Oka Y, Nakajima H, Fukuda Y, Elisseeva O. A, Yoshihara S, Hosen N, Ogata A, Kito K, Fujiki F, Nishida S Shirakata T Ohno S, Yasukawa M, Oji Y, Kawakami M, Morita S, Sakamoto J, Udaka K, Kawase I, Sugiyama H. Wilms’ tumor gene WT1 peptide-based immunotherapy induced minimal response in a patient with advanced, therapy-resistant multiple myeloma. Int J Hematol. 2007; 86: 414-417.
65. Tyler EM, Jungbluth AA, O'Reilly RJ, Koehne G. WT1-specific T-cell responses in high-risk multiple myeloma patients undergoing allogeneic T cell-depleted hematopoietic stem cell transplantation and donor lymphocyte infusions. Blood. 2013; 121: 308-317.
66. Izumoto S, Tsuboi A, Oka Y, Suzuki T, Hashiba T, Kagawa N, Hashimoto N, Maruno M, Elisseeva, OA, Shirakata T, Kawakami M, Oji Y, Nishida S, Ohno S, Kawase I, Hatazawa J, Morita S, Sakamoto J, Sugiyama H, Yoshimine T. Phase II clinical trial of Wilms tumor 1 peptide vaccination for patients with recurrent glioblastoma multiforme. J Neurosurg. 2008; 108: 963-971.
67. Hashimoto N, Tsuboi A, Kagawa N, Chiba Y, Izumoto S, Kinoshita M, Kijima N, Oka Y, Morimoto S, Nakajima H, Morita S, Sakamoto J, Nishida S, Hosen N, Oji Y, Arita N, Yoshimine T, Sugiyama H. Wilms tumor 1 peptide vaccination combined with temozolomide against newly diagnosed glioblastoma: safety and impact on immunological response. Cancer Immunol Immunother. 2015; 64: 707-716.
68. Tsuboi A, Hashimoto N, Fujiki F, Morimoto S, Kagawa N, Nakajima H, Hosen N, Nishida S, Nakata J, Morita S, Sakamoto J, Oji Y, Oka Y, Sugiyama H. A phase I clinical study of a cocktail vaccine of Wilms' tumor 1 (WT1) HLA class I and II peptides for recurrent malignant glioma. Cancer Immunol Immunother. 2019; 68: 331-340.
69. Chiba Y, Hashimoto N, Tsuboi A, Rabo C, Oka Y, Kinoshita M, Kagawa N, Oji Y, Sugiyama H, Yoshimine T. Prognostic value of WT1 protein expression level and MIB-1 staining index as predictor of response to WT1 immunotherapy in glioblastoma patients. Brain Tumor Pathol. 2010; 27: 29-34.
70. Sakai K, Shimodaira S, Maejima S, Udagawa N, Sano K, Higuchi Y, Koya T, Ochiai T, Koide M, Uehara S, Nakamura M, Sugiyama H, Yonemitsu Y, Okamoto M, Hongo K. Dendritic cell-based immunotherapy targeting Wilms' tumor 1 in patients with recurrent malignant glioma. J Neurosurg. 2015; 123: 989-997.
71. Sakai K, Shimodaira S, Maejima S, Sano K, Higuchi Y, Koya T, Sugiyama H, Hongo K. Clinical effect and immunological response in patients with advanced malignant glioma treated with WT1-pulsed dendritic cell-based immunotherapy: A report of two cases. Interdisciplinary Neurosurg.2017; 9:24-29.
72. Hashii Y, Oka Y, Kagawa N, Hashimoto N, Saitou H, Fukuya S, Kanegae M, Ikejima S, Oji Y, OzonoK, Tsuboi A, Sugiyama H. Encouraging clinical evolution of a pediatric patient with relapsed diffuse midline glioma who underwent WT1-targeting immunotherapy: A case report and literature review. Front Oncol. 2020; 10: 1188.
73. Yokota C, Takano K, Chiba Y, Kagawa N, Tsuboi A, Oka Y, Oji Y, Kinoshita M, Kijima N, Kishima H, Izumoto S, Sugiyama H, Hashimoto N. Maintenance of WT1 expression in tumor cells is associated with good prognosis in malignant glioma patients treated with WT1 peptide vaccine immunotherapy. Cancer Immunol Immunother. 2022; 71: 189-201.
74. Fu S, Piccioni DE, Liu H, Lukas RV, Kesari S, Aregawi D, Hong DS, Yamaguchi K, Whicher K, Zhang Y, Chen YL, Poola N, Eddy J, Blum D. A phase I study of the WT2725 dosing emulsion in patients with advanced malignancies. Sci Rep. 2021; 11: 22355.
75. Fujisaki H, Hashii Y, Terashima K, Goto H, Horibe K, Sugiyama K, Watanabe A, Sugimoto S, Yanagisawa T, Kikuta A, Kawamoto H, Hashimoto N, Hara J. Phase 1/2 study of DSP-7888 in pediatric patients with malignant glioma. 23rd Annual Scientific Meeting and Education Day of the Society for Neuro-oncology, New Orleans, 2018. Neuro Oncol. 2018; 20 (Suppl 6): vi202.
76. Ogasawara M, Miyashita M, Yamagishi Y, Ota S. Phase I/II Pilot Study of Wilms' Tumor 1 Peptide-Pulsed Dendritic Cell Vaccination Combined With Conventional Chemotherapy in Patients With Head and Neck Cancer. Ther Apher Dial. 2019; 23: 279-288.
77. Tsuboi A, Oka Y, Osaka T, Kumagai T, Tachibana I, Hayashi S, Murakami M, Nakajima H, Elisseeva OA, Wu F, Masuda T, Yasukawa M, Oji Y, Kawakami M, Hosen N, Ikegame K, Yoshihara S, Udaka K, Nakatsuka S, Aozasa K. Kawase I, Sugiyama H. WT1 peptide-based immunotherapy for patients with lung cancer. Microbiol Immunol. 2004; 48: 175-184.
78. Krug LM, Dao T, Brown AB, Maslak P, Travis W, Bekele S, Korontsvit T, Zakhaleva V, Wolchok J, Yuan J, Li H, Tyson L, Scheinberg DA. WT1 peptide vaccinations induce CD4 and CD8 T cell immune responses in patients with mesothelioma and non-small cell lung cancer. Cancer Immunol Immunother. 2010; 59: 1467-1479.
79. Takahashi H, Okamoto M, Shimodaira S, Tsujitani S, Nagaya M, Ishidao T, Kishimoto J, Yonemitsu Y; DC-vaccine study group at the Japan Society of Innovative Cell Therapy (J-SICT). Impact of dendritic cell vaccines pulsed with Wilms' tumour-1 peptide antigen on the survival of patients with advanced non-small cell lung cancers. Eur J Cancer. 2013; 49: 852-859.
80. May RJ, Dao T, Pinilla-Ibarz J, Korontsvit T, Zakhaleva V, Zhang RH, Maslak P, Scheinberg DA. Peptide epitopes from the Wilms' tumor 1 oncoprotein stimulate CD4+ and CD8+ T cells that recognize and kill human malignant mesothelioma tumor cells. Clin Cancer Res. 2007; 13: 4547-4555.
81. Zauderer MG, Tsao AS, Dao T, Panageas K, Lai WV, Rimner A, Rusch VW, Adusumilli PS, Ginsberg MS, Gomez D, Rice D, Mehran R, Scheinberg DA, Krug LM. A Randomized phase II trial of adjuvant galinpepimut-S, WT-1 analogue peptide vaccine, after multimodality therapy for patients with malignant pleural mesothelioma. Clin Cancer Res. 2017; 23: 7483.
82. Oji Y, Inoue M, Takeda Y, Hosen N, Shintani Y, Kawakami M, Harada T, Murakami Y, Iwai M, Fukuda M, Nishida S, Nakata J, Nakae Y, Takashima S, Shirakata T, Nakajima H, Hasegawa K, Kida H, Kijima T, Morimoto S, Fujiki F, Tsuboi A, Morii E, Morita S, Sakamoto J, Kumanogoh A, Oka Y, Okumura M, Sugiyama H. WT1 peptide-based immunotherapy for advanced thymic epithelial malignancies. Int J Cancer. 2018; 142: 2375-2382.
83. Takahashi N, Zhao C, Rajan A. WT1 as an immunotherapy target for thymic epithelial tumors: a novel method to activate anti-tumor immunity. Mediastinum. 2019; 3: 11.
84. Higgins M, Curigliano G, Dieras V, Kuemmel S, Kunz G, Fasching PA, Campone M, Bachelot T, Krivorotko P, Chan S, Ferro A, Schwartzberg L, Gillet M, De Sousa Alves PM, Wascotte V, Lehmann FF, Goss P. Safety and immunogenicity of neoadjuvant treatment using WT1-immunotherapeutic in combination with standard therapy in patients with WT1-positive Stage II/III breast cancer: a randomized Phase I study. Breast Cancer Res Treat. 2017; 162: 479-488.
85. Gillmore R, Xue SA, Holler A, Kaeda J, Hadjiminas D, Healy V, Dina R, Parry SC, Bellantuono I, Ghani Y, Coombes RC, Waxman J, Stauss HJ. Detection of Wilms' tumor antigen--specific CTL in tumor-draining lymph nodes of patients with early breast cancer. Clin Cancer Res. 2006; 12: 34-42.
86. Sasabe E, Hamada F, Iiyama T, Udaka K, Sugiyama H, Yamamoto T. Wilm's tumor gene WT1 peptide immunotherapy for pulmonary metastasis from adenoid cystic carcinoma of the salivary gland. Oral Oncology. 2011; 47: 77-78.
87. Shirakata T, Oka Y, Nishida S, Hosen N, Tsuboi A, Oji Y, Murao A, Tanaka H, Nakatsuka S, Inohara H, Sugiyama H. WT1 Peptide Therapy for a Patient with Chemotherapy-resistant Salivary Gland Cancer. Anticancer Res. 2012; 32: 1081-1086.
88. Matsuda T, Takeuchi H, Sakurai T, Mayanagi S, Booka E, Fujita T, Higuchi H, Taguchi J, Hamamoto Y, Takaishi H, Kawakubo H, Okamoto M, Sunamura M, Kawakami Y, Kitagawa Y. Pilot study of WT1 peptide-pulsed dendritic cell vaccination with docetaxel in esophageal cancer. Oncol Lett. 2018; 16: 1348-1356.
89. Ogasawara M, Miyashita M, Yamagishi Y, Ota S. Immunotherapy employing dendritic cell vaccination for patients with advanced or relapsed esophageal cancer. Ther Apher Dial. 2020; 24: 482-491.
90. Kobayashi M, Sakabe T, Chiba A, Nakajima A, Okamoto M, Shimodaira A, Yonemitsu Y, Shibamoto Y, Suzuki N, Nagaya M. Therapeutic effect of intratumoral injections of dendritic cells for locally recurrent gastric cancer: a case report. World J Surg Oncol. 2014; 12: 390.
91. Lu X, Liu J, Cui P, Liu T, Piao C, Xu X, Zhang Q, Xiao M, Liu X, Wang Y, Yang L. Am J Cancer Res. Co-inhibition of TIGIT, PD1, and Tim3 reverses dysfunction of Wilms tumor protein-1 (WT1)-specific CD8+ T lymphocytes after dendritic cell vaccination in gastric cancer. Am J Cancer Res. 2018; 8: 1564-1575.
92. Kaida M, Morita-Hoshi Y, Soeda A, Wakeda T, Yamaki Y, Kojima Y, Ueno H, Kondo S, Morizane C, Ikeda M, Okusaka T, Takaue Y, Heike Y. Phase 1 trial of Wilms tumor 1 (WT1) peptide vaccine and gemcitabine combination therapy in patients with advanced pancreatic or biliary tract cancer. J Immunother. 2011; 34: 92-99.
93. Nishida S, Koido S, Takeda Y,Honma S, Kimita H, Takahara A, Morita S, Ito T, Morimoto S, Hara K, Tsuboi A, Oka Y, Yanagisawa S, Toyama Y, Ikegami M, Kitagawa T, Eguchi H, Wada H, Nagano H, Nakata J, Nakae Y, Hosen N, Oji Y, Tanaka T, Kawase I, Kumanogoh A, Sakamoto J, Doki Y, Mori M,Ohkusa T, Tajiri H, Sugiyama H. Wilms Tumor Gene 1 (WT1) Peptide–based Cancer Vaccine Combined With Gemcitabine for Patients With Advanced Pancreatic Cancer. J Immunother. 2014; 37: 105-114.
94. Nishida S, Ishikawa T, Sugiyama H, et al. Combination gemcitabine and WT1 peptide vaccination improves progression-free survival in advanced pancreatic ductal adenocarcinoma: A phase II randomized study. Cancer Immunol Res. 2018; 6: 320.
95. Kimura Y, Tsukada J, Tomoda T, Takahashi H, Imai K, Shimamura K, Sunamura M, Yonemitsu Y, Shimodaira S, Koido S, Homma S, Okamoto M. Clinical and immunologic evaluation of dendritic cell-based immunotherapy in combination with gemcitabine and/or S-1 in patients with advanced pancreatic carcinoma. Pancreas. 2012; 41: 195-205.
96. Mayanagi S, Kitago M, Sakurai T, Matsuda T, Fujita T, Higuchi H, Taguchi J, Takeuchi H, Itano O, Aiura K, Hamamoto Y, Takaishi H, Okamoto M, Sunamura M, Kawakami Y, Kitagawa Y. Phase I pilot study of Wilms tumor gene 1 peptide-pulsed dendritic cell vaccination combined with gemcitabine in pancreatic cancer. Cancer Sci. 2015; 106: 397-406.
97. Hanada S, Tsuruta T, Hiraguchi K, Okamoto M, Sugiyama H, Koido S. Long-term survival of pancreatic cancer patients treated with multimodal therapy combined with WT1-targeted dendritic cell vaccines. Hum Vaccin Immunother. 2019; 15: 397-406.
98. Nagai K, Adachi T, Harada H, Eguchi S, Sugiyama H, Miyazaki Y. Dendritic cell-based immunotherapy pulsed with Wilms Tumor 1 peptide and MUC-1 as an adjuvant therapy for pancreatic ductal adenocarcinoma after curative resection: a PhaseⅠ/Ⅱa clinical trial. Anticancer Res. 2020; 40: 5765-5776.
99. Ota S, Miyashita M, Yamagishi Y, Ogasawara M. Baseline immunity predicts prognosis of pancreatic cancer patients treated with WT1 and/or MUC1 peptide-loaded dendritic cell vaccination and a standard chemotherapy. Hum Vaccin Immunother. 2021; 17: 1-10.
100. Koido S, Homma S, Okamoto M, Takakura K, Mori M, Yoshizaki S, Tsukinaga S, Odahara S, Koyama S, Imazu H, Uchiyama K, Kajihara M, Arakawa H, Misawa T, Toyama Y, Yanagisawa S, Ikegami M, Kan S, Hayashi K, Komita H, Kamata Y, Ito M, Ishidao T, Yusa SI, Shimodaira S, Gong J, Sugiyama H, Ohkusa T, Tajiri H. Treatment with Chemotherapy and Dendritic Cells Pulsed with Multiple Wilms' Tumor 1 (WT1)-Specific MHC Class I/II-Restricted Epitopes for Pancreatic Cancer. Clin Cancer Res. 2014; 20: 4228-4239.
101. Koido S, Okamoto M, Shimodaira S, Sugiyama H. Wilms' tumor 1 (WT1)-targeted cancer vaccines to extend survival for patients with pancreatic cancer. Immunotherapy. 2016; 8: 1309-1320.
102. Yanagisawa R, Koizumi T, Koya T, Sano K, Koido S, Nagai K, Kobayashi M, Okamoto M, Sugiyama H, Shimodaira S. WT1-pulsed Dendritic Cell Vaccine Combined wirh Chemotherapy for Resected Pancreatic Cancer in a Phase Ⅰ Study. Anticance Res. 2018; 38: 2217-2225.
103. Katsuda M, Miyazawa M, Ojima T, Katanuma A, Hakamada K, Sudo K, Asahara S, Endo I, Ueno M, Hara K, Yamada S, Fujii T, Satoi S, Ioka T, Ohira M, Akahori T, Kitano M, Nagano H, Furukawa M, Adachi T, Yamaue H. A double-blind randomized comparative clinical trial to evaluate the safety and efficacy of dendritic cell vaccine loaded with WT1 peptides (TLP0-001) in combination with S-1 in patients with advanced pancreatic cancer refractory to standard chemotherapy. Trials. 2019; 20: 242.
104. Koesters R, Linnebacher M, Coy JF, Germann A, Schwitalle Y, Findeisen P, von Knebel Doeberitz M. WT1 is a tumor-associated antigen in colon cancer that can be recognized by in vitro stimulated cytotoxic T cells. Int J Cancer. 2004; 109: 385-392.
105. Shimodaira S, Sano K, Hirabayashi K, Koya T, Higuchi Y, Mizuno Y, Yamaoka N, Yuzawa M, Kobayashi T, Ito K, Koizumi T. Dendritic Cell-Based Adjuvant Vaccination Targeting Wilms' Tumor 1 in Patients with Advanced Colorectal Cancer. Vaccines (Basel). 2015; 3: 1004-1018.
106. Iiyama T, Udaka K, Takeda, S, Takeuchi T, Adachi Y C, Ohtsuki Y, Tsuboi A, Nakatsuka S, Elisseeva O A, Oji Y, Kawakami M, Nakajima H, Nishida S, Shirakata T, Oka, Y, Shuin T, Sugiyama H. WT1(Wilms’ Tumor 1) peptide immunotherapy for renal cell carcinoma. Microbiol Immunol. 2007; 51: 519-530.
107. Morita Y, Heike Y, Kawakami M, Miura O, Nakatsuka S, Ebisawa M, Mori S, Tanosaki R, Fukuda T, Kim SW, Tobinai K, Takaue Y. Monitoring of WT1-specific cytotoxic T lymphocytes after allogeneic hematopoietic stem cell transplantation. Int J Cancer. 2006; 119: 1360–1367.
108. Ogasawara M, Miyashita M, Ota S. Vaccination of Urological Cancer Patients With WT1 Peptide-Pulsed Dendritic Cells in Combination With Molecular Targeted Therapy or Conventional Chemotherapy Induces Immunological and Clinical Responses. Ther Apher Dial. 2018; 22: 266-277
109. Ohno S, Kyo S, Myojo S, Dohi S, Ishizaki J, Miyamoto K, Morita S, Sakamoto J, Enomoto T, Kimura T, Oka Y, Tsuboi A, Sugiyama H, Inoue M. Wilms' tumor 1 (WT1) peptide immunotherapy for gynecological malignancy. Anticancer Res. 2009; 29: 4779-4784.
110. Dohi S, Ohno S, Ohno Y, Takakura M, Kyo S, Soma G, Sugiyama H, Inoue M. WT1 peptide vaccine stabilized intractable ovarian cancer patient for one year: a case report. Anticancer Res. 2011; 31: 2441-2446.
111. Miyatake T, Ueda Y, Morimoto A, Enomoto T, Oka Y, Nishida S, Tsuboi A, Shirakata T, Oji Y, Hosen N, Aozasa K, Morita S, Sakamoto J, Sugiyama H, Kimura T. WT1 Peptide Immunotherapy for Gynecologic Malignancies Resistant to Conventional Therapies: a Phase II trial. J Cancer Res Clin Oncol. 2013; 139: 457-463.
112. Nishida S, Morimoto S, Oji Y, Morita S, Shirakata T, Enomoto T, Tsuboi A, Ueda Y, Yoshino K, Shouq A, Kanegae M, Ohno S, Fujiki F, Nakajima H, Nakae Y, Nakata J, Hosen N, Kumanogoh A, Oka Y, Kimura T, Sugiyama H. Cellular and humoral immune responses induced by an HLA class I-restricted peptide cancer vaccine targeting WT1 are associated with favorable clinical outcomes in advanced ovarian cancer. J Immunother. 2022; 45: 56-66.
113. Coosemans A, Vanderstraeten A, Tuyaerts S, Verschuere T, Moerman P, Berneman Z, Vergote I, Amant F, Van Gool SW. Immunological response after WT1 mRNA-loaded dendritic cell immunotherapy in ovarian carcinoma and carcinosarcoma. Anticancer Res. 2013; 33: 3855-3859.
114. Coosemans A, Vanderstraeten A, Tuyaerts S, Verschuere T, Moerman P, Berneman ZN, Vergote I, Amant F, VAN Gool SW. Wilms' Tumor Gene 1 (WT1)-loaded dendritic cell immunotherapy in patients with uterine tumors: a phase I/II clinical trial. Anticancer Res. 2013; 33: 5495-5500.
115. Coosemans A, Wölfl M, Berneman ZN, Van Tendeloo V, Vergote I, Amant F, Van Gool SW. Immunological response after therapeutic vaccination with WT1 mRNA-loaded dendritic cells in end-stage endometrial carcinoma. Anticancer Res. 2010; 30: 3709-3714.
116. Coosemans A. Wilms' Tumour gene 1 (WT1) as an immunotherapeutic target in uterine cancer. Facts Views Vis ObGyn. 2011; 3: 89-99.
117. Kobayashi M, Chiba A, Izawa H, Yanagida E, Okamoto M, Shimodaira S, Yonemitsu Y, Shibamoto Y, Suzuki N, Nagaya M; DC-vaccine study group at the Japan Society of Innovative Cell Therapy (J-SICT). The feasibility and clinical effects of dendritic cell-based immunotherapy targeting synthesized peptides for recurrent ovarian cancer. J Ovarian Res. 2014; 7:48.
118. Nishida S, Tsuboi A, Tanemura A, Ito T, Nakajima H, Shirakata T, Morimoto S, Fujiki F, Hosen N, Oji Y, Kumanogoh A, Kawase I, Oka Y, Azuma I, Morita S, Sugiyama H. Immune adjuvant therapy using Bacillus Calmette-Guérin cell wall skeleton (BCG-CWS) in advanced malignancies: A phase 1 study of safety and immunogenicity assessments. Medicine (Baltimore). 2019; 98: e16771.
119. Nishioka M, Tanemura A, Nishida S, Nakano A, Tsuboi A, Oji Y, Oka Y, Azuma I, Sugiyama H, Katayama I. Vaccination with WT-1 (Wilms' tumor gene-1) peptide and BCG-CWS in melanoma. Eur J Dermatol. 2012; 22: 258-259.
120. Fukuda K, Funakoshi T, Sakurai T, Nakamura Y, Mori M, Tanese K, Tanikawa A, Taguchi J, Fujita T, Okamoto M, Amagai M, Kawakami Y. Peptide-pulsed dendritic cell vaccine in combination with carboplatin and paclitaxel chemotherapy for stage IV melanoma. Melanoma Res. 2017; 27: 326-334.
121. Hashii Y, Sato E, Ohta H, Oka Y, Sugiyama H, Ozono K. WT1 peptide immunotherapy for cancer in children and young adults. Pediat Blood Cancer. 2010; 55: 352-355.
122. Ohta H, Hashii Y, Yoneda A, Takizawa S, Kusuki S, Tokimasa S, Fukuzawa M, Tsuboi A, Murao A, Oka Y, Oji Y, Aozasa K, Nakatsuka S, Sugiyama H, Ozono K. WT1 (Wilms' tumor 1) peptide immunotherapy for childhood rhabdomyosarcoma, Pediatr Hematol Oncol. 2009; 26: 74-83.
123. Sawada A, Inoue M, Kondo O, Yamada-Nakata K, Ishihara T, Kuwae Y, Nishikawa M, Ammori Y, Akihiro A, Oji Y, Koyama M, Oka Y, Yasui M, Sugiyama H, Kawa K. Feasibility of Cancer Immunotherapy with WT1 Peptide Vaccination for Solid Hematological Malignancies in Children. Pediatr Blood Cancer. 2016; 63: 234-41.
124. Miyachi M, Teramukai S, Matsumoto K, Sasahara Y, Takahashi Y, Karakawa S, Kobayashi M, Cho Y, Koga Y, Horiguchi G, Yamada A, Ito-Ihara T, Matsuyama K, Oji Y, Sugiyama H, Hosoi H. Results from a randomized trial of DSP-7888, a novel WT1 peptide-based vaccine, maintenance therapy in patients with rhabdomyosarcoma (RMS) and non-rhabdomyosarcoma soft tissue sarcoma (NRSTS). Oral presentation at: The 53rd Annual Congress of the International Society of Paediatric Oncology, October 23, 2021, Virtual Meeting.
125. Sugiyama M, Seigo K, Hosoya Y, Iguchi A, Manabe A. 131 I-MIBG therapy with WT-1 peptide for refractory neuroblastoma. Pediatr Int. 2020; 62: 746-747.
126. Nakata J, Nakajima H, Sugiyama H, et al. Extremely strong infiltration of WT1-specific CTLs into mouse tumor by the combination vaccine with WT1-specific CTL and helper peptides. Oncotarget. 2018; 9: 36029.
127. Fujiki F, Oka Y, Kawakatsu M, Tsuboi A, Tanaka-Harada Y, Hosen N, Nishida S, Shirakata T, Nakajima H, Tatsumi N, Hashimoto N, Taguchi T, Ueda S, Nonomura N, Takeda Y, Ito T, Myoui A, Izumoto S, Maruno M, Yoshimine T, Noguchi S, Okuyama A, Kawase I, Oji Y, Sugiyama H. A clear correlation between WT1-specific Th response and clinical response in WT1 CTL epitope vaccination. Anticancer Res. 2010; 30: 2247-2254.
128. Takahara A, Koido S, Ito M, Nagasaki E, Sagawa Y, Iwamoto T, Komita H, Ochi T, Fujiwara H, Yasukawa M, Mineno J, Shiku H, Nishida S, Sugiyama H, Tajiri H, Homma S. Gemcitabine enhances Wilms' tumor gene WT1 expression and sensitizes human pancreatic cancer cells with WT1-specific T-cell-mediated antitumor immune response. Cancer Immunol Immunother. 2011; 60: 1289-1297.
129. Koido S, Kan S, Yoshida K, Yoshizaki S, Takakura K, Namiki Y, Tsukinaga S, Odahara S, Kajihara M, Okamoto M, Ito M, Yusa SI, Gong J, Sugiyama H, Ohkusa T, Homma S, Tajiri H. Immunogenic Modulation of Cholangiocarcinoma Cells by Chemoimmunotherapy. Anticancer Res. 2014; 34: 6353-6362.
130. Smith PL, Yogaratnam Y, Samad M, Kasow S, Dalgleish AG. Effect of Gemcitabine based chemotherapy on the immunogenicity of pancreatic tumour cells and T-cells. Clin Transl Oncol. 2021; 23: 110-121.
131. Soeda A, Morita-Hoshi Y, Makiyama H, Morizane C, Ueno H, Ikeda M, Okusaka T, Yamagata S, Takahashi N, Hyodo I, Takaue Y, Heike Y. Regular dose of gemcitabine induces an increase in CD14+ monocytes and CD11c+ dendritic cells in patients with advanced pancreatic cancer. Jpn J Clin Oncol. 2009; 39: 797-806.
132. Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol. 2008; 8: 59-73.
133. Bracci L, Schiavoni G, Sistigu A, Belardelli F. Immune-based mechanisms of cytotoxic chemotherapy: implications for the design of novel and rationale-based combined treatments against cancer. Cell Death Differ. 2014; 21: 15-25.
134. Pusuluri A, Wu D, Mitragotri S. J Control Release. Immunological consequences of chemotherapy: Single drugs, combination therapies and nanoparticle-based treatments. J Control Release. 2019; 305: 130-154.
135. Hashii Y, Sato-Miyashita E, Matsumura R, Kusuki S, Yoshida H, Ohta H, Hosen N, Tsuboi A, Oji Y, Oka Y, Sugiyama H, Ozono K. WT1 peptide vaccination following allogeneic stem cell transplantation in pediatric leukemic patients with high risk for relapse: successful maintenance of durable remission. Leukemia. 2012; 26: 530-532.
136. Maeda T, Hosen N, Fukushima K, Tsuboi A, Morimoto S, Matsui T, Sata H, Fujita J, Hasegawa K, Nishida S, Nakata J, Nakae Y, Takashima S, Nakajima H, Fujiki F, TatsumiN, Kondo T, Hino M, Oji Y, Oka Y, Kanakura Y, Kumanogoh A Sugiyama H. Maintenance of complete remission after allogeneic stem cell transplantation in leukemia patients treated with Wilms tumor 1 peptide vaccine. Blood Cancer J. 2013; e130. Doi: 10.1038/bcj.2013.29
137. Saito S, Yanagisawa R, Yoshikawa K, Higuchi Y, Koya T, Yoshizawa K, Tanaka M, Sakashita K, Kobayashi T, Kurata T, Hirabayashi K, Nakazawa Y, Shiohara M, Yonemitsu Y, Okamoto M, Sugiyama H, Koike K, Shimodaira S. Safety and tolerability of allogeneic dendritic cell vaccination with induction of Wilms tumor 1-specific T cells in a pediatric donor and pediatric patient with relapsed leukemia: a case report and review of the literature. Cytotherapy. 2015; 17: 330-335.
138. Ishikawa T, Fujii N, Imada M, Aoe M, Meguri Y, Inomata T, Nakashima H, Fujii K, Yoshida S, Nishimori H, Matsuoka KI, Kondo E, Maeda Y, Tanimoto M. Graft-versus-leukemia effect with a WT1-specific T-cell response induced by azacitidine and donor lymphocyte infusions after allogeneic hematopoietic stem cell transplantation. Cytotherapy. 2017, 19: 514-520.
139. Yokota C, Nakata J, Takano K, Nakajima H, Hayashibara H, Minagawa H, Chiba Y, Hirayama R, Kijima N, Kinoshita M, Hashii Y, Tsuboi A, Oka Y, Oji Y, Kumanogoh A, Sugiyama H, Kagawa N, Kishima H. Distinct difference in tumor-infiltrating immune cells between Wilms' tumor gene 1 peptide vaccine and anti-programmed cell death-1 antibody therapies. Neuro-Oncol Adv. 2021; 3:1-10.
140. Oji Y, Kitamura Y, Kamino E, Kitano A, Sawabata N, Inoue M, Mori M, Nakatsuka SI, Sakaguchi N, Miyazaki K, Nakamura M, Fukuda I, Nakamura J, Tatsumi N, Takakuwa T, Nishida S, Shirakata T, Hosen N, Tsuboi A, Nezu R, Maeda H, Oka Y, Kawase I, Aozasa K, Okumura M, Miyoshi S, Sugiyama H. WT1 IgG antibody for early detection of nonsmall cell lung cancer and as its prognostic factor. Int J Cancer. 2009; 125: 381-387.
141. Tada K, Kitano S, Shoji H, Nishimura T, Shimada Y, Nagashima K, Aoki K, Hiraoka N, Honma Y, Iwasa S, Okita N, Takashima A, Kato K, Yamada Y, Katayama N, Boku N, Heike Y, Hamaguchi T. Pretreatment Immune Status Correlates with Progression-Free Survival in Chemotherapy-Treated Metastatic Colorectal Cancer Patients. Cancer Immunol Res. 2016; 4: 592-599.
142. Pagès F, Mlecnik B, Marliot F, Bindea G, Ou FS, Bifulco C, Lugli A, Zlobec I, Rau TT, Berger MD, Nagtegaal ID, Börger EV, Hartmann A, Geppert C, Kolwelter J, Merkel S, Grützmann R, Eynde MVD, Mourin AJ, Kartheuser A, Léonard D, Remue C, Wang JY, Bavi P, Roehrl MHA, Ohashi PS, Nguyen LT, Han SJ, Gregor HLM, Bakhtiari SH, Wouters BG, Masucci GV, Andersson EK, Zavadova E, Vocka M, Spacek J, Petruzelka L, Konopasek B, Dundr P, Skalova H, Nemejcova K, Botti G, Tatangelo F, Delrio P, Ciliberto G, Maio M, Laghi L, Grizzi F, Fredriksen T, Buttard B, Angelova M, Vasaturo A, Maby P, Church SE, Angell HK, Lafontaine L, Bruni D, Sissy CE, Haicheur N, Kirilovsky A, Berger A, Lagorce C, Meyers JP, Paustian C, Feng Z, Merino CB, Dijkstra J, Water CVD , Vliet SVLV, Knijn N, Mușină AM, Scripcariu DV, Popivanova B, Xu M, Fujita T, Hazama S, Suzuki N, Nagano H, Okuno K, Torigoe T, Sato N, Furuhata T, Takemasa I, Itoh K, Patel PS, Vora HH, Shah B, Patel JB, Rajvik KN, Pandya SJ, Shukla SN, Wang Y, Zhang G, Kawakami Y, Marincola FM, Ascierto PA, Sargent DJ, Fox BA, Galon J. International validation of the consensus Immunoscore for the classification of colon cancer: a prognostic and accuracy study. Lancet. 2018; 391: 2128-2139.
143. Kitayama J, Yasuda K, Kawai K, Sunami E, Nagawa H. Circulating lymphocyte is an important determinant of the effectiveness of preoperative radiotherapy in advanced rectal cancer. BMC Cancer. 2011; 11: 64.
144. Yoshimoto Y, Suzuki Y, Mimura K, Ando K, Oike T, Sato H, Okonogi N, Maruyama T, Izawa S, Noda S, Fujii H, Kono K, Nakano T. Radiotherapy-induced anti-tumor immunity contributes to the therapeutic efficacy of irradiation and can be augmented by CTLA-4 blockade in a mouse model. PLOS One. 2014; 9: e92572.
145. Saito Y, Kitamura H, Hijikata A, Murasawa MT, Tanaka S, Takagi S, Uchida N, Suzuki N, Sone A, Najima Y, Ozawa H, Wake A, Taniguchi S, Shultz LD, Oharaand O, Ishikawa F. Identification of therapeutic targets for quiescent, chemotherapy-resistant human leukemia stem cells. Sci Transl Med. 2010; 17: 17-19.
146. Hosen N, Sonoda Y, Oji Y, Kimura T, Minamiguchi H, Tamaki H, Kawakami M, Asada M, Kanato K, Motomura M, Murakami M, Fujioka T, Masuda T, Kim EH, Tsuboi A, Oka Y, Soma T, Ogawa H, Sugiyama H. Very low frequencies of human normal CD34+ hematopoietic progenitor cells express the Wilms’ tumor gene WT1 at the levels comaprable to those in leukemia cells. Brit J Hematol. 2002; 116: 409-420.
147. Gerber J M, Kowalski L Q, Smith B D, Griffin C A, Vala M S, Collector M I, Perkins B, Zahurak M, Matsui W, Gocke C D, Sharkis S J, Levitsky H I, Jones R J. Characterization of chronic myeloid leukemia stem cells. Am J Hematol. 2011; 86: 31-37.
148. Kanato K, Hosen N, Yanagihara M, Nakagata N, Shirakata T, Nakazawa T, Nishida S, Tsuboi A, Kawakami M, Masuda T, Oka Y, Oji Y, Sugiyama H. The Wilms' tumor gene WT1 is a common marker of progenitor cells in fetal liver. Biochem Biophys Res Commun. 2005; 326: 836-843.
2. Call K M, Glaser T, Ito C Y, Buckler A J, Pelletier J, Haber D A, Rose E A, Kral A, Yeger H, Lewis W H, Jones C, Housman D E. Isolation and characterization of a zinc finger polypeptide gene at the human chromosome 11 Wilms' tumor locus. Cell. 1990; 60: 509-520.
3. Sugiyama H. WT1 (Wilms' tumor gene 1): biology and cancer immunotherapy. Jpn J Clin Oncol. 2010; 40: 377-387.
4. Hastie ND. Wilms' tumour 1 (WT1) in development, homeostasis and disease. Development. 2017; 144: 2862-2872.
5. Wagner KD, Cherfils-Vicini J, Hosen N, Hohenstein P, Gilson E, Hastie ND, Michiels JF, Wagner N. The Wilms' tumour suppressor Wt1 is a major regulator of tumour angiogenesis and progression. Nat Commun. 2014; 5: 5852.
6. Wagner K D, Maï M E, Ladomery M, Belali T, Leccia N, Michiels J F, Wagner N. Altered VEGF Splicing Isoform Balance in Tumor Endothelium Involves Activation of Splicing Factors Srpk1 and Srsf1 by the Wilms' Tumor Suppressor Wt1. Cells. 2019; 8: 41.
7. Miwa H, Beran M, Saunders GF. Expression of the Wilms' tumor gene (WT1) in human leukemias. Leukemia. 1992; 6: 405-409.
8. Inoue K, Sugiyama H, Ogawa H, Nakagawa M, Yamagami T, Miwa H, Kita K, Hiraoka A, Masaoka T, Nasu K, Kyo T, Dohy H, Nakauchi H, Ishidate T, Akiyama T, Kishimoto T. WT1 as a new prognostic factor and a new marker for the detection of minimal residual disease in acute leukemia. Blood. 1994; 84: 3071-3079.
9. Yamagami T, Sugiyama H, Inoue K, Ogawa H, Tatekawa T, Hirata M, Kudoh T, Akiyama T, Murakami A, Maekawa T, Kishimoto T. Growth inhibition of human leukemic cells by WT1 (Wilms tumor gene) antisense oligodeoxynucleotides: Implications for the involvement of WT1 in leukemogenesis. Blood. 1996; 87: 2878-2884.
10. Algar E M, Khromykh T, Smith S I, Blackburn D M, Bryson G J, Smith P J. A WT1 antisense oligonucleotide inhibits proliferation and induces apoptosis in myeloid leukaemia cell lines. Oncogene. 1996; 12: 1005-1014.
11. Oji Y, Ogawa H, Tamaki H, Oka Y, Tsuboi A, Kim EH, Soma T, Tatekawa T, Kawakami M, Asada M, Kishimoto T, Sugiyama H. Expression of the Wilms' tumor gene WT1 in solid tumors and its involvement in tumor cell growth. Jpn J Cancer Res. 1999; 90: 194-204.
12. Nakatsuka S, Oji Y, Horiuchi T, Kanda T, Kitagawa M, Takeuchi T, Kawano K, Kuwae Y, Yamauchi A, Okumura M, Kitamura Y, Oka Y, Kawase I, Sugiyama H, Aozasa K. Immunohistochemical detection of WT1 protein in a variety of cancer cells. Mod Pathol. 2006; 19: 804-814.
13. Qi XW, Zhang F, Wu H, Liu JL, Zong BG, Xu C, Jiang J. Wilms' tumor 1 (WT1) expression and prognosis in solid cancer patients: a systematic review and meta-analysis. Sci Rep. 2015; 5:8924.
14. Inoue K, Ogawa H, Yamagami T, Soma T, Tani Y, Tatekawa T, Oji Y, Tamaki H, Kyo T, Dohy H, Hiraoka A, Masaoka T, Kishimoto T, Sugiyama H. Long-term follow-up of minimal residual disease in leukemia patients by monitoring WT1 (Wilms tumor gene) expression levels. Blood. 1996; 88: 2267-2278.
15. Cilloni D, Saglio G.WT1 as a universal marker for minimal residual disease detection and quantification in myeloid leukemias and in myelodysplastic syndrome. Acta Haematol. 2004; 112: 79-84.
16. Cilloni D, Gottardi E, De Micheli D, Serra A, Volpe G, Messa F, Rege-Cambrin G, Guerrasio A, Divona M, Lo Coco F, Saglio G. Quantitative assessment of WT1 expression by real time quantitative PCR may be a useful tool for monitoring minimal residual disease in acute leukemia patients. Leukemia. 2002; 16(10): 2115-2121.
17. Hashii Y, Kosaka Y, Watanabe K, Kato K, Imaizumi M, Kaneko T, Sunami S, Watanabe A, Hiramatsu H, Koga Y, Hirayama M, Nakao T, Hata T, Uchida N, Ishiyama K, Mitani K, Hidaka M, Kitamura K, Tsunemine H, Ueda Y, Mugitani A, Usuki K, Kanda Y, Miyazaki Y, Imai K, Naoe T, Koh K, Sugiyama H, Horibe K. Clinical Significance of WT1 mRNA Levels in Japanese Acute Lymphoblastic Leukemia Patients. J Leuk. 2017; 5: 243. Doi: 10.4172/2329-6917.1000243
18. Tamaki H, Ogawa H, Ohyashiki K, Oyhashiki JH, Iwama H, Inoue K, Soma T, Oka Y, Tatekawa T, Oji Y, Tsuboi A, Kim EH, Kawakami M, Fuchigami K, Tomonaga M, Toyama K, Aozasa K, Kishimoto T, Sugiyama H. The Wilms' tumor gene WT1 is a good marker for diagnosis of disease progression of myelodysplastic syndromes. Leukemia. 1999; 13: 393-399.
19. Cilloni D, Gottardi E, Messa F, Fava M, Scaravaglio P, Bertini M, Girotto M, Marinone C, Ferrero D, Gallamini A, Levis A, Saglio G; Piedmont Study Group on Myleodysplastic Syndromes. Significant correlation between the degree of WT1 expression and the International Prognostic Scoring System Score in patients with myelodysplastic syndromes. J Clin Oncol. 2003; 21: 1988-1995.
20. Ueda Y, Mizutani C, Nannya Y, Kurokawa M, Kobayashi S, Takeuchi J, Tamura H, Ogata K, Dan K, Shibayama H, Kanakura Y, Niimi K, Sasaki K, Watanabe M, Emi N, Teramura M, Motoji T, Kida M, Usuki K, Takada S, Sakura T, Ito Y, Ohyashiki K, Ogawa H, Suzuki T, Ozawa K, Imai K, Kasai M, Hata T, Miyazaki Y, Morita Y, Kanamaru A, Matsuda A, Tohyama K, Koga D, Tamaki H, Mitani K, Naoe T, Sugiyama H, Takaku F. Clinical evaluation of WT1 mRNA expression levels in peripheral blood and bone marrow in patients with myelodysplastic syndromes. Leuk Lymphoma. 2013; 54: 1450-1458.
21. Oka Y, Udaka K, Tsuboi A, Elisseeva OA, Ogawa H, Aozasa K, Kishimoto T, Sugiyama H. Cancer Immunotherapy targeting Wilms’ tumor gene WT1 product. J Immunol. 2000; 164: 1873-1880.
22. Gaiger A, Reese V, Disis M L, Cheever M A. Immunity to WT1 in the animal model and in patients with acute myeloid leukemia. Blood. 2000; 96: 1480-1489.
23. Oka Y, Elisseeva OA, Tsuboi A, Ogawa H, Tamaki H, Li H, Oji Y, Kim EH, Soma T, Asada M, Ueda K, Sugiyama H. Human cytotoxic T lymphocyte responses specific for peptides of wild-type Wilms’ tumor gene WT1 product. Immunogenetics. 2000; 51: 99-107
24. Gao L, Bellantuono I, Elsässer A, Marley SB, Gordon MY, Goldman JM, Stauss HJ. Selective elimination of leukemic CD34(+) progenitor cells by cytotoxic T lymphocytes specific for WT1. Blood. 2000; 95: 2198-2203.
25. Ohminami H, Yasukawa M, Fujita S. HLA class I-restricted lysis of leukemia cells by a CD8(+) cytotoxic T-lymphocyte clone specific for WT1 peptide. Blood. 2000; 95: 286-293.
26. Cheever MA, Allison JP, Ferris AS, Finn OJ, Hastings BM, Hecht TT, Mellman I, Prindiville SA, Viner JL, Weiner LM, Matrisian LM. The Prioritization of Cancer Antigens: A National Cancer Institute Pilot Project for the Acceleration of Translational Research. Clin Cancer Res. 2009; 15: 5323-5337.
27. Fujiki F, Oka Y, Tsuboi A, Kawakami M, Kawakatsu M, Nakajima H, Elisseeva OA, Harada Y, Ito K, Li Z, Tatsumi N, Sakaguchi N, Fujioka T, Masuda T, Yasukawa M, Udaka K, Kawase I, Oji Y, Sugiyama H. Identification and characterization of a WT1 (Wilms Tumor Gene) protein-derived HLA-DRB1*0405-restricted 16-mer helper peptide that promotes the induction and activation of WT1-specific cytotoxic T lymphocytes. J Immunother. 2007; 30: 282-93.
28. Nakajima H, Nakata J, Imafuku K, Hayashibara H, Isokawa K, Udaka K, Fujiki F, Morimoto S, Hasegawa K, Hosen N, Hashii Y, Nishida S, Tsuboi A, Oka Y, Oji Y, Sogo S, Sugiyama H. Identification of mouse helper epitopes for WT1-specific CD4+ T cells. Cancer Immunol Immunother. 2021; 70: 3323-3335.
29. Oka, Y, Tsuboi A, Murakami M, Hirai M, Tominaga N, Nakajima H, Masuda T, Nakano A, Kawakami M, Oji Y, Ikegame K, Hosen N, Udaka K, Yasukawa M, Ogawa H, Kawase I, Sugiyama H. WT1 peptide-based immunotherapy for patients with overt leukemia from myelodysplastic syndome (MDS) or MDS with myelofibrosis. Int J Hematol. 2003; 78: 56-61.
30. Oka Y, Tsuboi A, Taguchi T, Osaki T, Kyo T, Nakajima, Elisseeva OA, Oji Y, Kawakami M, Ikegame K, Hosen, N, Yoshihara S, Wu F, Fujiki F, Murakami M, Masuda T, Nishida S, Shirakata T, Nakatsuka S, Sasaki A, Udaka K, Dohy H, Aozasa K, Noguchi S, Kawase I, Sugiyama H. Induction of WT1 (Wilms’ tumor gene)-specific cytotoxic T lymphocytes by WT1 peptide vaccine and the resultant cancer regression. Proc Natl Acad Sci U S A. 2004; 101:13885-13890.
31. Rezvani K, Yong A S, Mielke S, Savani B N, Musse L, Superata J, Jafarpour B, Boss C, Barrett A J. Leukemia-associated antigen-specific T-cell responses following combined PR1 and WT1 peptide vaccination in patients with myeloid malignancies. Blood, 2008; 111: 236-42.
32. Keilholz U, Letsch A, Busse A, Asemissen AM, Bauer S, Blau IW, Hofmann WK, Uharek L, Thiel E, Scheibenbogen C. A clinical and immunologic phase 2 trial of Wilms tumor gene product 1 (WT1) peptide vaccination in patients with AML and MDS. Blood. 2009; 113: 6541-8.
33. Yasukawa M, Fujiwara H, Ochi T, Suemori K, Narumi H, Azuma T, Kuzushima K. Clinical efficacy of WT1 peptide vaccination in patients with acute myelogenous leukemia and myelodysplastic syndrome. Am J Hematol. 2009; 84: 314-315.
34. Maslak PG, Dao T, Krug LM, Chanel S, Korontsvit T, Zakhaleva V, Zhang R, Wolchok JD, Yuan J, Pinilla-Ibarz J, Berman E, Weiss M, Jurcic J, Frattini MG, Scheinberg DA. Vaccination with synthetic analog peptides derived from WT1 oncoprotein induces T-cell responses in patients with complete remission from acute myeloid leukemia. Blood. 2010; 116: 171-179.
35. Koido S, Okamoto M, Kobayashi M, Shimodaira S, Sugiyama H. Significance of Wilms' tumor 1 antigen as a cancer vaccine for pancreatic cancer. Discov Med. 2017; 24: 41-49.
36. Koya T, Date I, Kawaguchi H, Watanabe A, Sakamoto T, Togi M, Kato T Jr, Yoshida K, Kojima S, Yanagisawa R, Koido S, Sugiyama H, Shimodaira S. Dendritic Cells Pre-Pulsed with Wilms' Tumor 1 in Optimized Culture for Cancer Vaccination. Pharmaceutics. 2020; 12: 305.
37. Van Driessche A, Van de Velde AL, Nijs G, Braeckman T, Stein B, De Vries JM, Berneman ZN, Van Tendeloo VF. Clinical-grade manufacturing of autologous mature mRNA-electroporated dendritic cells and safety testing in acute myeloid leukemia patients in a phase I dose-escalation clinical trial. Cytotherapy. 2009; 11:653-668.
38. Dagvadorj N, Deuretzbacher A, Weisenberger D, Baumeister E, Trebing J, Lang I, Köchel C, Kapp M, Kapp K, Beilhack A, Hünig T, Einsele H, Wajant H, Grigoleit GU. Targeting of the WT1 91-138 fragment to human dendritic cells improves leukemia-specific T-cell responses providing an alternative approach to WT1-based vaccination. Cancer Immunol Immunother. 2017; 66: 319-332.
39. Tsuboi A, Oka Y, Udaka K, Murakami M, Masuda T, Nakano A, Nakajima H, Yasukawa M, Hiraki A, Oji Y, Kawakami M, Hosen N, Fujioka T, Wu F, Taniguchi Y, Nishida S, Asada M, Ogawa H, Kawase I, Sugiyama H. Enhanced induction of human WT1-specific cytotoxic T lymphocytes with a 9-mer WT1 peptide modified at HLA-A*2402-binding residues. Cancer Immunol Immunother. 2002; 51: 614-620.
40. Tsuboi A, Oka Y, Kyo T, Katayama Y, Elisseeva OA, Kawakami M, Nishida S, Morimoto S, Murao A, Nakajima H, Hosen N, Oji Y, Sugiyama H. Long-term WT1 peptide vaccination for patients with acute myeloid leukemia with minimal residual disease. Leukemia. 2012; 26: 1410-1413.
41. Mailänder V, Scheibenbogen C, Thiel E, Letsch A, Blau IW, Keilholz U. Complete remission in a patient with recurrent acute myeloid leukemia induced by vaccination with WT1 peptide in the absence of hematological or renal toxicity. Leukemia. 2004; 18: 165-166.
42. Ochsenreither S, Fusi A, Geikowski A, Stather D, Busse A, Stroux A, Letsch A, Keilholz U. Wilms' tumor protein 1 (WT1) peptide vaccination in AML patients: predominant TCR CDR3β sequence associated with remission in one patient is detectable in other vaccinated patients. Cancer Immunol Immunother. 2012; 61: 313-322.
43. Uttenthal B, Martinez-Davila I, Ivey A, Craddock C, Chen F, Virchis A, Kottaridis P, Grimwade D, Khwaja A, Stauss H, Morris EC. Wilms' Tumour 1 (WT1) peptide vaccination in patients with acute myeloid leukaemia induces short-lived WT1-specific immune responses. Br J Haematol. 2014; 164: 366-375.
44. Brayer J, Lancet JE, Powers J, List A, Balducci L, Komrokji R, Pinilla-Ibarz J. WT1 vaccination in AML and MDS: A pilot trial with synthetic analog peptides. Am J Hematol. 2015; 90: 602-607.
45. Shah NN, Loeb DM, Khuu H, Stroncek D, Ariyo T, Raffeld M, Delbrook C, Mackall CL, Wayne AS, Fry TJ. Induction of Immune Response after Allogeneic Wilms' Tumor 1 Dendritic Cell Vaccination and Donor Lymphocyte Infusion in Patients with Hematologic Malignancies and Post-Transplantation Relapse. Biol Blood Marrow Transplant. 2016; 22: 2149-2154.
46. Nakata J, Nakae Y, Kawakami M, Morimoto S, Motooka D, Hosen N, Fujiki F, Nakajima H, Hasegawa K, Nishida S, Tsuboi A, Oji Y, Oka Y, Kumanogoh A, Sugiyama H. Wilms tumour 1 peptide vaccine as a cure-oriented post-chemotherapy strategy for patients with acute myeloid leukaemia at high risk of relapse. Br J Haematol. 2018; 182: 287-290.
47. Nakata J, Oji Y, Oka Y, Sugiyama H. What should we tackle next in acute myeloid leukemia? Wilms tumor gene 1 vaccine therapy would be a promising and versatile strategy for acute myeloid leukemia. Expert Rev Hematol. 2019; 12: 211-213.
48. Maslak PG, Dao T, Scheinberg DA, Bernal Y, Chanel SM, Zhang R, Frattini M, Rosenblat T, Jurcic JG, Brentjens RJ, Arcila ME, Rampal R, Park JH, Douer D, Katz L, Sarlis N, Tallman M, Scheinberg DA. Phase 2 trial of a multivalent WT1 peptide vaccine (galinpepimut-S) in acute myeloid leukemia. Blood Adv. 2018; 2(3): 224.
49. Anguille S, Van de Velde AL, Smits EL, Van Tendeloo VF, Juliusson G, Cools N, Nijs G, Stein B, Lion E, Van Driessche A, Vandenbosch I, Verlinden A, Gadisseur AP, Schroyens WA, Muylle L, Vermeulen K, Maes MB, Deiteren K, Malfait R, Gostick E, Lammens M, Couttenye MM, Jorens P, Goossens H, Price DA, Ladell K, Oka Y, Fujiki F, Oji Y, Sugiyama H, Berneman ZN. Dendritic cell vaccination as postremission treatment to prevent or delay relapse in acute myeloid leukemia. Blood. 2017; 130: 1713-1721.
50. Van Tendeloo VF, Van de Velde A, Van Driessche A, Cools N, Anguille S, Ladell K, Gostick E, Vermeulen K, Pieters K, Nijs G, Stein B, Smits EL, Schroyens WA, Gadisseur AP, Vrelust I, Jorens PG, Goossens H, de Vries IJ, Price DA, Oji Y, Oka Y, Sugiyama H, Berneman ZN. Induction of complete and molecular remissions in acute myeloid leukemia by Wilms' tumor 1 antigen-targeted dendritic cell vaccination. Proc Natl Acad Sci U S A. 2010; 107: 13824-13829.
51. Kobayashi Y, Sakura T, Miyawaki S, Toga K, Sogo S, Heike Y. A new peptide vaccine OCV-501: in vitro pharmacology and phase 1 study in patients with acute myeloid leukemia. Cancer Immunol Immunother. 2017; 66: 851-863.
52. Kiguchi T, Yamaguchi M, Takezako N, Miyawaki S, Masui K, Ihara Y, Hirota M, Shimofurutani N, Naoe T. Cancer Immunol Immunother. Efficacy and safety of Wilms' tumor 1 helper peptide OCV-501 in elderly patients with acute myeloid leukemia: a multicenter, randomized, double-blind, placebo-controlled phase 2 trial. Cancer Immunol Immunother. https://doi.org/10.1007/s00262-021-03074-4.
53. Oji Y, Oka Y, Nishida S, Tsuboi A, Kawakami M, Shirakata T, Takahashi K, Murao A, Nakajima H, Narita M, Takahashi M, Morita S, Sakamoto J, Tanaka T, Kawase I, Hosen N, Sugiyama H. WT1 peptide vaccine induces reduction in minimal residual disease in an Imatinib-treated CML patient. Eur J Haematol. 2010; 85: 358-360.
54. Narita M, Masuko M, Kurasaki T, Kitajima T, Takenouchi S, Saitoh A, Watanabe N, Furukawa T, Toba K, Fuse I, Aizawa Y, Kawakami M, Oka Y, Sugiyama H, Takahashi M. WT1 peptide vaccination in combination with imatinib therapy for a patient with CML in the chronic phase. Int J Med Sci. 2010; 7: 72-81.
55. Saitoh A, Narita M, Watanabe N, Tochiki N, Yamahira A, Nakamura T, Kaji M, Masuko M, Furukawa T, Toba K, Fuse I, Aizawa Y, Takahashi M. WT1 peptide vaccination in a CML patient: induction of effective cytotoxic T lymphocytes and significance of peptide administration interval. Med Oncol. 2011; 28: 219-230.
56. Hughes A, Clarson J, Tang C, Vidovic L, White DL, Hughes TP, Yong AS.CML patients with deep molecular responses to TKI have restored immune effectors and decreased PD-1 and immune suppressors. Blood. 2017; 129: 1166-1176.
57. Dong WZ, Dan L, jun HX. Graft-versus-leukemia effects of Wilms’ tumor 1 protein-specific cytotoxic T lymphocytes in patients with chronic myeloid leukemia after allogeneic hematopoietic stem cell transplantation. Chin Med J. 2010; 123: 912-916.
58. Ueda Y, Ogura M, Miyakoshi S, Suzuki T, Heike Y, Tagashira S, Tsuchiya S, Ohyashiki K, Miyazaki Y. Phase 1/2 study of the WT1 peptide cancer vaccine WT4869 in patients with myelodysplastic syndrome. Cancer Sci. 2017; 108: 2445-2453.
59. Miyakoshi S, Usuki K, Matsumura I, Ueda Y, Iwasaki H, Miyamoto T, Origuchi M, Tagashira S, Ichiro Naoi, Naoe T, Kizaki M, Heike Y, Akashi K, Miyazaki Y. Preliminary results from a phase 1/2 study of DSP-7888, a novel WT1 peptide-based vaccine, in patients with myelodysplastic syndrome (MDS). Blood. 2016; 128: 4335.
60. Usuki K, Ueda Y, Fujita J, Matsumura I, Aotsuka N, Sekiguchi N, Nakazato T, Iwasaki H, Watanabe A, Sugimoto S, Yamakawa EK, Naoe T, Kizaki M, Heike Y, Miyazaki Y, Akashi K. Phase 1/2 study of DSP-7888 in patients with higher-risk (HR) myelodysplastic syndromes (MDS) after failure of azacitidine (AZA) therapy. https://library.ehaweb.org/eha/2019/24th/266961/kensuke.usuki.phase.1.2.study.of.dsp-7888.in.patients.with.higher-risk.%28hr%29.html.
61. Spira A, Hansen AR, Harb WA, Curtis KK, Koga-Yamakawa E, Origuchi M, Li Z, Ertik B, Shaib WL. Multicenter, Open-Label, Phase I Study of DSP-7888 Dosing Emulsion in Patients with Advanced Malignancies. Target Oncol. 2021; 16: 461-469.
62. Ogasawara M, Miyashita M, Yamagishi Y, Ota S. Wilms’ tumor 1 peptide-loaded dendritic cell vaccination in patients with relapsed or refractory malignant lymphoma. Leuk Lymph. http://doi.org/10.1080/10428194.2022.2038371.
63. Israyelyan A, La Rosa C, Tsai W, Kaltcheva T, Srivastava T, Aquino L, Li J, Kim Y, Palmer J, Streja L, Senitzer D, Zaia JA, Rosenwald A, Forman SJ, Nakamura R, Diamond DJ. Detection and preliminary characterization of CD8+T lymphocytes specific for Wilms' tumor antigen in patients with non-Hodgkin lymphoma. Leuk Lymph. 2013; 54: 2490-2499.
64. Tsuboi A, Oka Y, Nakajima H, Fukuda Y, Elisseeva O. A, Yoshihara S, Hosen N, Ogata A, Kito K, Fujiki F, Nishida S Shirakata T Ohno S, Yasukawa M, Oji Y, Kawakami M, Morita S, Sakamoto J, Udaka K, Kawase I, Sugiyama H. Wilms’ tumor gene WT1 peptide-based immunotherapy induced minimal response in a patient with advanced, therapy-resistant multiple myeloma. Int J Hematol. 2007; 86: 414-417.
65. Tyler EM, Jungbluth AA, O'Reilly RJ, Koehne G. WT1-specific T-cell responses in high-risk multiple myeloma patients undergoing allogeneic T cell-depleted hematopoietic stem cell transplantation and donor lymphocyte infusions. Blood. 2013; 121: 308-317.
66. Izumoto S, Tsuboi A, Oka Y, Suzuki T, Hashiba T, Kagawa N, Hashimoto N, Maruno M, Elisseeva, OA, Shirakata T, Kawakami M, Oji Y, Nishida S, Ohno S, Kawase I, Hatazawa J, Morita S, Sakamoto J, Sugiyama H, Yoshimine T. Phase II clinical trial of Wilms tumor 1 peptide vaccination for patients with recurrent glioblastoma multiforme. J Neurosurg. 2008; 108: 963-971.
67. Hashimoto N, Tsuboi A, Kagawa N, Chiba Y, Izumoto S, Kinoshita M, Kijima N, Oka Y, Morimoto S, Nakajima H, Morita S, Sakamoto J, Nishida S, Hosen N, Oji Y, Arita N, Yoshimine T, Sugiyama H. Wilms tumor 1 peptide vaccination combined with temozolomide against newly diagnosed glioblastoma: safety and impact on immunological response. Cancer Immunol Immunother. 2015; 64: 707-716.
68. Tsuboi A, Hashimoto N, Fujiki F, Morimoto S, Kagawa N, Nakajima H, Hosen N, Nishida S, Nakata J, Morita S, Sakamoto J, Oji Y, Oka Y, Sugiyama H. A phase I clinical study of a cocktail vaccine of Wilms' tumor 1 (WT1) HLA class I and II peptides for recurrent malignant glioma. Cancer Immunol Immunother. 2019; 68: 331-340.
69. Chiba Y, Hashimoto N, Tsuboi A, Rabo C, Oka Y, Kinoshita M, Kagawa N, Oji Y, Sugiyama H, Yoshimine T. Prognostic value of WT1 protein expression level and MIB-1 staining index as predictor of response to WT1 immunotherapy in glioblastoma patients. Brain Tumor Pathol. 2010; 27: 29-34.
70. Sakai K, Shimodaira S, Maejima S, Udagawa N, Sano K, Higuchi Y, Koya T, Ochiai T, Koide M, Uehara S, Nakamura M, Sugiyama H, Yonemitsu Y, Okamoto M, Hongo K. Dendritic cell-based immunotherapy targeting Wilms' tumor 1 in patients with recurrent malignant glioma. J Neurosurg. 2015; 123: 989-997.
71. Sakai K, Shimodaira S, Maejima S, Sano K, Higuchi Y, Koya T, Sugiyama H, Hongo K. Clinical effect and immunological response in patients with advanced malignant glioma treated with WT1-pulsed dendritic cell-based immunotherapy: A report of two cases. Interdisciplinary Neurosurg.2017; 9:24-29.
72. Hashii Y, Oka Y, Kagawa N, Hashimoto N, Saitou H, Fukuya S, Kanegae M, Ikejima S, Oji Y, OzonoK, Tsuboi A, Sugiyama H. Encouraging clinical evolution of a pediatric patient with relapsed diffuse midline glioma who underwent WT1-targeting immunotherapy: A case report and literature review. Front Oncol. 2020; 10: 1188.
73. Yokota C, Takano K, Chiba Y, Kagawa N, Tsuboi A, Oka Y, Oji Y, Kinoshita M, Kijima N, Kishima H, Izumoto S, Sugiyama H, Hashimoto N. Maintenance of WT1 expression in tumor cells is associated with good prognosis in malignant glioma patients treated with WT1 peptide vaccine immunotherapy. Cancer Immunol Immunother. 2022; 71: 189-201.
74. Fu S, Piccioni DE, Liu H, Lukas RV, Kesari S, Aregawi D, Hong DS, Yamaguchi K, Whicher K, Zhang Y, Chen YL, Poola N, Eddy J, Blum D. A phase I study of the WT2725 dosing emulsion in patients with advanced malignancies. Sci Rep. 2021; 11: 22355.
75. Fujisaki H, Hashii Y, Terashima K, Goto H, Horibe K, Sugiyama K, Watanabe A, Sugimoto S, Yanagisawa T, Kikuta A, Kawamoto H, Hashimoto N, Hara J. Phase 1/2 study of DSP-7888 in pediatric patients with malignant glioma. 23rd Annual Scientific Meeting and Education Day of the Society for Neuro-oncology, New Orleans, 2018. Neuro Oncol. 2018; 20 (Suppl 6): vi202.
76. Ogasawara M, Miyashita M, Yamagishi Y, Ota S. Phase I/II Pilot Study of Wilms' Tumor 1 Peptide-Pulsed Dendritic Cell Vaccination Combined With Conventional Chemotherapy in Patients With Head and Neck Cancer. Ther Apher Dial. 2019; 23: 279-288.
77. Tsuboi A, Oka Y, Osaka T, Kumagai T, Tachibana I, Hayashi S, Murakami M, Nakajima H, Elisseeva OA, Wu F, Masuda T, Yasukawa M, Oji Y, Kawakami M, Hosen N, Ikegame K, Yoshihara S, Udaka K, Nakatsuka S, Aozasa K. Kawase I, Sugiyama H. WT1 peptide-based immunotherapy for patients with lung cancer. Microbiol Immunol. 2004; 48: 175-184.
78. Krug LM, Dao T, Brown AB, Maslak P, Travis W, Bekele S, Korontsvit T, Zakhaleva V, Wolchok J, Yuan J, Li H, Tyson L, Scheinberg DA. WT1 peptide vaccinations induce CD4 and CD8 T cell immune responses in patients with mesothelioma and non-small cell lung cancer. Cancer Immunol Immunother. 2010; 59: 1467-1479.
79. Takahashi H, Okamoto M, Shimodaira S, Tsujitani S, Nagaya M, Ishidao T, Kishimoto J, Yonemitsu Y; DC-vaccine study group at the Japan Society of Innovative Cell Therapy (J-SICT). Impact of dendritic cell vaccines pulsed with Wilms' tumour-1 peptide antigen on the survival of patients with advanced non-small cell lung cancers. Eur J Cancer. 2013; 49: 852-859.
80. May RJ, Dao T, Pinilla-Ibarz J, Korontsvit T, Zakhaleva V, Zhang RH, Maslak P, Scheinberg DA. Peptide epitopes from the Wilms' tumor 1 oncoprotein stimulate CD4+ and CD8+ T cells that recognize and kill human malignant mesothelioma tumor cells. Clin Cancer Res. 2007; 13: 4547-4555.
81. Zauderer MG, Tsao AS, Dao T, Panageas K, Lai WV, Rimner A, Rusch VW, Adusumilli PS, Ginsberg MS, Gomez D, Rice D, Mehran R, Scheinberg DA, Krug LM. A Randomized phase II trial of adjuvant galinpepimut-S, WT-1 analogue peptide vaccine, after multimodality therapy for patients with malignant pleural mesothelioma. Clin Cancer Res. 2017; 23: 7483.
82. Oji Y, Inoue M, Takeda Y, Hosen N, Shintani Y, Kawakami M, Harada T, Murakami Y, Iwai M, Fukuda M, Nishida S, Nakata J, Nakae Y, Takashima S, Shirakata T, Nakajima H, Hasegawa K, Kida H, Kijima T, Morimoto S, Fujiki F, Tsuboi A, Morii E, Morita S, Sakamoto J, Kumanogoh A, Oka Y, Okumura M, Sugiyama H. WT1 peptide-based immunotherapy for advanced thymic epithelial malignancies. Int J Cancer. 2018; 142: 2375-2382.
83. Takahashi N, Zhao C, Rajan A. WT1 as an immunotherapy target for thymic epithelial tumors: a novel method to activate anti-tumor immunity. Mediastinum. 2019; 3: 11.
84. Higgins M, Curigliano G, Dieras V, Kuemmel S, Kunz G, Fasching PA, Campone M, Bachelot T, Krivorotko P, Chan S, Ferro A, Schwartzberg L, Gillet M, De Sousa Alves PM, Wascotte V, Lehmann FF, Goss P. Safety and immunogenicity of neoadjuvant treatment using WT1-immunotherapeutic in combination with standard therapy in patients with WT1-positive Stage II/III breast cancer: a randomized Phase I study. Breast Cancer Res Treat. 2017; 162: 479-488.
85. Gillmore R, Xue SA, Holler A, Kaeda J, Hadjiminas D, Healy V, Dina R, Parry SC, Bellantuono I, Ghani Y, Coombes RC, Waxman J, Stauss HJ. Detection of Wilms' tumor antigen--specific CTL in tumor-draining lymph nodes of patients with early breast cancer. Clin Cancer Res. 2006; 12: 34-42.
86. Sasabe E, Hamada F, Iiyama T, Udaka K, Sugiyama H, Yamamoto T. Wilm's tumor gene WT1 peptide immunotherapy for pulmonary metastasis from adenoid cystic carcinoma of the salivary gland. Oral Oncology. 2011; 47: 77-78.
87. Shirakata T, Oka Y, Nishida S, Hosen N, Tsuboi A, Oji Y, Murao A, Tanaka H, Nakatsuka S, Inohara H, Sugiyama H. WT1 Peptide Therapy for a Patient with Chemotherapy-resistant Salivary Gland Cancer. Anticancer Res. 2012; 32: 1081-1086.
88. Matsuda T, Takeuchi H, Sakurai T, Mayanagi S, Booka E, Fujita T, Higuchi H, Taguchi J, Hamamoto Y, Takaishi H, Kawakubo H, Okamoto M, Sunamura M, Kawakami Y, Kitagawa Y. Pilot study of WT1 peptide-pulsed dendritic cell vaccination with docetaxel in esophageal cancer. Oncol Lett. 2018; 16: 1348-1356.
89. Ogasawara M, Miyashita M, Yamagishi Y, Ota S. Immunotherapy employing dendritic cell vaccination for patients with advanced or relapsed esophageal cancer. Ther Apher Dial. 2020; 24: 482-491.
90. Kobayashi M, Sakabe T, Chiba A, Nakajima A, Okamoto M, Shimodaira A, Yonemitsu Y, Shibamoto Y, Suzuki N, Nagaya M. Therapeutic effect of intratumoral injections of dendritic cells for locally recurrent gastric cancer: a case report. World J Surg Oncol. 2014; 12: 390.
91. Lu X, Liu J, Cui P, Liu T, Piao C, Xu X, Zhang Q, Xiao M, Liu X, Wang Y, Yang L. Am J Cancer Res. Co-inhibition of TIGIT, PD1, and Tim3 reverses dysfunction of Wilms tumor protein-1 (WT1)-specific CD8+ T lymphocytes after dendritic cell vaccination in gastric cancer. Am J Cancer Res. 2018; 8: 1564-1575.
92. Kaida M, Morita-Hoshi Y, Soeda A, Wakeda T, Yamaki Y, Kojima Y, Ueno H, Kondo S, Morizane C, Ikeda M, Okusaka T, Takaue Y, Heike Y. Phase 1 trial of Wilms tumor 1 (WT1) peptide vaccine and gemcitabine combination therapy in patients with advanced pancreatic or biliary tract cancer. J Immunother. 2011; 34: 92-99.
93. Nishida S, Koido S, Takeda Y,Honma S, Kimita H, Takahara A, Morita S, Ito T, Morimoto S, Hara K, Tsuboi A, Oka Y, Yanagisawa S, Toyama Y, Ikegami M, Kitagawa T, Eguchi H, Wada H, Nagano H, Nakata J, Nakae Y, Hosen N, Oji Y, Tanaka T, Kawase I, Kumanogoh A, Sakamoto J, Doki Y, Mori M,Ohkusa T, Tajiri H, Sugiyama H. Wilms Tumor Gene 1 (WT1) Peptide–based Cancer Vaccine Combined With Gemcitabine for Patients With Advanced Pancreatic Cancer. J Immunother. 2014; 37: 105-114.
94. Nishida S, Ishikawa T, Sugiyama H, et al. Combination gemcitabine and WT1 peptide vaccination improves progression-free survival in advanced pancreatic ductal adenocarcinoma: A phase II randomized study. Cancer Immunol Res. 2018; 6: 320.
95. Kimura Y, Tsukada J, Tomoda T, Takahashi H, Imai K, Shimamura K, Sunamura M, Yonemitsu Y, Shimodaira S, Koido S, Homma S, Okamoto M. Clinical and immunologic evaluation of dendritic cell-based immunotherapy in combination with gemcitabine and/or S-1 in patients with advanced pancreatic carcinoma. Pancreas. 2012; 41: 195-205.
96. Mayanagi S, Kitago M, Sakurai T, Matsuda T, Fujita T, Higuchi H, Taguchi J, Takeuchi H, Itano O, Aiura K, Hamamoto Y, Takaishi H, Okamoto M, Sunamura M, Kawakami Y, Kitagawa Y. Phase I pilot study of Wilms tumor gene 1 peptide-pulsed dendritic cell vaccination combined with gemcitabine in pancreatic cancer. Cancer Sci. 2015; 106: 397-406.
97. Hanada S, Tsuruta T, Hiraguchi K, Okamoto M, Sugiyama H, Koido S. Long-term survival of pancreatic cancer patients treated with multimodal therapy combined with WT1-targeted dendritic cell vaccines. Hum Vaccin Immunother. 2019; 15: 397-406.
98. Nagai K, Adachi T, Harada H, Eguchi S, Sugiyama H, Miyazaki Y. Dendritic cell-based immunotherapy pulsed with Wilms Tumor 1 peptide and MUC-1 as an adjuvant therapy for pancreatic ductal adenocarcinoma after curative resection: a PhaseⅠ/Ⅱa clinical trial. Anticancer Res. 2020; 40: 5765-5776.
99. Ota S, Miyashita M, Yamagishi Y, Ogasawara M. Baseline immunity predicts prognosis of pancreatic cancer patients treated with WT1 and/or MUC1 peptide-loaded dendritic cell vaccination and a standard chemotherapy. Hum Vaccin Immunother. 2021; 17: 1-10.
100. Koido S, Homma S, Okamoto M, Takakura K, Mori M, Yoshizaki S, Tsukinaga S, Odahara S, Koyama S, Imazu H, Uchiyama K, Kajihara M, Arakawa H, Misawa T, Toyama Y, Yanagisawa S, Ikegami M, Kan S, Hayashi K, Komita H, Kamata Y, Ito M, Ishidao T, Yusa SI, Shimodaira S, Gong J, Sugiyama H, Ohkusa T, Tajiri H. Treatment with Chemotherapy and Dendritic Cells Pulsed with Multiple Wilms' Tumor 1 (WT1)-Specific MHC Class I/II-Restricted Epitopes for Pancreatic Cancer. Clin Cancer Res. 2014; 20: 4228-4239.
101. Koido S, Okamoto M, Shimodaira S, Sugiyama H. Wilms' tumor 1 (WT1)-targeted cancer vaccines to extend survival for patients with pancreatic cancer. Immunotherapy. 2016; 8: 1309-1320.
102. Yanagisawa R, Koizumi T, Koya T, Sano K, Koido S, Nagai K, Kobayashi M, Okamoto M, Sugiyama H, Shimodaira S. WT1-pulsed Dendritic Cell Vaccine Combined wirh Chemotherapy for Resected Pancreatic Cancer in a Phase Ⅰ Study. Anticance Res. 2018; 38: 2217-2225.
103. Katsuda M, Miyazawa M, Ojima T, Katanuma A, Hakamada K, Sudo K, Asahara S, Endo I, Ueno M, Hara K, Yamada S, Fujii T, Satoi S, Ioka T, Ohira M, Akahori T, Kitano M, Nagano H, Furukawa M, Adachi T, Yamaue H. A double-blind randomized comparative clinical trial to evaluate the safety and efficacy of dendritic cell vaccine loaded with WT1 peptides (TLP0-001) in combination with S-1 in patients with advanced pancreatic cancer refractory to standard chemotherapy. Trials. 2019; 20: 242.
104. Koesters R, Linnebacher M, Coy JF, Germann A, Schwitalle Y, Findeisen P, von Knebel Doeberitz M. WT1 is a tumor-associated antigen in colon cancer that can be recognized by in vitro stimulated cytotoxic T cells. Int J Cancer. 2004; 109: 385-392.
105. Shimodaira S, Sano K, Hirabayashi K, Koya T, Higuchi Y, Mizuno Y, Yamaoka N, Yuzawa M, Kobayashi T, Ito K, Koizumi T. Dendritic Cell-Based Adjuvant Vaccination Targeting Wilms' Tumor 1 in Patients with Advanced Colorectal Cancer. Vaccines (Basel). 2015; 3: 1004-1018.
106. Iiyama T, Udaka K, Takeda, S, Takeuchi T, Adachi Y C, Ohtsuki Y, Tsuboi A, Nakatsuka S, Elisseeva O A, Oji Y, Kawakami M, Nakajima H, Nishida S, Shirakata T, Oka, Y, Shuin T, Sugiyama H. WT1(Wilms’ Tumor 1) peptide immunotherapy for renal cell carcinoma. Microbiol Immunol. 2007; 51: 519-530.
107. Morita Y, Heike Y, Kawakami M, Miura O, Nakatsuka S, Ebisawa M, Mori S, Tanosaki R, Fukuda T, Kim SW, Tobinai K, Takaue Y. Monitoring of WT1-specific cytotoxic T lymphocytes after allogeneic hematopoietic stem cell transplantation. Int J Cancer. 2006; 119: 1360–1367.
108. Ogasawara M, Miyashita M, Ota S. Vaccination of Urological Cancer Patients With WT1 Peptide-Pulsed Dendritic Cells in Combination With Molecular Targeted Therapy or Conventional Chemotherapy Induces Immunological and Clinical Responses. Ther Apher Dial. 2018; 22: 266-277
109. Ohno S, Kyo S, Myojo S, Dohi S, Ishizaki J, Miyamoto K, Morita S, Sakamoto J, Enomoto T, Kimura T, Oka Y, Tsuboi A, Sugiyama H, Inoue M. Wilms' tumor 1 (WT1) peptide immunotherapy for gynecological malignancy. Anticancer Res. 2009; 29: 4779-4784.
110. Dohi S, Ohno S, Ohno Y, Takakura M, Kyo S, Soma G, Sugiyama H, Inoue M. WT1 peptide vaccine stabilized intractable ovarian cancer patient for one year: a case report. Anticancer Res. 2011; 31: 2441-2446.
111. Miyatake T, Ueda Y, Morimoto A, Enomoto T, Oka Y, Nishida S, Tsuboi A, Shirakata T, Oji Y, Hosen N, Aozasa K, Morita S, Sakamoto J, Sugiyama H, Kimura T. WT1 Peptide Immunotherapy for Gynecologic Malignancies Resistant to Conventional Therapies: a Phase II trial. J Cancer Res Clin Oncol. 2013; 139: 457-463.
112. Nishida S, Morimoto S, Oji Y, Morita S, Shirakata T, Enomoto T, Tsuboi A, Ueda Y, Yoshino K, Shouq A, Kanegae M, Ohno S, Fujiki F, Nakajima H, Nakae Y, Nakata J, Hosen N, Kumanogoh A, Oka Y, Kimura T, Sugiyama H. Cellular and humoral immune responses induced by an HLA class I-restricted peptide cancer vaccine targeting WT1 are associated with favorable clinical outcomes in advanced ovarian cancer. J Immunother. 2022; 45: 56-66.
113. Coosemans A, Vanderstraeten A, Tuyaerts S, Verschuere T, Moerman P, Berneman Z, Vergote I, Amant F, Van Gool SW. Immunological response after WT1 mRNA-loaded dendritic cell immunotherapy in ovarian carcinoma and carcinosarcoma. Anticancer Res. 2013; 33: 3855-3859.
114. Coosemans A, Vanderstraeten A, Tuyaerts S, Verschuere T, Moerman P, Berneman ZN, Vergote I, Amant F, VAN Gool SW. Wilms' Tumor Gene 1 (WT1)-loaded dendritic cell immunotherapy in patients with uterine tumors: a phase I/II clinical trial. Anticancer Res. 2013; 33: 5495-5500.
115. Coosemans A, Wölfl M, Berneman ZN, Van Tendeloo V, Vergote I, Amant F, Van Gool SW. Immunological response after therapeutic vaccination with WT1 mRNA-loaded dendritic cells in end-stage endometrial carcinoma. Anticancer Res. 2010; 30: 3709-3714.
116. Coosemans A. Wilms' Tumour gene 1 (WT1) as an immunotherapeutic target in uterine cancer. Facts Views Vis ObGyn. 2011; 3: 89-99.
117. Kobayashi M, Chiba A, Izawa H, Yanagida E, Okamoto M, Shimodaira S, Yonemitsu Y, Shibamoto Y, Suzuki N, Nagaya M; DC-vaccine study group at the Japan Society of Innovative Cell Therapy (J-SICT). The feasibility and clinical effects of dendritic cell-based immunotherapy targeting synthesized peptides for recurrent ovarian cancer. J Ovarian Res. 2014; 7:48.
118. Nishida S, Tsuboi A, Tanemura A, Ito T, Nakajima H, Shirakata T, Morimoto S, Fujiki F, Hosen N, Oji Y, Kumanogoh A, Kawase I, Oka Y, Azuma I, Morita S, Sugiyama H. Immune adjuvant therapy using Bacillus Calmette-Guérin cell wall skeleton (BCG-CWS) in advanced malignancies: A phase 1 study of safety and immunogenicity assessments. Medicine (Baltimore). 2019; 98: e16771.
119. Nishioka M, Tanemura A, Nishida S, Nakano A, Tsuboi A, Oji Y, Oka Y, Azuma I, Sugiyama H, Katayama I. Vaccination with WT-1 (Wilms' tumor gene-1) peptide and BCG-CWS in melanoma. Eur J Dermatol. 2012; 22: 258-259.
120. Fukuda K, Funakoshi T, Sakurai T, Nakamura Y, Mori M, Tanese K, Tanikawa A, Taguchi J, Fujita T, Okamoto M, Amagai M, Kawakami Y. Peptide-pulsed dendritic cell vaccine in combination with carboplatin and paclitaxel chemotherapy for stage IV melanoma. Melanoma Res. 2017; 27: 326-334.
121. Hashii Y, Sato E, Ohta H, Oka Y, Sugiyama H, Ozono K. WT1 peptide immunotherapy for cancer in children and young adults. Pediat Blood Cancer. 2010; 55: 352-355.
122. Ohta H, Hashii Y, Yoneda A, Takizawa S, Kusuki S, Tokimasa S, Fukuzawa M, Tsuboi A, Murao A, Oka Y, Oji Y, Aozasa K, Nakatsuka S, Sugiyama H, Ozono K. WT1 (Wilms' tumor 1) peptide immunotherapy for childhood rhabdomyosarcoma, Pediatr Hematol Oncol. 2009; 26: 74-83.
123. Sawada A, Inoue M, Kondo O, Yamada-Nakata K, Ishihara T, Kuwae Y, Nishikawa M, Ammori Y, Akihiro A, Oji Y, Koyama M, Oka Y, Yasui M, Sugiyama H, Kawa K. Feasibility of Cancer Immunotherapy with WT1 Peptide Vaccination for Solid Hematological Malignancies in Children. Pediatr Blood Cancer. 2016; 63: 234-41.
124. Miyachi M, Teramukai S, Matsumoto K, Sasahara Y, Takahashi Y, Karakawa S, Kobayashi M, Cho Y, Koga Y, Horiguchi G, Yamada A, Ito-Ihara T, Matsuyama K, Oji Y, Sugiyama H, Hosoi H. Results from a randomized trial of DSP-7888, a novel WT1 peptide-based vaccine, maintenance therapy in patients with rhabdomyosarcoma (RMS) and non-rhabdomyosarcoma soft tissue sarcoma (NRSTS). Oral presentation at: The 53rd Annual Congress of the International Society of Paediatric Oncology, October 23, 2021, Virtual Meeting.
125. Sugiyama M, Seigo K, Hosoya Y, Iguchi A, Manabe A. 131 I-MIBG therapy with WT-1 peptide for refractory neuroblastoma. Pediatr Int. 2020; 62: 746-747.
126. Nakata J, Nakajima H, Sugiyama H, et al. Extremely strong infiltration of WT1-specific CTLs into mouse tumor by the combination vaccine with WT1-specific CTL and helper peptides. Oncotarget. 2018; 9: 36029.
127. Fujiki F, Oka Y, Kawakatsu M, Tsuboi A, Tanaka-Harada Y, Hosen N, Nishida S, Shirakata T, Nakajima H, Tatsumi N, Hashimoto N, Taguchi T, Ueda S, Nonomura N, Takeda Y, Ito T, Myoui A, Izumoto S, Maruno M, Yoshimine T, Noguchi S, Okuyama A, Kawase I, Oji Y, Sugiyama H. A clear correlation between WT1-specific Th response and clinical response in WT1 CTL epitope vaccination. Anticancer Res. 2010; 30: 2247-2254.
128. Takahara A, Koido S, Ito M, Nagasaki E, Sagawa Y, Iwamoto T, Komita H, Ochi T, Fujiwara H, Yasukawa M, Mineno J, Shiku H, Nishida S, Sugiyama H, Tajiri H, Homma S. Gemcitabine enhances Wilms' tumor gene WT1 expression and sensitizes human pancreatic cancer cells with WT1-specific T-cell-mediated antitumor immune response. Cancer Immunol Immunother. 2011; 60: 1289-1297.
129. Koido S, Kan S, Yoshida K, Yoshizaki S, Takakura K, Namiki Y, Tsukinaga S, Odahara S, Kajihara M, Okamoto M, Ito M, Yusa SI, Gong J, Sugiyama H, Ohkusa T, Homma S, Tajiri H. Immunogenic Modulation of Cholangiocarcinoma Cells by Chemoimmunotherapy. Anticancer Res. 2014; 34: 6353-6362.
130. Smith PL, Yogaratnam Y, Samad M, Kasow S, Dalgleish AG. Effect of Gemcitabine based chemotherapy on the immunogenicity of pancreatic tumour cells and T-cells. Clin Transl Oncol. 2021; 23: 110-121.
131. Soeda A, Morita-Hoshi Y, Makiyama H, Morizane C, Ueno H, Ikeda M, Okusaka T, Yamagata S, Takahashi N, Hyodo I, Takaue Y, Heike Y. Regular dose of gemcitabine induces an increase in CD14+ monocytes and CD11c+ dendritic cells in patients with advanced pancreatic cancer. Jpn J Clin Oncol. 2009; 39: 797-806.
132. Zitvogel L, Apetoh L, Ghiringhelli F, Kroemer G. Immunological aspects of cancer chemotherapy. Nat Rev Immunol. 2008; 8: 59-73.
133. Bracci L, Schiavoni G, Sistigu A, Belardelli F. Immune-based mechanisms of cytotoxic chemotherapy: implications for the design of novel and rationale-based combined treatments against cancer. Cell Death Differ. 2014; 21: 15-25.
134. Pusuluri A, Wu D, Mitragotri S. J Control Release. Immunological consequences of chemotherapy: Single drugs, combination therapies and nanoparticle-based treatments. J Control Release. 2019; 305: 130-154.
135. Hashii Y, Sato-Miyashita E, Matsumura R, Kusuki S, Yoshida H, Ohta H, Hosen N, Tsuboi A, Oji Y, Oka Y, Sugiyama H, Ozono K. WT1 peptide vaccination following allogeneic stem cell transplantation in pediatric leukemic patients with high risk for relapse: successful maintenance of durable remission. Leukemia. 2012; 26: 530-532.
136. Maeda T, Hosen N, Fukushima K, Tsuboi A, Morimoto S, Matsui T, Sata H, Fujita J, Hasegawa K, Nishida S, Nakata J, Nakae Y, Takashima S, Nakajima H, Fujiki F, TatsumiN, Kondo T, Hino M, Oji Y, Oka Y, Kanakura Y, Kumanogoh A Sugiyama H. Maintenance of complete remission after allogeneic stem cell transplantation in leukemia patients treated with Wilms tumor 1 peptide vaccine. Blood Cancer J. 2013; e130. Doi: 10.1038/bcj.2013.29
137. Saito S, Yanagisawa R, Yoshikawa K, Higuchi Y, Koya T, Yoshizawa K, Tanaka M, Sakashita K, Kobayashi T, Kurata T, Hirabayashi K, Nakazawa Y, Shiohara M, Yonemitsu Y, Okamoto M, Sugiyama H, Koike K, Shimodaira S. Safety and tolerability of allogeneic dendritic cell vaccination with induction of Wilms tumor 1-specific T cells in a pediatric donor and pediatric patient with relapsed leukemia: a case report and review of the literature. Cytotherapy. 2015; 17: 330-335.
138. Ishikawa T, Fujii N, Imada M, Aoe M, Meguri Y, Inomata T, Nakashima H, Fujii K, Yoshida S, Nishimori H, Matsuoka KI, Kondo E, Maeda Y, Tanimoto M. Graft-versus-leukemia effect with a WT1-specific T-cell response induced by azacitidine and donor lymphocyte infusions after allogeneic hematopoietic stem cell transplantation. Cytotherapy. 2017, 19: 514-520.
139. Yokota C, Nakata J, Takano K, Nakajima H, Hayashibara H, Minagawa H, Chiba Y, Hirayama R, Kijima N, Kinoshita M, Hashii Y, Tsuboi A, Oka Y, Oji Y, Kumanogoh A, Sugiyama H, Kagawa N, Kishima H. Distinct difference in tumor-infiltrating immune cells between Wilms' tumor gene 1 peptide vaccine and anti-programmed cell death-1 antibody therapies. Neuro-Oncol Adv. 2021; 3:1-10.
140. Oji Y, Kitamura Y, Kamino E, Kitano A, Sawabata N, Inoue M, Mori M, Nakatsuka SI, Sakaguchi N, Miyazaki K, Nakamura M, Fukuda I, Nakamura J, Tatsumi N, Takakuwa T, Nishida S, Shirakata T, Hosen N, Tsuboi A, Nezu R, Maeda H, Oka Y, Kawase I, Aozasa K, Okumura M, Miyoshi S, Sugiyama H. WT1 IgG antibody for early detection of nonsmall cell lung cancer and as its prognostic factor. Int J Cancer. 2009; 125: 381-387.
141. Tada K, Kitano S, Shoji H, Nishimura T, Shimada Y, Nagashima K, Aoki K, Hiraoka N, Honma Y, Iwasa S, Okita N, Takashima A, Kato K, Yamada Y, Katayama N, Boku N, Heike Y, Hamaguchi T. Pretreatment Immune Status Correlates with Progression-Free Survival in Chemotherapy-Treated Metastatic Colorectal Cancer Patients. Cancer Immunol Res. 2016; 4: 592-599.
142. Pagès F, Mlecnik B, Marliot F, Bindea G, Ou FS, Bifulco C, Lugli A, Zlobec I, Rau TT, Berger MD, Nagtegaal ID, Börger EV, Hartmann A, Geppert C, Kolwelter J, Merkel S, Grützmann R, Eynde MVD, Mourin AJ, Kartheuser A, Léonard D, Remue C, Wang JY, Bavi P, Roehrl MHA, Ohashi PS, Nguyen LT, Han SJ, Gregor HLM, Bakhtiari SH, Wouters BG, Masucci GV, Andersson EK, Zavadova E, Vocka M, Spacek J, Petruzelka L, Konopasek B, Dundr P, Skalova H, Nemejcova K, Botti G, Tatangelo F, Delrio P, Ciliberto G, Maio M, Laghi L, Grizzi F, Fredriksen T, Buttard B, Angelova M, Vasaturo A, Maby P, Church SE, Angell HK, Lafontaine L, Bruni D, Sissy CE, Haicheur N, Kirilovsky A, Berger A, Lagorce C, Meyers JP, Paustian C, Feng Z, Merino CB, Dijkstra J, Water CVD , Vliet SVLV, Knijn N, Mușină AM, Scripcariu DV, Popivanova B, Xu M, Fujita T, Hazama S, Suzuki N, Nagano H, Okuno K, Torigoe T, Sato N, Furuhata T, Takemasa I, Itoh K, Patel PS, Vora HH, Shah B, Patel JB, Rajvik KN, Pandya SJ, Shukla SN, Wang Y, Zhang G, Kawakami Y, Marincola FM, Ascierto PA, Sargent DJ, Fox BA, Galon J. International validation of the consensus Immunoscore for the classification of colon cancer: a prognostic and accuracy study. Lancet. 2018; 391: 2128-2139.
143. Kitayama J, Yasuda K, Kawai K, Sunami E, Nagawa H. Circulating lymphocyte is an important determinant of the effectiveness of preoperative radiotherapy in advanced rectal cancer. BMC Cancer. 2011; 11: 64.
144. Yoshimoto Y, Suzuki Y, Mimura K, Ando K, Oike T, Sato H, Okonogi N, Maruyama T, Izawa S, Noda S, Fujii H, Kono K, Nakano T. Radiotherapy-induced anti-tumor immunity contributes to the therapeutic efficacy of irradiation and can be augmented by CTLA-4 blockade in a mouse model. PLOS One. 2014; 9: e92572.
145. Saito Y, Kitamura H, Hijikata A, Murasawa MT, Tanaka S, Takagi S, Uchida N, Suzuki N, Sone A, Najima Y, Ozawa H, Wake A, Taniguchi S, Shultz LD, Oharaand O, Ishikawa F. Identification of therapeutic targets for quiescent, chemotherapy-resistant human leukemia stem cells. Sci Transl Med. 2010; 17: 17-19.
146. Hosen N, Sonoda Y, Oji Y, Kimura T, Minamiguchi H, Tamaki H, Kawakami M, Asada M, Kanato K, Motomura M, Murakami M, Fujioka T, Masuda T, Kim EH, Tsuboi A, Oka Y, Soma T, Ogawa H, Sugiyama H. Very low frequencies of human normal CD34+ hematopoietic progenitor cells express the Wilms’ tumor gene WT1 at the levels comaprable to those in leukemia cells. Brit J Hematol. 2002; 116: 409-420.
147. Gerber J M, Kowalski L Q, Smith B D, Griffin C A, Vala M S, Collector M I, Perkins B, Zahurak M, Matsui W, Gocke C D, Sharkis S J, Levitsky H I, Jones R J. Characterization of chronic myeloid leukemia stem cells. Am J Hematol. 2011; 86: 31-37.
148. Kanato K, Hosen N, Yanagihara M, Nakagata N, Shirakata T, Nakazawa T, Nishida S, Tsuboi A, Kawakami M, Masuda T, Oka Y, Oji Y, Sugiyama H. The Wilms' tumor gene WT1 is a common marker of progenitor cells in fetal liver. Biochem Biophys Res Commun. 2005; 326: 836-843.