Alterations between Effective and Ineffective Multipotent Mesenchymal Stromal Cells Used for Acute Graft Versus Host Disease Prophylaxis
Main Article Content
Nina Drize
http://orcid.org/0000-0002-7150-0403
Nataliya Petinati
http://orcid.org/0000-0001-6591-3183
Irina Shupounova
http://orcid.org/0000-0003-1189-0283
Natalia Sats
http://orcid.org/0000-0002-1559-9381
Alexey Bigildeev
http://orcid.org/0000-0003-0215-9085
Larisa Kuzmina
http://orcid.org/0000-0001-6201-6276
Elena Parovichnikova
http://orcid.org/0000-0002-1825-0097
Valeriy Savchenko
http://orcid.org/0000-0001-8188-5557
http://orcid.org/0000-0002-7150-0403
Nataliya Petinati
http://orcid.org/0000-0001-6591-3183
Irina Shupounova
http://orcid.org/0000-0003-1189-0283
Natalia Sats
http://orcid.org/0000-0002-1559-9381
Alexey Bigildeev
http://orcid.org/0000-0003-0215-9085
Larisa Kuzmina
http://orcid.org/0000-0001-6201-6276
Elena Parovichnikova
http://orcid.org/0000-0002-1825-0097
Valeriy Savchenko
http://orcid.org/0000-0001-8188-5557
Abstract
Multipotent mesenchymal stromal cells (MSCs) are applied for prophylaxis of acute graft versus host disease (aGvHD) after allogeneic hematopoietic cell transplantation (allo-HCT). Not all samples of MSC used in National Research Center for Hematology were efficient for aGvHD prevention. The suitabilityof MSCs for aGvHD prophylaxis was studied. MSCs derived from the bone marrow of HCT donor were injected intravenously precisely at the moment of blood cell reconstitution. MSCs were cultivated for 3 passages. The characteristics of donor bone marrow samples including colony forming unit fibroblast (CFU-F) concentration, growth parameters of MSCs and the relative expression levels (REL) of different genes in them were analyzed. MSCs infusion induced a decrease in aGvHD development in patients with related and unrelated donors compared with the standard prophylaxis group. aGvHD prophylaxis with MSCs was ineffective in 13.5% of cases. In these MSC samples, a significant decrease in total cell production and the REL of CFH, FGFR1, PDGFRa and ICAM1 were observed. This study showed that MSCs injection resulted in a significant 2-fold decrease in aGvHD development compared with patients in the standard prophylaxis group. The effective MSC samples are characterized by higher total cell production and REL of CFH, FGFR1, PDGFRa and ICAM1 than ineffective.
Article Details
How to Cite
DRIZE, Nina et al.
Alterations between Effective and Ineffective Multipotent Mesenchymal Stromal Cells Used for Acute Graft Versus Host Disease Prophylaxis.
Medical Research Archives, [S.l.], v. 4, n. 1, june 2016.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/501>. Date accessed: 27 dec. 2024.
Keywords
aGvHD prophylaxis, MSC, CFU-F, gene expression
Section
Research Articles
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
Aggarwal, S., & Pittenger, M. F. (2005). Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood, 105(4), 1815–22. http://doi.org/10.1182/blood-2004-04-1559
Ankrum, J. A., Ong, J. F., & Karp, J. M. (2014). Mesenchymal stem cells: immune evasive, not immune privileged. Nature Biotechnology. http://doi.org/10.1038/nbt.2816
Appelbaum, F. R. (2003). The current status of hematopoietic cell transplantation. Annual Review of Medicine, 54, 491–512. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12414918
Arai, Y., Kondo, T., Yamazaki, H., Takenaka, K., Sugita, J., Kobayashi, T., … Teshima, T. (2016). Allogeneic unrelated bone marrow transplantation from older donors results in worse prognosis in recipients with aplastic anemia. Haematologica, 101(5), 644–52. http://doi.org/10.3324/haematol.2015.139469
Bigildeev, A. E., Zhironkina, O. A., Shipounova, I. N., Sats, N. V, Kotyashova, S. Y., & Drize, N. I. (2012). Clonal composition of human multipotent mesenchymal stromal cells. Experimental Hematology, 40(10), 847–56.e4. http://doi.org/10.1016/j.exphem.2012.06.006
Billingham, R. E. (1967). The biology of graft-versus-host reactions. Harvey lectures (Vol. 62). Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/4875305
Chomczynski, P., & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry, 162(1), 156–9. http://doi.org/10.1006/abio.1987.9999
Colter, D. C., Sekiya, I., & Prockop, D. J. (2001). Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proceedings of the National Academy of Sciences of the United States of America, 98(14), 7841–5. http://doi.org/10.1073/pnas.141221698
Deans, R. J., & Moseley, a B. (2000). Mesenchymal stem cells: biology and potential clinical uses. Experimental Hematology, 28(8), 875–84. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10989188
Fallarino, F., Grohmann, U., Vacca, C., Bianchi, R., Orabona, C., Spreca, A., … Puccetti, P. (2002). T cell apoptosis by tryptophan catabolism. Cell Death and Differentiation, 9(10), 1069–77. http://doi.org/10.1038/sj.cdd.4401073
Ferrara, J. L., Levy, R., & Chao, N. J. (1999). Pathophysiologic mechanisms of acute graft-vs.-host disease. Biology of Blood and Marrow Transplantation : Journal of the American Society for Blood and Marrow Transplantation, 5(6), 347–56. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10595812
Fong, T. A., & Mosmann, T. R. (1990). Alloreactive murine CD8+ T cell clones secrete the Th1 pattern of cytokines. Journal of Immunology (Baltimore, Md. : 1950), 144(5), 1744–52. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/2137843
Glucksberg, H., Storb, R., Fefer, A., Buckner, C. D., Neiman, P. E., Clift, R. A., … Thomas, E. D. (1974). Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation, 18(4), 295–304. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/4153799
Introna, M., & Rambaldi, A. (2015). Mesenchymal stromal cells for prevention and treatment of graft-versus-host disease: successes and hurdles. Current Opinion in Organ Transplantation, 20(1), 72–8. http://doi.org/10.1097/MOT.0000000000000158
Jones, B. J., & McTaggart, S. J. (2008). Immunosuppression by mesenchymal stromal cells: from culture to clinic. Experimental Hematology, 36(6), 733–41. http://doi.org/10.1016/j.exphem.2008.03.006
Kim, N., Im, K.-I., Lim, J.-Y., Jeon, E.-J., Nam, Y.-S., Kim, E.-J., & Cho, S.-G. (2013). Mesenchymal stem cells for the treatment and prevention of graft-versus-host disease: experiments and practice. Annals of Hematology, 92(10), 1295–308. http://doi.org/10.1007/s00277-013-1796-z
Kollman, C., Spellman, S. R., Zhang, M.-J., Hassebroek, A., Anasetti, C., Antin, J. H., … Eapen, M. (2016). The effect of donor characteristics on survival after unrelated donor transplantation for hematologic malignancy. Blood, 127(2), 260–7. http://doi.org/10.1182/blood-2015-08-663823
Kuzmina, L. A., Petinati, N. A., Parovichnikova, E. N., Lubimova, L. S., Gribanova, E. O., Gaponova, T. V, … Savchenko, V. G. (2012). Multipotent Mesenchymal Stromal Cells for the Prophylaxis of Acute Graft-versus-Host Disease-A Phase II Study. Stem Cells International, 2012, 968213. http://doi.org/10.1155/2012/968213
Kuzmina, L. A., Petinati, N. A., Shipounova, I. N., Sats, N. V., Bigildeev, A. E., Zezina, E. A., … Savchenko, V. G. (2015). Analysis of multipotent mesenchymal stromal cells used for acute graft-versus-host disease prophylaxis. European Journal of Haematology. http://doi.org/10.1111/ejh.12613
Kuzmina, L. A., Petinati, N. A., Shipounova, I. N., Sats, N. V, Bigildeev, A. E., Zezina, E. A., … Savchenko, V. G. (2015). Analysis of multipotent mesenchymal stromal cells used for acute graft-versus-host disease prophylaxis. European Journal of Haematology. http://doi.org/10.1111/ejh.12613
Lange, C., Cakiroglu, F., Spiess, A., Cappallo-obermann, H., Dierlamm, J., & Zander, A. R. (2007). Accelerated and Safe Expansion of Human Mesenchymal Stromal Cells in Animal Serum-Free Medium for Transplantation and Regenerative Medicine. J Cell Physiol., 8904(January), 18–26. http://doi.org/10.1002/JCP
Le Blanc, K., Rasmusson, I., Sundberg, B., Götherström, C., Hassan, M., Uzunel, M., & Ringdén, O. (2004). Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet, 363(9419), 1439–41. http://doi.org/10.1016/S0140-6736(04)16104-7
Maziarz, R. T., Devos, T., Bachier, C. R., Goldstein, S. C., Leis, J. F., Devine, S. M., … Lazarus, H. M. (2015). Single and Multiple Dose MultiStem (Multipotent Adult Progenitor Cell) Therapy Prophylaxis of Acute Graft-versus-Host Disease in Myeloablative Allogeneic Hematopoietic Cell Transplantation: A Phase 1 Trial. Biology of Blood and Marrow Transplantation, 21(4), 720–728. http://doi.org/10.1016/j.bbmt.2014.12.025
Meisel, R., Zibert, A., Laryea, M., Göbel, U., Däubener, W., & Dilloo, D. (2004). Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood, 103(12), 4619–21. http://doi.org/10.1182/blood-2003-11-3909
Menssen, A., Häupl, T., Sittinger, M., Delorme, B., Charbord, P., & Ringe, J. (2011). Differential gene expression profiling of human bone marrow-derived mesenchymal stem cells during adipogenic development. BMC Genomics, 12(1), 461. http://doi.org/10.1186/1471-2164-12-461
Prasad, V. K., Lucas, K. G., Kleiner, G. I., Talano, J. A. M., Jacobsohn, D., Broadwater, G., … Kurtzberg, J. (2011). Efficacy and safety of ex vivo cultured adult human mesenchymal stem cells (ProchymalTM) in pediatric patients with severe refractory acute graft-versus-host disease in a compassionate use study. Biology of Blood and Marrow Transplantation : Journal of the American Society for Blood and Marrow Transplantation, 17(4), 534–41. http://doi.org/10.1016/j.bbmt.2010.04.014
Prockop, D. J., Brenner, M., Fibbe, W. E., Horwitz, E., Le Blanc, K., Phinney, D. G., … Keating, A. (2010). Defining the risks of mesenchymal stromal cell therapy. Cytotherapy, 12(5), 576–8. http://doi.org/10.3109/14653249.2010.507330
Ren, G., Zhao, X., Zhang, L., Zhang, J., L’Huillier, A., Ling, W., … Shi, Y. (2010). Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. Journal of Immunology (Baltimore, Md. : 1950), 184(5), 2321–8. http://doi.org/10.4049/jimmunol.0902023
Ringdén, O., Uzunel, M., Rasmusson, I., Remberger, M., Sundberg, B., Lönnies, H., … Le Blanc, K. (2006a). Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation, 81(10), 1390–7. http://doi.org/10.1097/01.tp.0000214462.63943.14
Ringdén, O., Uzunel, M., Rasmusson, I., Remberger, M., Sundberg, B., Lönnies, H., … Le Blanc, K. (2006b). Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation, 81(10), 1390–7. http://doi.org/10.1097/01.tp.0000214462.63943.14
Rizk, M., Monaghan, M., Shorr, R., Kekre, N., Bredeson, C. N., & Allan, D. S. (2016). Heterogeneity in studies of mesenchymal stromal cells to treat or prevent GVHD: a scoping review of the evidence. Biology of Blood and Marrow Transplantation : Journal of the American Society for Blood and Marrow Transplantation. http://doi.org/10.1016/j.bbmt.2016.04.010
Samsonraj, R. M., Rai, B., Sathiyanathan, P., Puan, K. J., Rötzschke, O., Hui, J. H., … Cool, S. M. (2015). Establishing criteria for human mesenchymal stem cell potency. Stem Cells (Dayton, Ohio). http://doi.org/10.1002/stem.1982
Samuelsson, H., Ringdén, O., Lönnies, H., & Le Blanc, K. (2009). Optimizing in vitro conditions for immunomodulation and expansion of mesenchymal stromal cells. Cytotherapy, 11(2), 129–36. http://doi.org/10.1080/14653240802684194
Schmittgen, T. D., & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3(6), 1101–1108. http://doi.org/10.1038/nprot.2008.73
Schu, S., Nosov, M., O’Flynn, L., Shaw, G., Treacy, O., Barry, F., … Ritter, T. (2012). Immunogenicity of allogeneic mesenchymal stem cells. Journal of Cellular and Molecular Medicine, 16(9), 2094–103. http://doi.org/10.1111/j.1582-4934.2011.01509.x
Servais, S., Beguin, Y., Delens, L., Ehx, G., Fransolet, G., Hannon, M., … Baron, F. (2016). Novel approaches for preventing acute graft-versus-host disease after allogeneic hematopoietic stem cell transplantation. Expert Opinion on Investigational Drugs, 1–16. http://doi.org/10.1080/13543784.2016.1182498
Shi, Y., Hu, G., Su, J., Li, W., Chen, Q., Shou, P., … Ren, G. (2010). Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair. Cell Research, 20(5), 510–8. http://doi.org/10.1038/cr.2010.44
Shipounova, I. N., Petinati, N. A., Bigildeev, A. E., Sats, N. V., Drize, N. J., Kuzmina, L. A., … Savchenko, V. G. (2013). Hierarchy of mesenchymal stem cells: Comparison of multipotentmesenchymal stromal cells with fibroblast colony forming units. Journal of Biomedical Science and Engineering, 06(08), 66–73. http://doi.org/10.4236/jbise.2013.68A1007
Shipounova, I. N., Petinati, N. A., Bigildeev, A. E., Zezina, E. A., Drize, N. I., Kuzmina, L. A., … Savchenko, V. G. (2014). Analysis of results of acute graft-versus-host disease prophylaxis with donor multipotent mesenchymal stromal cells in patients with hemoblastoses after allogeneic bone marrow transplantation. Biochemistry (Moscow), 79(12), 1363–1370. http://doi.org/10.1134/S0006297914120104
Sivanathan, K. N., & Gronthos, S. (2014). Interferon-Gamma Modification of Mesenchymal Stem Cells : Implications of Autologous and Allogeneic Mesenchymal Stem Cell Therapy in Allotransplantation, (Dc). http://doi.org/10.1007/s12015-014-9495-2
Staunton, D. E., Dustin, M. L., Erickson, H. P., & Springer, T. A. (1990). The arrangement of the immunoglobulin-like domains of ICAM-1 and the binding sites for LFA-1 and rhinovirus. Cell, 61(2), 243–54. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1970514
Svinareva, D. A., Petrova, T. V., Shipunova, I. N., Momotiuk, K. S., Mikhaǐlova, E. A., & Drize, N. I. (2009). The study of parameters of mesenchymal stromal cells differentiation in donors and patients with aplastic anemia. Terapevticheskiǐ Arkhiv, 81(7), 66–70. Retrieved from http://www.scopus.com/inward/record.url?eid=2-s2.0-74249083051&partnerID=tZOtx3y1
Tu, Z., Li, Q., Bu, H., & Lin, F. (2010). Mesenchymal stem cells inhibit complement activation by secreting factor H. Stem Cells and Development, 19(11), 1803–9. http://doi.org/10.1089/scd.2009.0418
Vaes, B., Van’t Hof, W., Deans, R., & Pinxteren, J. (2012). Application of MultiStem(®) Allogeneic Cells for Immunomodulatory Therapy: Clinical Progress and Pre-Clinical Challenges in Prophylaxis for Graft Versus Host Disease. Frontiers in Immunology, 3(NOV), 345. http://doi.org/10.3389/fimmu.2012.00345
Visentainer, J. E. L., Lieber, S. R., Persoli, L. B. L., Vigorito, A. C., Aranha, F. J. P., de Brito Eid, K. A., … de Souza, C. A. (2003). Serum cytokine levels and acute graft-versus-host disease after HLA-identical hematopoietic stem cell transplantation. Experimental Hematology, 31(11), 1044–50. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/14585368
von Bahr, L., Sundberg, B., Lönnies, L., Sander, B., Karbach, H., Hägglund, H., … Ringdén, O. (2012). Long-term complications, immunologic effects, and role of passage for outcome in mesenchymal stromal cell therapy. Biology of Blood and Marrow Transplantation : Journal of the American Society for Blood and Marrow Transplantation, 18(4), 557–64. http://doi.org/10.1016/j.bbmt.2011.07.023
Welniak, L. A., Blazar, B. R., & Murphy, W. J. (2007). Immunobiology of allogeneic hematopoietic stem cell transplantation. Annual Review of Immunology, 25, 139–70. http://doi.org/10.1146/annurev.immunol.25.022106.141606
Zhang, B., Yin, Y., Lai, R. C., Tan, S. S., Choo, A. B. H., & Lim, S. K. (2014). Mesenchymal stem cells secrete immunologically active exosomes. Stem Cells and Development, 23(11), 1233–44. http://doi.org/10.1089/scd.2013.0479
Ankrum, J. A., Ong, J. F., & Karp, J. M. (2014). Mesenchymal stem cells: immune evasive, not immune privileged. Nature Biotechnology. http://doi.org/10.1038/nbt.2816
Appelbaum, F. R. (2003). The current status of hematopoietic cell transplantation. Annual Review of Medicine, 54, 491–512. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12414918
Arai, Y., Kondo, T., Yamazaki, H., Takenaka, K., Sugita, J., Kobayashi, T., … Teshima, T. (2016). Allogeneic unrelated bone marrow transplantation from older donors results in worse prognosis in recipients with aplastic anemia. Haematologica, 101(5), 644–52. http://doi.org/10.3324/haematol.2015.139469
Bigildeev, A. E., Zhironkina, O. A., Shipounova, I. N., Sats, N. V, Kotyashova, S. Y., & Drize, N. I. (2012). Clonal composition of human multipotent mesenchymal stromal cells. Experimental Hematology, 40(10), 847–56.e4. http://doi.org/10.1016/j.exphem.2012.06.006
Billingham, R. E. (1967). The biology of graft-versus-host reactions. Harvey lectures (Vol. 62). Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/4875305
Chomczynski, P., & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry, 162(1), 156–9. http://doi.org/10.1006/abio.1987.9999
Colter, D. C., Sekiya, I., & Prockop, D. J. (2001). Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of human marrow stromal cells. Proceedings of the National Academy of Sciences of the United States of America, 98(14), 7841–5. http://doi.org/10.1073/pnas.141221698
Deans, R. J., & Moseley, a B. (2000). Mesenchymal stem cells: biology and potential clinical uses. Experimental Hematology, 28(8), 875–84. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10989188
Fallarino, F., Grohmann, U., Vacca, C., Bianchi, R., Orabona, C., Spreca, A., … Puccetti, P. (2002). T cell apoptosis by tryptophan catabolism. Cell Death and Differentiation, 9(10), 1069–77. http://doi.org/10.1038/sj.cdd.4401073
Ferrara, J. L., Levy, R., & Chao, N. J. (1999). Pathophysiologic mechanisms of acute graft-vs.-host disease. Biology of Blood and Marrow Transplantation : Journal of the American Society for Blood and Marrow Transplantation, 5(6), 347–56. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10595812
Fong, T. A., & Mosmann, T. R. (1990). Alloreactive murine CD8+ T cell clones secrete the Th1 pattern of cytokines. Journal of Immunology (Baltimore, Md. : 1950), 144(5), 1744–52. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/2137843
Glucksberg, H., Storb, R., Fefer, A., Buckner, C. D., Neiman, P. E., Clift, R. A., … Thomas, E. D. (1974). Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation, 18(4), 295–304. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/4153799
Introna, M., & Rambaldi, A. (2015). Mesenchymal stromal cells for prevention and treatment of graft-versus-host disease: successes and hurdles. Current Opinion in Organ Transplantation, 20(1), 72–8. http://doi.org/10.1097/MOT.0000000000000158
Jones, B. J., & McTaggart, S. J. (2008). Immunosuppression by mesenchymal stromal cells: from culture to clinic. Experimental Hematology, 36(6), 733–41. http://doi.org/10.1016/j.exphem.2008.03.006
Kim, N., Im, K.-I., Lim, J.-Y., Jeon, E.-J., Nam, Y.-S., Kim, E.-J., & Cho, S.-G. (2013). Mesenchymal stem cells for the treatment and prevention of graft-versus-host disease: experiments and practice. Annals of Hematology, 92(10), 1295–308. http://doi.org/10.1007/s00277-013-1796-z
Kollman, C., Spellman, S. R., Zhang, M.-J., Hassebroek, A., Anasetti, C., Antin, J. H., … Eapen, M. (2016). The effect of donor characteristics on survival after unrelated donor transplantation for hematologic malignancy. Blood, 127(2), 260–7. http://doi.org/10.1182/blood-2015-08-663823
Kuzmina, L. A., Petinati, N. A., Parovichnikova, E. N., Lubimova, L. S., Gribanova, E. O., Gaponova, T. V, … Savchenko, V. G. (2012). Multipotent Mesenchymal Stromal Cells for the Prophylaxis of Acute Graft-versus-Host Disease-A Phase II Study. Stem Cells International, 2012, 968213. http://doi.org/10.1155/2012/968213
Kuzmina, L. A., Petinati, N. A., Shipounova, I. N., Sats, N. V., Bigildeev, A. E., Zezina, E. A., … Savchenko, V. G. (2015). Analysis of multipotent mesenchymal stromal cells used for acute graft-versus-host disease prophylaxis. European Journal of Haematology. http://doi.org/10.1111/ejh.12613
Kuzmina, L. A., Petinati, N. A., Shipounova, I. N., Sats, N. V, Bigildeev, A. E., Zezina, E. A., … Savchenko, V. G. (2015). Analysis of multipotent mesenchymal stromal cells used for acute graft-versus-host disease prophylaxis. European Journal of Haematology. http://doi.org/10.1111/ejh.12613
Lange, C., Cakiroglu, F., Spiess, A., Cappallo-obermann, H., Dierlamm, J., & Zander, A. R. (2007). Accelerated and Safe Expansion of Human Mesenchymal Stromal Cells in Animal Serum-Free Medium for Transplantation and Regenerative Medicine. J Cell Physiol., 8904(January), 18–26. http://doi.org/10.1002/JCP
Le Blanc, K., Rasmusson, I., Sundberg, B., Götherström, C., Hassan, M., Uzunel, M., & Ringdén, O. (2004). Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet, 363(9419), 1439–41. http://doi.org/10.1016/S0140-6736(04)16104-7
Maziarz, R. T., Devos, T., Bachier, C. R., Goldstein, S. C., Leis, J. F., Devine, S. M., … Lazarus, H. M. (2015). Single and Multiple Dose MultiStem (Multipotent Adult Progenitor Cell) Therapy Prophylaxis of Acute Graft-versus-Host Disease in Myeloablative Allogeneic Hematopoietic Cell Transplantation: A Phase 1 Trial. Biology of Blood and Marrow Transplantation, 21(4), 720–728. http://doi.org/10.1016/j.bbmt.2014.12.025
Meisel, R., Zibert, A., Laryea, M., Göbel, U., Däubener, W., & Dilloo, D. (2004). Human bone marrow stromal cells inhibit allogeneic T-cell responses by indoleamine 2,3-dioxygenase-mediated tryptophan degradation. Blood, 103(12), 4619–21. http://doi.org/10.1182/blood-2003-11-3909
Menssen, A., Häupl, T., Sittinger, M., Delorme, B., Charbord, P., & Ringe, J. (2011). Differential gene expression profiling of human bone marrow-derived mesenchymal stem cells during adipogenic development. BMC Genomics, 12(1), 461. http://doi.org/10.1186/1471-2164-12-461
Prasad, V. K., Lucas, K. G., Kleiner, G. I., Talano, J. A. M., Jacobsohn, D., Broadwater, G., … Kurtzberg, J. (2011). Efficacy and safety of ex vivo cultured adult human mesenchymal stem cells (ProchymalTM) in pediatric patients with severe refractory acute graft-versus-host disease in a compassionate use study. Biology of Blood and Marrow Transplantation : Journal of the American Society for Blood and Marrow Transplantation, 17(4), 534–41. http://doi.org/10.1016/j.bbmt.2010.04.014
Prockop, D. J., Brenner, M., Fibbe, W. E., Horwitz, E., Le Blanc, K., Phinney, D. G., … Keating, A. (2010). Defining the risks of mesenchymal stromal cell therapy. Cytotherapy, 12(5), 576–8. http://doi.org/10.3109/14653249.2010.507330
Ren, G., Zhao, X., Zhang, L., Zhang, J., L’Huillier, A., Ling, W., … Shi, Y. (2010). Inflammatory cytokine-induced intercellular adhesion molecule-1 and vascular cell adhesion molecule-1 in mesenchymal stem cells are critical for immunosuppression. Journal of Immunology (Baltimore, Md. : 1950), 184(5), 2321–8. http://doi.org/10.4049/jimmunol.0902023
Ringdén, O., Uzunel, M., Rasmusson, I., Remberger, M., Sundberg, B., Lönnies, H., … Le Blanc, K. (2006a). Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation, 81(10), 1390–7. http://doi.org/10.1097/01.tp.0000214462.63943.14
Ringdén, O., Uzunel, M., Rasmusson, I., Remberger, M., Sundberg, B., Lönnies, H., … Le Blanc, K. (2006b). Mesenchymal stem cells for treatment of therapy-resistant graft-versus-host disease. Transplantation, 81(10), 1390–7. http://doi.org/10.1097/01.tp.0000214462.63943.14
Rizk, M., Monaghan, M., Shorr, R., Kekre, N., Bredeson, C. N., & Allan, D. S. (2016). Heterogeneity in studies of mesenchymal stromal cells to treat or prevent GVHD: a scoping review of the evidence. Biology of Blood and Marrow Transplantation : Journal of the American Society for Blood and Marrow Transplantation. http://doi.org/10.1016/j.bbmt.2016.04.010
Samsonraj, R. M., Rai, B., Sathiyanathan, P., Puan, K. J., Rötzschke, O., Hui, J. H., … Cool, S. M. (2015). Establishing criteria for human mesenchymal stem cell potency. Stem Cells (Dayton, Ohio). http://doi.org/10.1002/stem.1982
Samuelsson, H., Ringdén, O., Lönnies, H., & Le Blanc, K. (2009). Optimizing in vitro conditions for immunomodulation and expansion of mesenchymal stromal cells. Cytotherapy, 11(2), 129–36. http://doi.org/10.1080/14653240802684194
Schmittgen, T. D., & Livak, K. J. (2008). Analyzing real-time PCR data by the comparative CT method. Nature Protocols, 3(6), 1101–1108. http://doi.org/10.1038/nprot.2008.73
Schu, S., Nosov, M., O’Flynn, L., Shaw, G., Treacy, O., Barry, F., … Ritter, T. (2012). Immunogenicity of allogeneic mesenchymal stem cells. Journal of Cellular and Molecular Medicine, 16(9), 2094–103. http://doi.org/10.1111/j.1582-4934.2011.01509.x
Servais, S., Beguin, Y., Delens, L., Ehx, G., Fransolet, G., Hannon, M., … Baron, F. (2016). Novel approaches for preventing acute graft-versus-host disease after allogeneic hematopoietic stem cell transplantation. Expert Opinion on Investigational Drugs, 1–16. http://doi.org/10.1080/13543784.2016.1182498
Shi, Y., Hu, G., Su, J., Li, W., Chen, Q., Shou, P., … Ren, G. (2010). Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair. Cell Research, 20(5), 510–8. http://doi.org/10.1038/cr.2010.44
Shipounova, I. N., Petinati, N. A., Bigildeev, A. E., Sats, N. V., Drize, N. J., Kuzmina, L. A., … Savchenko, V. G. (2013). Hierarchy of mesenchymal stem cells: Comparison of multipotentmesenchymal stromal cells with fibroblast colony forming units. Journal of Biomedical Science and Engineering, 06(08), 66–73. http://doi.org/10.4236/jbise.2013.68A1007
Shipounova, I. N., Petinati, N. A., Bigildeev, A. E., Zezina, E. A., Drize, N. I., Kuzmina, L. A., … Savchenko, V. G. (2014). Analysis of results of acute graft-versus-host disease prophylaxis with donor multipotent mesenchymal stromal cells in patients with hemoblastoses after allogeneic bone marrow transplantation. Biochemistry (Moscow), 79(12), 1363–1370. http://doi.org/10.1134/S0006297914120104
Sivanathan, K. N., & Gronthos, S. (2014). Interferon-Gamma Modification of Mesenchymal Stem Cells : Implications of Autologous and Allogeneic Mesenchymal Stem Cell Therapy in Allotransplantation, (Dc). http://doi.org/10.1007/s12015-014-9495-2
Staunton, D. E., Dustin, M. L., Erickson, H. P., & Springer, T. A. (1990). The arrangement of the immunoglobulin-like domains of ICAM-1 and the binding sites for LFA-1 and rhinovirus. Cell, 61(2), 243–54. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/1970514
Svinareva, D. A., Petrova, T. V., Shipunova, I. N., Momotiuk, K. S., Mikhaǐlova, E. A., & Drize, N. I. (2009). The study of parameters of mesenchymal stromal cells differentiation in donors and patients with aplastic anemia. Terapevticheskiǐ Arkhiv, 81(7), 66–70. Retrieved from http://www.scopus.com/inward/record.url?eid=2-s2.0-74249083051&partnerID=tZOtx3y1
Tu, Z., Li, Q., Bu, H., & Lin, F. (2010). Mesenchymal stem cells inhibit complement activation by secreting factor H. Stem Cells and Development, 19(11), 1803–9. http://doi.org/10.1089/scd.2009.0418
Vaes, B., Van’t Hof, W., Deans, R., & Pinxteren, J. (2012). Application of MultiStem(®) Allogeneic Cells for Immunomodulatory Therapy: Clinical Progress and Pre-Clinical Challenges in Prophylaxis for Graft Versus Host Disease. Frontiers in Immunology, 3(NOV), 345. http://doi.org/10.3389/fimmu.2012.00345
Visentainer, J. E. L., Lieber, S. R., Persoli, L. B. L., Vigorito, A. C., Aranha, F. J. P., de Brito Eid, K. A., … de Souza, C. A. (2003). Serum cytokine levels and acute graft-versus-host disease after HLA-identical hematopoietic stem cell transplantation. Experimental Hematology, 31(11), 1044–50. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/14585368
von Bahr, L., Sundberg, B., Lönnies, L., Sander, B., Karbach, H., Hägglund, H., … Ringdén, O. (2012). Long-term complications, immunologic effects, and role of passage for outcome in mesenchymal stromal cell therapy. Biology of Blood and Marrow Transplantation : Journal of the American Society for Blood and Marrow Transplantation, 18(4), 557–64. http://doi.org/10.1016/j.bbmt.2011.07.023
Welniak, L. A., Blazar, B. R., & Murphy, W. J. (2007). Immunobiology of allogeneic hematopoietic stem cell transplantation. Annual Review of Immunology, 25, 139–70. http://doi.org/10.1146/annurev.immunol.25.022106.141606
Zhang, B., Yin, Y., Lai, R. C., Tan, S. S., Choo, A. B. H., & Lim, S. K. (2014). Mesenchymal stem cells secrete immunologically active exosomes. Stem Cells and Development, 23(11), 1233–44. http://doi.org/10.1089/scd.2013.0479