Potential Links Between YB-1 and Fatty Acid Synthesis in Clear Cell Renal Carcinoma
Main Article Content
Abstract
According to the National Institutes of Health, clear cell renal cell carcinoma (ccRCC) is the most common type of Renal Cell Carcinoma (RCC), making up approximately 75% of total renal carcinoma cases. Clear cell Renal Cell Carcinoma is characterized by a significant accumulation of lipids in the cytoplasm, which allows light from microscopes to pass through giving them a “clear” phenotype. Many of these lipids are in the form of fatty acids, both free and incorporated into lipid droplets. RCC is typically associated with a poor prognosis due to the lack of specific symptoms. Some symptoms include blood in urine, fever, lump on the side, weight loss, fatigue, to name a few; all of which can be associated with non-specific, non-cancerous, health conditions that contribute to difficult diagnosis. Treatment of RCC has typically been centered around radical nephrectomy as the standard of care, but due to the potentially small size of lesions and the possibility of causing surgically induced chronic kidney disease, treatments have shifted to more cautious, less invasive approaches. These approaches include active surveillance, nephron-sparing surgery, and other minimally invasive techniques like cryotherapy and renal ablation. Although these techniques have had the desired effect of reducing the number of surgeries, there is still considerable potential for renal impairment and the chance that tumors can grow out of control without surgery. With the difficulty that surrounds the treatment of ccRCC and its considerably high mortality rate amongst urological cancers, it is important to look for novel approaches to improve patient outcomes. This review looks at available literature and our data that suggests the lipogenic enzyme stearoyl-CoA desaturase may be more beneficial to patient survival than once thought. As our understanding of the importance of lipids in cell metabolism and longevity matures, it is important to present new perspectives that present a new understanding of ccRCC and the role of lipids in survival mechanisms engaged by transformed cells during cancer progression.
In this review, we provide evidence that pharmacological inhibition of lipid desaturation in renal cancer patients is not without risk, and that the presence of unsaturated fatty acids may be a beneficial factor in patient outcomes. Although more direct experimental evidence is needed to make definitive conclusions, it is clear that the work reviewed herein should challenge our current understanding of cancer biology and may inform novel approaches to the diagnosis and treatment of ccRCC.
Keywords:
YB-1, ccRCC, SCD1, MUFA, cancer, lipid metabolism, TCGA, kidney
Article Details
How to Cite
MCAULEY, Carter et al.
Potential Links Between YB-1 and Fatty Acid Synthesis in Clear Cell Renal Carcinoma.
Medical Research Archives, [S.l.], v. 8, n. 10, oct. 2020.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/2273>. Date accessed: 18 nov. 2024.
doi: https://doi.org/10.18103/mra.v8i10.2273.
Section
Review 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
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10. Qiu B, Ackerman D, Sanchez DJ, et al. HIF2alpha-Dependent Lipid Storage Promotes Endoplasmic Reticulum Homeostasis in Clear-Cell Renal Cell Carcinoma. Cancer Discov. 2015;5(6):652-667.
11. Wise DR, DeBerardinis RJ, Mancuso A, et al. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci U S A. 2008;105(48):18782-18787.
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13. DeNicola GM, Cantley LC. Cancer's Fuel Choice: New Flavors for a Picky Eater. Mol Cell. 2015;60(4):514-523.
14. Li Z, Kang Y. Lipid Metabolism Fuels Cancer's Spread. Cell Metab. 2017;25(2):228-230.
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16. Aljohani A, Khan MI, Bonneville A, et al. Hepatic stearoyl CoA desaturase 1 deficiency increases glucose uptake in adipose tissue partially through the PGC-1alpha-FGF21 axis in mice. J Biol Chem. 2019;294(51):19475-19485.
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19. Igal RA. Stearoyl-CoA desaturase-1: a novel key player in the mechanisms of cell proliferation, programmed cell death and transformation to cancer. Carcinogenesis. 2010;31(9):1509-1515.
20. Spector AA. The importance of free fatty acid in tumor nutrition. Cancer Res. 1967;27(9):1580-1586.
21. Peck B, Schug ZT, Zhang Q, et al. Inhibition of fatty acid desaturation is detrimental to cancer cell survival in metabolically compromised environments. Cancer and Metabolism. 2016;4(1).
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26. Kikuchi K, Tsukamoto H. Stearoyl-CoA desaturase and tumorigenesis. Chemico-Biological Interactions. 2020;316:108917.
27. Koeberle A, Löser K, Thürmer M. Stearoyl-CoA desaturase-1 and adaptive stress signaling. Biochim Biophys Acta. 2016;1861(11):1719-1726.
28. Paton CM, Ntambi JM. Biochemical and physiological function of stearoyl-CoA desaturase. Am J Physiol Endocrinol Metab. 2009;297(1):E28-37.
29. Sampath H, Miyazaki M, Dobrzyn A, Ntambi JM. Stearoyl-CoA desaturase-1 mediates the pro-lipogenic effects of dietary saturated fat. J Biol Chem. 2007;282(4):2483-2493.
30. Igal RA. Stearoyl CoA desaturase-1: New insights into a central regulator of cancer metabolism. Biochim Biophys Acta. 2016;1861(12 Pt A):1865-1880.
31. Song Y, Zhong L, Zhou J, et al. Data-Independent Acquisition-Based Quantitative Proteomic Analysis Reveals Potential Biomarkers of Kidney Cancer. Proteomics Clin Appl. 2017;11(11-12).
32. Cao Q, Ruan H, Wang K, et al. Overexpression of PLIN2 is a prognostic marker and attenuates tumor progression in clear cell renal cell carcinoma. Int J Oncol. 2018;53(1):137-147.
33. Yao M, Huang Y, Shioi K, et al. Expression of adipose differentiation-related protein: a predictor of cancer-specific survival in clear cell renal carcinoma. Clin Cancer Res. 2007;13(1):152-160.
34. Tun HW, Marlow LA, von Roemeling CA, et al. Pathway signature and cellular differentiation in clear cell renal cell carcinoma. PLoS One. 2010;5(5):e10696.
35. Wang Y, Su J, Fu D, et al. The Role of YB1 in Renal Cell Carcinoma Cell Adhesion. Int J Med Sci. 2018;15(12):1304-1311.
36. Wang Y, Chen Y, Geng H, Qi C, Liu Y, Yue D. Overexpression of YB1 and EZH2 are associated with cancer metastasis and poor prognosis in renal cell carcinomas. Tumour Biol. 2015;36(9):7159-7166.
37. Cohen SB, Ma W, Valova VA, et al. Genotoxic stress-induced nuclear localization of oncoprotein YB-1 in the absence of proteolytic processing. Oncogene. 2010;29(3):403-410.
38. Yadav BS, Singh S, Shaw AK, Mani A. Structure prediction and docking-based molecular insights of human YB-1 and nucleic acid interaction. J Biomol Struct Dyn. 2016;34(12):2561-2580.
39. Kang S, Lee TA, Ra EA, et al. Differential control of interleukin-6 mRNA levels by cellular distribution of YB-1. PLoS One. 2014;9(11):e112754.
40. Guryanov SG, Filimonov VV, Timchenko AA, et al. The major mRNP protein YB-1: structural and association properties in solution. Biochim Biophys Acta. 2013;1834(2):559-567.
41. Kljashtorny V, Nikonov S, Ovchinnikov L, et al. The Cold Shock Domain of YB-1 Segregates RNA from DNA by Non-Bonded Interactions. PLoS One. 2015;10(7):e0130318.
42. Yang X-J, Zhu H, Mu S-R, et al. Crystal structure of a Y-box binding protein 1 (YB-1)-RNA complex reveals key features and residues interacting with RNA. J Biol Chem. 2019;294(28):10998-11010.
43. Okamoto T, Izumi H, Imamura T, et al. Direct interaction of p53 with the Y-box binding protein, YB-1: a mechanism for regulation of human gene expression. Oncogene. 2000;19(54):6194-6202.
44. Sutherland BW, Kucab J, Wu J, et al. Akt phosphorylates the Y-box binding protein 1 at Ser102 located in the cold shock domain and affects the anchorage-independent growth of breast cancer cells. Oncogene. 2005;24(26):4281-4292.
45. Holm PS, Bergmann S, Jurchott K, et al. YB-1 relocates to the nucleus in adenovirus-infected cells and facilitates viral replication by inducing E2 gene expression through the E2 late promoter. J Biol Chem. 2002;277(12):10427-10434.
46. Stein U, Jürchott K, Walther W, Bergmann S, Schlag PM, Royer HD. Hyperthermia-induced nuclear translocation of transcription factor YB-1 leads to enhanced expression of multidrug resistance-related ABC transporters. J Biol Chem. 2001;276(30):28562-28569.
47. Astanehe A, Finkbeiner M, To K, Dunn SE. The Transcription Factor Y-Box Binding Protein-1 (Yb-1) Induces Expression of the Pik3ca Oncogene Leading to Increased Invasion Ofbasal-Like Breast Carcinoma Cells. Clinical & Investigative Medicine. 2008;31(4):3.
48. Higashi K, Inagaki Y, Suzuki N, et al. Y-box-binding Protein YB-1 Mediates Transcriptional Repression of Human α2(I) Collagen Gene Expression by Interferon-γ. Journal of Biological Chemistry. 2003;278(7):5156-5162.
49. Coles LS, Lambrusco L, Burrows J, et al. Phosphorylation of cold shock domain/Y-box proteins by ERK2 and GSK3beta and repression of the human VEGF promoter. FEBS Lett. 2005;579(24):5372-5378.
50. Chatterjee M, Rancso C, Stühmer T, et al. The Y-box binding protein YB-1 is associated with progressive disease and mediates survival and drug resistance in multiple myeloma. Blood. 2008;111(7):3714-3722.
51. Evdokimova V, Tognon C, Ng T, et al. Translational activation of snail1 and other developmentally regulated transcription factors by YB-1 promotes an epithelial-mesenchymal transition. Cancer Cell. 2009;15(5):402-415.
52. Ha B, Lee EB, Cui J, Kim Y, Jang HH. YB-1 overexpression promotes a TGF-beta1-induced epithelial-mesenchymal transition via Akt activation. Biochem Biophys Res Commun. 2015;458(2):347-351.
53. Harada M, Kotake Y, Ohhata T, et al. YB-1 promotes transcription of cyclin D1 in human non-small-cell lung cancers. Genes Cells. 2014;19(6):504-516.
54. Sutherland BW, Kucab J, Wu J, et al. Akt phosphorylates the Y-box binding protein 1 at Ser102 located in the cold shock domain and affects the anchorage-independent growth of breast cancer cells. Oncogene. 2005;24(26):4281-4292.
55. Somasekharan SP, El-Naggar A, Leprivier G, et al. YB-1 regulates stress granule formation and tumor progression by translationally activating G3BP1. J Cell Biol. 2015;208(7):913-929.
56. Lee C, Dhillon J, Wang MYC, et al. Targeting YB-1 in HER-2 overexpressing breast cancer cells induces apoptosis via the mTOR/STAT3 pathway and suppresses tumor growth in mice. Cancer Res. 2008;68(21):8661-8666.
57. Liang C, Ma Y, Yong L, et al. Y-box binding protein-1 promotes tumorigenesis and progression via the epidermal growth factor receptor/AKT pathway in spinal chordoma. Cancer Sci. 2019;110(1):166-179.
58. Bargou RC, Jürchott K, Wagener C, et al. Nuclear localization and increased levels of transcription factor YB-1 in primary human breast cancers are associated with intrinsic MDR1 gene expression. Nat Med. 1997;3(4):447-450.
59. D'Costa NM, Lowerison MR, Raven PA, et al. Y-box binding protein-1 is crucial in acquired drug resistance development in metastatic clear-cell renal cell carcinoma. J Exp Clin Cancer Res. 2020;39(1):33.
60. Homer C, Knight DA, Hananeia L, et al. Y-box factor YB1 controls p53 apoptotic function. Oncogene. 2005;24(56):8314-8325.
61. Evdokimova VM, Ovchinnikov LP. Translational regulation by Y-box transcription factor: involvement of the major mRNA-associated protein, p50. Int J Biochem Cell Biol. 1999;31(1):139-149.
62. Stickeler E, Fraser SD, Honig A, Chen AL, Berget SM, Cooper TA. The RNA binding protein YB-1 binds A/C-rich exon enhancers and stimulates splicing of the CD44 alternative exon v4. EMBO J. 2001;20(14):3821-3830.
63. Li J, Hawkins IC, Harvey CD, Jennings JL, Link AJ, Patton JG. Regulation of alternative splicing by SRrp86 and its interacting proteins. Mol Cell Biol. 2003;23(21):7437-7447.
64. Kromhout D, Menotti A, Alberti-Fidanza A, et al. Comparative ecologic relationships of saturated fat, sucrose, food groups, and a Mediterranean food pattern score to 50-year coronary heart disease mortality rates among 16 cohorts of the Seven Countries Study. Eur J Clin Nutr. 2018;72(8):1103-1110.
2. Zhang P, Ro JY. Renal cell carcinoma. annals of urologic oncology. 2018;1(1):1-18.
3. Cairns P. Renal cell carcinoma. Cancer Biomark. 2010;9(1-6):461-473.
4. Rini BI, Campbell SC, Escudier B. Renal cell carcinoma. Lancet. 2009;373(9669):1119-1132.
5. Brannon AR, Reddy A, Seiler M, et al. Molecular Stratification of Clear Cell Renal Cell Carcinoma by Consensus Clustering Reveals Distinct Subtypes and Survival Patterns. Genes Cancer. 2010;1(2):152-163.
6. Yao M, Tabuchi H, Nagashima Y, et al. Gene expression analysis of renal carcinoma: adipose differentiation-related protein as a potential diagnostic and prognostic biomarker for clear-cell renal carcinoma. J Pathol. 2005;205(3):377-387.
7. Jeffords EF, Samuel; Cole, Breanna; Root, Kate; Chekouo, Thierry; Melvin, Richard G.; Bemis, Lynne; Simmons Jr, Glenn E. . Y‑box binding protein 1 acts as a negative regulator of stearoyl CoA desaturase 1 in clear cell renal cell carcinoma. Oncology Letters 2020;20(5).
8. Gnarra JR, Tory K, Weng Y, et al. Mutations of the VHL tumour suppressor gene in renal carcinoma. Nat Genet. 1994;7(1):85-90.
9. Kuroda N, Hosokawa T, Michal M, et al. Clear cell renal cell carcinoma with focal renal angiomyoadenomatous tumor-like area. Ann Diagn Pathol. 2011;15(3):202-206.
10. Qiu B, Ackerman D, Sanchez DJ, et al. HIF2alpha-Dependent Lipid Storage Promotes Endoplasmic Reticulum Homeostasis in Clear-Cell Renal Cell Carcinoma. Cancer Discov. 2015;5(6):652-667.
11. Wise DR, DeBerardinis RJ, Mancuso A, et al. Myc regulates a transcriptional program that stimulates mitochondrial glutaminolysis and leads to glutamine addiction. Proc Natl Acad Sci U S A. 2008;105(48):18782-18787.
12. Wise DR, Thompson CB. Glutamine addiction: a new therapeutic target in cancer. Trends Biochem Sci. 2010;35(8):427-433.
13. DeNicola GM, Cantley LC. Cancer's Fuel Choice: New Flavors for a Picky Eater. Mol Cell. 2015;60(4):514-523.
14. Li Z, Kang Y. Lipid Metabolism Fuels Cancer's Spread. Cell Metab. 2017;25(2):228-230.
15. Braig S. Chemical genetics in tumor lipogenesis. Biotechnol Adv. 2018;36(6):1724-1729.
16. Aljohani A, Khan MI, Bonneville A, et al. Hepatic stearoyl CoA desaturase 1 deficiency increases glucose uptake in adipose tissue partially through the PGC-1alpha-FGF21 axis in mice. J Biol Chem. 2019;294(51):19475-19485.
17. Ameer F, Scandiuzzi L, Hasnain S, Kalbacher H, Zaidi N. De novo lipogenesis in health and disease. Metabolism. 2014;63(7):895-902.
18. Iida T, Ubukata M, Mitani I, et al. Discovery of potent liver-selective stearoyl-CoA desaturase-1 (SCD1) inhibitors, thiazole-4-acetic acid derivatives, for the treatment of diabetes, hepatic steatosis, and obesity. Eur J Med Chem. 2018;158:832-852.
19. Igal RA. Stearoyl-CoA desaturase-1: a novel key player in the mechanisms of cell proliferation, programmed cell death and transformation to cancer. Carcinogenesis. 2010;31(9):1509-1515.
20. Spector AA. The importance of free fatty acid in tumor nutrition. Cancer Res. 1967;27(9):1580-1586.
21. Peck B, Schug ZT, Zhang Q, et al. Inhibition of fatty acid desaturation is detrimental to cancer cell survival in metabolically compromised environments. Cancer and Metabolism. 2016;4(1).
22. Takahashi M, Rhodes DR, Furge KA, et al. Gene expression profiling of clear cell renal cell carcinoma: gene identification and prognostic classification. Proc Natl Acad Sci U S A. 2001;98(17):9754-9759.
23. Saito K, Arai E, Maekawa K, et al. Lipidomic Signatures and Associated Transcriptomic Profiles of Clear Cell Renal Cell Carcinoma. Sci Rep. 2016;6:28932.
24. Zhao Z, Liu Y, Liu Q, et al. The mRNA Expression Signature and Prognostic Analysis of Multiple Fatty Acid Metabolic Enzymes in Clear Cell Renal Cell Carcinoma. J Cancer. 2019;10(26):6599-6607.
25. von Roemeling CA, Marlow LA, Wei JJ, et al. Stearoyl-CoA desaturase 1 is a novel molecular therapeutic target for clear cell renal cell carcinoma. Clin Cancer Res. 2013;19(9):2368-2380.
26. Kikuchi K, Tsukamoto H. Stearoyl-CoA desaturase and tumorigenesis. Chemico-Biological Interactions. 2020;316:108917.
27. Koeberle A, Löser K, Thürmer M. Stearoyl-CoA desaturase-1 and adaptive stress signaling. Biochim Biophys Acta. 2016;1861(11):1719-1726.
28. Paton CM, Ntambi JM. Biochemical and physiological function of stearoyl-CoA desaturase. Am J Physiol Endocrinol Metab. 2009;297(1):E28-37.
29. Sampath H, Miyazaki M, Dobrzyn A, Ntambi JM. Stearoyl-CoA desaturase-1 mediates the pro-lipogenic effects of dietary saturated fat. J Biol Chem. 2007;282(4):2483-2493.
30. Igal RA. Stearoyl CoA desaturase-1: New insights into a central regulator of cancer metabolism. Biochim Biophys Acta. 2016;1861(12 Pt A):1865-1880.
31. Song Y, Zhong L, Zhou J, et al. Data-Independent Acquisition-Based Quantitative Proteomic Analysis Reveals Potential Biomarkers of Kidney Cancer. Proteomics Clin Appl. 2017;11(11-12).
32. Cao Q, Ruan H, Wang K, et al. Overexpression of PLIN2 is a prognostic marker and attenuates tumor progression in clear cell renal cell carcinoma. Int J Oncol. 2018;53(1):137-147.
33. Yao M, Huang Y, Shioi K, et al. Expression of adipose differentiation-related protein: a predictor of cancer-specific survival in clear cell renal carcinoma. Clin Cancer Res. 2007;13(1):152-160.
34. Tun HW, Marlow LA, von Roemeling CA, et al. Pathway signature and cellular differentiation in clear cell renal cell carcinoma. PLoS One. 2010;5(5):e10696.
35. Wang Y, Su J, Fu D, et al. The Role of YB1 in Renal Cell Carcinoma Cell Adhesion. Int J Med Sci. 2018;15(12):1304-1311.
36. Wang Y, Chen Y, Geng H, Qi C, Liu Y, Yue D. Overexpression of YB1 and EZH2 are associated with cancer metastasis and poor prognosis in renal cell carcinomas. Tumour Biol. 2015;36(9):7159-7166.
37. Cohen SB, Ma W, Valova VA, et al. Genotoxic stress-induced nuclear localization of oncoprotein YB-1 in the absence of proteolytic processing. Oncogene. 2010;29(3):403-410.
38. Yadav BS, Singh S, Shaw AK, Mani A. Structure prediction and docking-based molecular insights of human YB-1 and nucleic acid interaction. J Biomol Struct Dyn. 2016;34(12):2561-2580.
39. Kang S, Lee TA, Ra EA, et al. Differential control of interleukin-6 mRNA levels by cellular distribution of YB-1. PLoS One. 2014;9(11):e112754.
40. Guryanov SG, Filimonov VV, Timchenko AA, et al. The major mRNP protein YB-1: structural and association properties in solution. Biochim Biophys Acta. 2013;1834(2):559-567.
41. Kljashtorny V, Nikonov S, Ovchinnikov L, et al. The Cold Shock Domain of YB-1 Segregates RNA from DNA by Non-Bonded Interactions. PLoS One. 2015;10(7):e0130318.
42. Yang X-J, Zhu H, Mu S-R, et al. Crystal structure of a Y-box binding protein 1 (YB-1)-RNA complex reveals key features and residues interacting with RNA. J Biol Chem. 2019;294(28):10998-11010.
43. Okamoto T, Izumi H, Imamura T, et al. Direct interaction of p53 with the Y-box binding protein, YB-1: a mechanism for regulation of human gene expression. Oncogene. 2000;19(54):6194-6202.
44. Sutherland BW, Kucab J, Wu J, et al. Akt phosphorylates the Y-box binding protein 1 at Ser102 located in the cold shock domain and affects the anchorage-independent growth of breast cancer cells. Oncogene. 2005;24(26):4281-4292.
45. Holm PS, Bergmann S, Jurchott K, et al. YB-1 relocates to the nucleus in adenovirus-infected cells and facilitates viral replication by inducing E2 gene expression through the E2 late promoter. J Biol Chem. 2002;277(12):10427-10434.
46. Stein U, Jürchott K, Walther W, Bergmann S, Schlag PM, Royer HD. Hyperthermia-induced nuclear translocation of transcription factor YB-1 leads to enhanced expression of multidrug resistance-related ABC transporters. J Biol Chem. 2001;276(30):28562-28569.
47. Astanehe A, Finkbeiner M, To K, Dunn SE. The Transcription Factor Y-Box Binding Protein-1 (Yb-1) Induces Expression of the Pik3ca Oncogene Leading to Increased Invasion Ofbasal-Like Breast Carcinoma Cells. Clinical & Investigative Medicine. 2008;31(4):3.
48. Higashi K, Inagaki Y, Suzuki N, et al. Y-box-binding Protein YB-1 Mediates Transcriptional Repression of Human α2(I) Collagen Gene Expression by Interferon-γ. Journal of Biological Chemistry. 2003;278(7):5156-5162.
49. Coles LS, Lambrusco L, Burrows J, et al. Phosphorylation of cold shock domain/Y-box proteins by ERK2 and GSK3beta and repression of the human VEGF promoter. FEBS Lett. 2005;579(24):5372-5378.
50. Chatterjee M, Rancso C, Stühmer T, et al. The Y-box binding protein YB-1 is associated with progressive disease and mediates survival and drug resistance in multiple myeloma. Blood. 2008;111(7):3714-3722.
51. Evdokimova V, Tognon C, Ng T, et al. Translational activation of snail1 and other developmentally regulated transcription factors by YB-1 promotes an epithelial-mesenchymal transition. Cancer Cell. 2009;15(5):402-415.
52. Ha B, Lee EB, Cui J, Kim Y, Jang HH. YB-1 overexpression promotes a TGF-beta1-induced epithelial-mesenchymal transition via Akt activation. Biochem Biophys Res Commun. 2015;458(2):347-351.
53. Harada M, Kotake Y, Ohhata T, et al. YB-1 promotes transcription of cyclin D1 in human non-small-cell lung cancers. Genes Cells. 2014;19(6):504-516.
54. Sutherland BW, Kucab J, Wu J, et al. Akt phosphorylates the Y-box binding protein 1 at Ser102 located in the cold shock domain and affects the anchorage-independent growth of breast cancer cells. Oncogene. 2005;24(26):4281-4292.
55. Somasekharan SP, El-Naggar A, Leprivier G, et al. YB-1 regulates stress granule formation and tumor progression by translationally activating G3BP1. J Cell Biol. 2015;208(7):913-929.
56. Lee C, Dhillon J, Wang MYC, et al. Targeting YB-1 in HER-2 overexpressing breast cancer cells induces apoptosis via the mTOR/STAT3 pathway and suppresses tumor growth in mice. Cancer Res. 2008;68(21):8661-8666.
57. Liang C, Ma Y, Yong L, et al. Y-box binding protein-1 promotes tumorigenesis and progression via the epidermal growth factor receptor/AKT pathway in spinal chordoma. Cancer Sci. 2019;110(1):166-179.
58. Bargou RC, Jürchott K, Wagener C, et al. Nuclear localization and increased levels of transcription factor YB-1 in primary human breast cancers are associated with intrinsic MDR1 gene expression. Nat Med. 1997;3(4):447-450.
59. D'Costa NM, Lowerison MR, Raven PA, et al. Y-box binding protein-1 is crucial in acquired drug resistance development in metastatic clear-cell renal cell carcinoma. J Exp Clin Cancer Res. 2020;39(1):33.
60. Homer C, Knight DA, Hananeia L, et al. Y-box factor YB1 controls p53 apoptotic function. Oncogene. 2005;24(56):8314-8325.
61. Evdokimova VM, Ovchinnikov LP. Translational regulation by Y-box transcription factor: involvement of the major mRNA-associated protein, p50. Int J Biochem Cell Biol. 1999;31(1):139-149.
62. Stickeler E, Fraser SD, Honig A, Chen AL, Berget SM, Cooper TA. The RNA binding protein YB-1 binds A/C-rich exon enhancers and stimulates splicing of the CD44 alternative exon v4. EMBO J. 2001;20(14):3821-3830.
63. Li J, Hawkins IC, Harvey CD, Jennings JL, Link AJ, Patton JG. Regulation of alternative splicing by SRrp86 and its interacting proteins. Mol Cell Biol. 2003;23(21):7437-7447.
64. Kromhout D, Menotti A, Alberti-Fidanza A, et al. Comparative ecologic relationships of saturated fat, sucrose, food groups, and a Mediterranean food pattern score to 50-year coronary heart disease mortality rates among 16 cohorts of the Seven Countries Study. Eur J Clin Nutr. 2018;72(8):1103-1110.