Inactivation of bone morphogenetic protein 2 may predict clinical outcome and poor overall survival for renal cell carcinoma through epigenetic pathways

Oncotarget

Volumn 6, Issue 11, 2015, Pages 9577-9591

  Mitsui, Yozo ^a,b   Hirata, Hiroshi ^b   Arichi, Naoko ^a   Hiraki, Miho ^a   Yasumoto, Hiroaki ^a   Chang, Inik ^c   Fukuhara, Shinichiro ^d   Yamamura, Soichiro ^b   Shahryari, Varahram ^b   Deng, Guoren ^b   Sharanjot Saini, ^b   Shahana Majid, ^b   Rajvir Dahiya, ^b   Yuichiro Tanaka, ^b   Hiroaki Shiina, ^a  

^a SHIMANE UNIVERSITY FACULTY OF MEDICINE   (Japan)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c Yonsei University   (South Korea)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Bone morphogenetic protein 2; DNA methylation; Molecular marker; Renal cell carcinoma

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; CYCLIN DEPENDENT KINASE INHIBITOR 1; CYCLIN DEPENDENT KINASE INHIBITOR 1B; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45ALPHA; MESSENGER RNA; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIMETABOLITE; AZACITIDINE; BMP2 PROTEIN, HUMAN; DECITABINE; HYBRID PROTEIN; RNA; TUMOR PROTEIN;

APOPTOSIS; ARTICLE; BMP 2 GENE; CANCER CELL; CANCER GRADING; CANCER STAGING; CANCER SURVIVAL; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; COLONY FORMATION; DNA METHYLATION; DNA SEQUENCE; DOWN REGULATION; EPIGENETICS; GENE EXPRESSION; KIDNEY CARCINOMA; NEPHRECTOMY; OVERALL SURVIVAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; AGED; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; CARCINOMA, RENAL CELL; DRUG EFFECTS; FEMALE; GENE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; HUMAN; KIDNEY NEOPLASMS; KIDNEY TUBULE; MALE; METABOLISM; MIDDLE AGED; MORTALITY; PROMOTER REGION; TREATMENT OUTCOME; TUMOR CELL LINE;

AGED; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; AZACITIDINE; BONE MORPHOGENETIC PROTEIN 2; CARCINOMA, RENAL CELL; CELL LINE, TUMOR; DNA METHYLATION; DOWN-REGULATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, CDC; HUMANS; KIDNEY NEOPLASMS; KIDNEY TUBULES; MALE; MIDDLE AGED; NEOPLASM PROTEINS; NEPHRECTOMY; PROMOTER REGIONS, GENETIC; RECOMBINANT FUSION PROTEINS; RNA, MESSENGER; RNA, NEOPLASM; TRANSFECTION; TREATMENT OUTCOME;

EID: 84928732607     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.3445     Document Type: Article

References (42)

1. Curti BD. Renal cell carcinoma. JAMA 2004; 292: 97-100.
2. De Mulder PH, van Herpen CM, Mulders PA. Currentbtreatment of renal cell carcinoma. Annals oncology: official journal of the European Society for Medical Oncology/ESMO. 2004; 15 Suppl 4: iv319-328.
3. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. Cancer J Clin 2012; 62: 10-29.
4. Rini BI, Campbell SC, Escudier B. Renal cell carcinoma. Lancet 2009; 373: 119-132.
5. Heng DY, Xie W, Regan MM, Harshman LC, Bjarnason GA, Vaishampayan UN, Mackenzie M, Wood L, Donskov F, Tan MH, Rha SY, Agarwal N, et al. External validation and comparison with other models of the International Metastatic Renal-Cell Carcioma Database Consortium prognostic model: a population-based study. Lacet Oncol 2013; 14: 141-148.
6. Utsumi T, Ueda T, Fukasawa S, Komaru A, Sazuka T, Kawamura K, Imamoto T, Nihei N, Suzuki H, Ichikawa T. Prognostic models for renal cell carcinoma recurrence:external validation in a Japanese population. Int J Urol 2011; 18: 667-671.
7. Wozney JM, Rosen V, Celeste AJ, Mitsock LM, Whitters MJ, Kriz RW, Hewick RM, Wang EA. Novel regulators of bone formation: molecular clones and activities. Science 1988; 242: 1528-1534.
8. Kawamura C, Kizaki M, Ikeda Y. Bone morphogenetic protein (BMP)-2 induces apoptosis in human myeloma cells. Leuk Lymphoma 2002; 43: 635-639.
9. Hallahan AR, Pritchard JI, Chandraratna RA, Ellenbogen RG, Geyer JR, Overland RP, Strand AD, Tapscott SJ, Olson JM. BMP-2 mediates retinoid-induced apoptosis in medulloblastoma cells through a paracrine effect. Nat Med 2003; 9: 1033-1038.
10. Zhang Y, Chen X, Qiao M, Zhang BQ, Wang N, Zhang Z, Liao Z, Zeng L, Deng Y, Deng F, Zhang J, Yin L, Liu W, et al. Bone morphogenetic protein 2 inhibits the proliferation and growth of human colorectal cancer cells. Oncol Rep 2014; 32: 1013-1020.
11. Zhang J, Ge Y, Sun L, Cao J, Wu Q, Guo L, Wang Z. Effect of bone morphogenetic protein-2 on proliferation and apoptosis of gastric cancer cells. Int J Med Sci 2012; 9:182-192.
12. Herpin A, Cunningham C. Cross-talk between the bone morphogenetic protein pathway and other major signaling pathways results in tightly regulated cell-specific outcomes. FEBS J 2007; 274: 2977-2985.
13. Nohe A, Keating E, Knaus P, Petersen NO. Signal transduction of bone morphogenetic protein receptors. Cell Signal 2004; 16: 291-299.
14. Wen ZX, Akiyama Y, Baylin SB Yuasa Y. Frequent epigenetic silencing of the bone morphogenetic protein 2 gene through methylation in gastric carcinomas. Oncogene 2006; 25: 2666-2673.
15. Kodach LL, Jacobs RJ, Voorneveld PW, Wildenberg ME, Verspaget HW, van Wezel T, Morreau H, Hommes DW, Peppelenbosch MP, van den Brink GR, Hardwick JC. Statins augment the chemosensitivity of colorectal cancer cells inducing epigenetic reprogramming and reducing colorectal cancer cell 'stemness' via the bone morphogenetic protein pathway. Gut 2011; 60: 1544-1553.
16. Brubaker KD, Corey E, Brown LG, Vessella RL. Bone morphogenetic protein signaling in prostate cancer cell lines. J Cell Biochem 2004; 91: 151-160.
17. Johnsen IK, Kappler R, Auernhammer CJ, Beuschlein F. Bone morphogenetic proteins 2 and 5 are down-regulated in adrenocortical carcinoma and modulate adrenal cell proliferation and steroidogenesis. Cancer Res 2009; 69:5784-5792.
18. Wang L, Park P, Zhang H, La Marca F, Claeson A, Than K, Rahman S, Lin CY. BMP-2 inhibits tumor growth of human renal cell carcinoma and induces bone formation. Int J Cancer 2012; 131: 1941-1950.
19. Markić D, Ćelić T, Gršković A, Španjol J, Fučkar Ž, Grahovac B, Dord{stroke}ević G, Bobinac D. mRNA expression of bone morphogenetic proteins their receptors in human renal cell carcinoma. Urol Int 2011; 87: 353-358.
20. Sidransky D. Emerging molecular makers of cancer. Nat Rev Cancer 2002; 2: 210-219.
21. Kristensen LS, Raynor MP, Candiloro I, Dobrovic A. Methylation profiling of normal individuals mosaic promoter methylation of cancer-associated genes. Oncotarget 2012; 3: 450-461.
22. Nakamura Y, Ozaki T, Koseki H, Nakagawara A, Sakiyama S. Accumulation of p27KIP is associated with BMP2-induced growth arrest and neuronal differentiation of human neuroblastoma-derived cell lines. BBRC 2003; 307:206-213.
23. Wu WK, Sung JJ, Wu YC, Li ZJ, Yu L, Cho CH. Bone morphogenetic protein signaling is required for the antimitogenic effect of the proteasome inhibitor MG-132 on colon cancer cells. Br J Pharmacol 2008; 154: 632-638.
24. Shirai YT, Ehata S, Yashiro M, Yanagihara K, Hirakawa K, Miyazono K. Bone morphogenetic protein-2 and -4 play tumor suppressive roles in human diffuse-type gastric carcinoma. Am J Pathol 2011; 179: 2920-2930.
25. Liu S, Yin F, Fan W, Wang S, Guo XR, Zhang JN, Tian ZM, Fan M. Over-expression of BMPR-IB reduces the malignancy of glioblastoma cells by upregulation of p21 and p27Kip1. J Exp Clin Cancer Res 2012; 31: 52.
26. Chang I, Liu J, Majid S, Saini S, Zaman MS, Yamamura S, Shahryari V, Chiyomaru T, Deng G, Dahiya R, Tanaka Y. Catechol-O-methyltransferase-mediated metabolism of 4-hydroxyestradiol inhibits the growth of human renal cancer cells through the apoptotic pathway. Carcinogenesis 2012; 33: 420-426.
27. Tamura RE, de Vasconcellos JF, Sarkar D, Libermann TA, Fisher PB, Zerbini LF. GADD45 proteins: central players in tumorgenesis. Curr Mol Med 2012; 12: 634-651.
28. Simard EP, Ward EM, Siegel R, Jemal A. Cancers with increasing incidence trends in the United States: 1999 through 2008. CA Cancer J Clin 2012; 62: 118-124.
29. Washio M, Mori M. Risk factor for renal cell carcinoma in Japanese population. Clin Med Oncol 2009; 3: 71-75.
30. Banyra O, Tarchynets M, Shulyak A. Renal cell carcinoma:how to hit the target? Cent European J Urol 2014; 66: 394-404.
31. Belldegrun AS, Chamie K, Kloepfer P, Fall B, Bevan P, Strökel S, Wilhelm O, Pantuck AJ. ARISER: A randomized double blind phase III study to evaluate adjuvant cG250 treatment versus placebo in patients with high-risk ccRCCResults and implications for adjuvant clinical trials. J Clin Oncol 2013; (31 Suppl): 4507. Abstr.
32. Arai E, Kanai Y. Genetic and epigenetic alterations during renal carcinogenesis. Int J Clin Expo Pathol 2010; 4: 57-73.
33. Hu CY, Mohtat D, Yu Y, Ko YA, Shenoy N, Bhattacharya S, Izquierdo MC, Park AS, Giricz O, Vallumsetla N, Gundabolu K, Ware K, Bhagat TD, et al. Kidney cancer is characterized by aberrant methylation of tissue-specific enhancers that are prognostic for overall survival. Clin Cancer Res 2014; 20: 4349-4360.
34. Hengst L, Dulic V, Singerland JM, Lees E, Reed SI. A cell cycle-regulated inhibitor of cyclin-dependent kinases. Proc Natl Acad Sci USA 1991; 91: 5921-5925.
35. Polyak K, Lee MH, Erdjument-Bromage H, Koff A, Roberts JM, Tempst P, Massagué J. Cloning p27KIP1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antiitogenic signals. Cell 1994; 78: 59-66.
36. Toyoshima H, Hunter T. p27, a novel inhibitor of G1 cyclin-Cdk protein kinase activity, is related to p21. Cell 1994; 78: 67-74.
37. Sgambato A, Camerini A, Genovese G, De Luca F, Viacava P, Migaldi M, Boninsegna A, Cecchi M, Sepich CA, Rossi G, Arena V, Cittadini A, Amoroso D. Loss of nulear p27KIP1 and α-dystroglycan is a frequent event and is a strong predictor of poor outcome in renal cell carcinoma. Cancer Sci 2010; 101: 2080-2086.
38. Gayed BA, Youssef RF, Bagrodia A, Kapur P, Darwish OM, Krabbe LM, Sagalowsky A, Lotan Y, Margulis V. Prognostic role of cell cycle and proliferative biomarkers in patients with clear cell renal cell carcinoma. J Urol 2013; 190: 1662-1667.
39. Abdollahi A, Lord KA, Hoffman-Liebermann B, Liebermann DA. Sequence and expression of a cDNA encoding MyD118: a novel myeloid differentiation primaryresponse gene induced by multiple cytokines. Oncogene 1991; 6: 165-167.
40. Amanullah A, Azam N, Balliet A, Hollander C, Hoffman B, Fornace A, Liebermann D. Cell signalling: cell survival and a Gadd45-factor deficiency. Nature 2003; 424: 741-742.
41. Ijiri K, Zerbini LF, Peng H, Correa RG, Lu B, Walsh N, Zhao Y, Taniguchi N, Huang XL, Otu H, Wang H, Wang JF, Komiya S, et al. A novel role for GADD45beta as a mediator of MMP-13 gene expression during chondrocyte terminal differentiation. J Biol Chem 2005; 280: 38544-38555.
42. Tront J, Hoffman B, Liebermann D. Gadd45a suppresses ras-driven mammary tumorigenesis by activation of JNK and p38 stress signaling resulting in apoptosis and senescence. Cancer Res 2006; 17: 8448-8454.