DNA methylation and histone modifications cause silencing of Wnt antagonist gene in human renal cell carcinoma cell lines

International Journal of Cancer

Volumn 123, Issue 3, 2008, Pages 535-542

  Kawamoto, Ken ^a   Hirata, Hiroshi ^a   Kikuno, Nobuyuki ^a   Tanaka, Yuichiro ^a   Nakagawa, Masayuki ^b   Dahiya, Rajvir ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

DNA methylation; Histone modification; Renal cell carcinoma; sFRP2 gene; Wnt antagonist

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; BISULFITE; DNA; HISTONE; HISTONE H3; HISTONE H4; SECRETED FRIZZLED RELATED PROTEIN 2; TRICHOSTATIN A; WNT PROTEIN;

ARTICLE; CANCER CELL CULTURE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA SEQUENCE; GENE ACTIVATION; GENE REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; KIDNEY CARCINOMA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN MODIFICATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; AZACITIDINE; BLOTTING, WESTERN; CARCINOMA, RENAL CELL; CELL LINE, TUMOR; CPG ISLANDS; DNA METHYLATION; DNA MODIFICATION METHYLASES; ENZYME INHIBITORS; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HISTONE DEACETYLASES; HISTONES; HUMANS; HYDROXAMIC ACIDS; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; KIDNEY NEOPLASMS; MEMBRANE PROTEINS; PROMOTER REGIONS (GENETICS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; WNT PROTEINS;

EID: 46049102805     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.23514     Document Type: Article

References (47)

1. Hellebrekers DM, Castermans K, Vire E, Dings RP, Hoebers NT, Mayo KH, Oude Egbrink MG, Molema G, Fuks F, van Engeland M, Griffioen AW. Epigenetic regulation of tumor endothelial cell anergy: silencing of intercellular adhesion molecule-1 by histone modifications. Cancer Res 2006;66:10770-7.
2. Jenuwein T, Allis CD. Translating the histone code. Science 2001;293:1074-80.
3. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003;33(Suppl):245-54.
4. Esteller M. CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene 2002;21:5427-40.
5. Zhu WG, Dai Z, Ding H, Srinivasan K, Hall J, Duan W, Villalona-Calero MA, Plass C, Otterson GA. Increased expression of unmethylated CDKN2D by 5-aza-2′-deoxycytidine in human lung cancer cells. Oncogene 2001;20:7787-96.
6. Nakagawachi T, Soejima H, Urano T, Zhao W, Higashimoto K, Satoh Y, Matsukura S, Kudo S, Kitajima Y, Harada H, Furukawa K, Matsuzaki H, et al. Silencing effect of CpG island hypermethylation and histone modifications on O6-methylguanine-DNA methyltransferase (MGMT) gene expression in human cancer. Oncogene 2003;22:8835-44.
7. Esteller M. Epigenetics provides a new generation of oncogenes and tumour-suppressor genes. Br J Cancer 2007;96(Suppl):R26-R30.
8. Zhang Z, Joh K, Yatsuki H, Zhao W, Soejima H, Higashimoto K, Noguchi M, Yokoyama M, Iwasaka T, Mukai T. Retinole acid receptor β2 is epigenetically silenced either by DNA methylation or repressive histone modifications at the promoter in cervical cancer cells. Cancer Lett 2007;247:318-27.
9. Rountree MR, Bachman KE, Herman JG, Baylin SB. DNA methylation, chromatin inheritance, and cancer. Oncogene 2001;20:3156-65.
10. Jones PA, Baylin SB. The fundamental role of epigenetic events in cancer. Nat Rev Genet 2002;3:415-28.
11. Suzuki H, Watkins DN, Jair KW, Schuebel KE, Markowitz SD, Chen WD, Pretlow TP, Yang B, Akiyama Y, Van Engeland M, Toyota M, Tokino T, et al. Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer. Nat Genet 2004;36:417-22.
12. Finch PW, He X, Kelley MJ, Uren A, Schaudies RP, Popescu NC, Rudikoff S, Aaronson SA, Varmus HE, Rubin JS. Purification and molecular cloning of a secreted. Frizzled-related antagonist of Wnt action. Proc Natl Acad Sci USA 1997;94:6770-5.
13. Melkonyan HS, Chang WC, Shapiro JP, Mahadevappa M, Fitzpatrick PA, Kiefer MC, Tomei LD, Umansky SR. SARPs: a family of secreted apoptosis-related proteins. Proc Natl Acad Sci USA 1997;94:13636-41.
14. Urakami S, Shiina H, Enokida H, Hirata H, Kawamoto K, Kawakami T, Kikuno N, Tanaka Y, Majid S, Nakagawa M, Igawa M, Dahiya R. Wnt antagonist family genes as biomarkers for diagnosis, staging, and prognosis of renal cell carcinoma using tumor and serum DNA. Clin Cancer Res 2006;12:6989-97.
15. Suzuki H, Gabrielson E, Chen W, Anbazhagan R, van Engeland M, Weijenberg MP, Herman JG, Baylin SB. A genomic screen for genes upregulated by demethylation and histone deacetylase inhibition in human colorectal cancer. Nat Genet 2002;31:141-9.
16. Urakami S, Shiina H, Enokida H, Kawakami T, Kawamoto K, Hirata H, Tanaka Y, Kikuno N, Nakagawa M, Igawa M, Dahiya R. Combination analysis of hypermethylated Wnt-antagonist family genes as a novel epigenetic biomarker panel for bladder cancer detection. Clin Cancer Res 2006;12:2109-16.
17. Nojima M, Suzuki H, Toyota M, Watanabe Y, Maruyama R, Sasaki S, Sasaki Y, Mita H, Nishikawa N, Yamaguchi K, Hirata K, Itoh F, et al. Frequent epigenetic inactivation of SFRP genes and constitutive activation of Wnt signaling in gastric cancer. Oncogene 2007;26:4699-713.
18. McGarvey KM, Fahrner JA, Greene E, Martens J, Jenuwein T, Baylin SB. Silenced tumor suppressor genes reactivated by DNA demethylation do not return to a fully euchromatic chromatin state. Cancer Res 2006;66:3541-9.
19. Kikuno N, Moriyama-Gonda N, Yoshino T, Yoneda T, Urakami S, Terashima M, Yoshida M, Kishi H, Shigeno K, Shiina H, Igawa M. Blockade of paclitaxel-induced thymidine Phosphorylase expression can accelerate apoptosis in human prostate cancer cells. Cancer Res 2004;64:7526-32.
20. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics 2002;18:1427-31.
21. Soejima H, Nakagawachi T, Zhao W, Higashimoto K, Urano T, Matsukura S, Kitajima Y, Takeuchi M, Nakayama M, Oshimura M, Miyazaki K, Joh K, et al. Silencing of imprinted CDKN1C gene expression is associated with loss of CpG and histone H3 lysine 9 methylation at DMR-LIT1 in esophageal cancer. Oncogene 2004;23:4380-8.
22. Bannister AJ, Kouzarides T. Reversing histone methylation. Nature 2005;436:1103-6.
23. Kawano Y, Kypta R. Secreted antagonists of the Wnt signalling pathway. J Cell Sci 2003;116:2627-34.
24. Urakami S, Shiina H, Enokida H, Kawakami T, Tokizane T, Ogishima T, Tanaka Y, Li LC, Ribeiro-Filho LA, Terashima M, Kikuno N, Adachi H, et al. Epigenetic inactivation of Wnt inhibitory factor-1 plays an important role in bladder cancer through aberrant canonical Wnt/beta-catenin signaling pathway. Clin Cancer Res 2006;12:383-91.
25. Fukui T, Kondo M, Ito G, Maeda O, Sato N, Yoshioka H, Yokoi K, Ueda Y, Shimokata K, Sekido Y. Transcriptional silencing of secreted frizzled related protein 1 (SFRP 1) by promoter hypermethylation in non-small-cell lung cancer. Oncogene 2005;24:6323-7.
26. Zou H, Molina JR, Harrington JJ, Osborn NK, Klatt KK, Romero Y, Burgart LJ, Ahlquist DA. Aberrant methylation of secreted frizzled-related protein genes in esophageal adenocarcinoma and Barrett's esophagus. Int J Cancer 2005;116:584-91.
27. Huang J, Zhang YL, Teng XM, Lin Y, Zheng DL, Yang PY, Han ZG. Down-regulation of SFRP1 as a putative tumor suppressor gene can contribute to human hepatocellular carcinoma. BMC Cancer 2007;7:126.
28. Dahl E, Wiesmann F, Woenckhaus M, Stoehr R, Wild PJ, Veeck J, Knuchel R, Klopocki E, Sauter G, Simon R, Wieland WF, Walter B, et al. Frequent loss of SFRP1 expression in multiple human solid tumours: association with aberrant promoter methylation in renal cell carcinoma. Oncogene 2007;26:5680-91.
29. Gumz ML, Zou H, Kreinest PA, Childs AC, Belmonte LS, Legrand SN, Wu KJ, Luxon BA, Sinha M, Parker AS, Sun LZ, Ahlquist DA, et al. Secreted frizzled-related protein 1 loss contributes to tumor phenotype of clear cell renal cell carcinoma. Clin Cancer Res 2007;13:4740-9.
30. Nojima M, Suzuki H, Toyota M, Watanabe Y, Maruyama R, Sasaki S, Sasaki Y, Mita H, Nishikawa N, Yamaguchi K, Hirata K, Itoh F, et al. Frequent epigenetic inactivation of SFRP genes and constitutive activation of Wnt signaling in gastric cancer. Oncogene 2007;26:4699-713.
31. Baylin SB, Hoppener JW, de Bustros A, Steenbergh PH, Lips CJ, Nelkin BD. DNA methylation patterns of the calcitonin gene in human lung cancers and lymphomas. Cancer Res 1986;46:2917-22.
32. Kondo Y, Shen L, Issa JP. Critical role of histone methylation in tumor suppressor gene silencing in colorectal cancer. Mol Cell Biol 2003;23:206-15.
33. Fahrner JA, Eguchi S, Herman JG, Baylin SB. Dependence of histone modifications and gene expression on DNA hypermethylation in cancer. Cancer Res 2002;62:7213-8.
34. Nguyen CT, Weisenberger DJ, Velicescu M, Gonzales FA, Lin JC, Liang G, Jones PA. Histone H3-lysine 9 methylation is associated with aberrant gene silencing in cancer cells and is rapidly reversed by 5-aza-2′- deoxycytidine. Cancer Res 2002;62:6456-61.
35. Coombes MM, Briggs KL, Bone JR, Clayman GL, El-Naggar AK, Dent SY. Resetting the histone code at CDKN2A in HNSCC by inhibition of DNA methylation. Oncogene 2003;22:8902-11.
36. Wozniak RJ, Klimecki WT, Lau SS, Feinstein Y, Futscher BW. 5-Aza-2′-deoxycytidine-mediated reductions in G9A histone methyltransferase and histone H3 K9 di-methylation levels are linked to tumor suppressor gene reactivation. Oncogene 2007;26:77-90.
37. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, Strouboulis J, Wolffe AP. Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 1998;19:187-91.
38. Ng HH, Zhang Y, Hendrich B, Johnson CA, Turner BM, Erdjument-Bromage H, Tempst P, Reinberg D, Bird A. MBD2 is a transcriptional repressor belonging to the MeCP1 histone deacetylase complex. Nat Genet 1999;23:58-61.
39. Wade PA, Gegonne A, Jones PL, Ballestar E, Aubry F, Wolffe AP. Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet 1999;23:62-6.
40. Nakayama T, Watanabe M, Yamanaka M, Hirokawa Y, Suzuki H, Ito H, Yatani R, Shiraishi T. The role of epigenetic modifications in retinoic acid receptor β2 gene expression in human prostate cancers. Lab Invest 2001;81:1049-57.
41. Creusot F, Acs G, Christman JK. Inhibition of DNA methyltransferase and induction of Friend erythroleukemia cell differentiation by 5-aza-cytidine and 5-aza-2′-deoxycytidine. J Biol Chem 1982;257:2041-8.
42. McCabe MT, Davis JN, Day ML. Regulation of DNA methyltransferase 1 by the pRb/E2F1 pathway. Cancer Res 2005;65:3624-32.
43. Biniszkiewicz D, Gribnau J, Ramsahoye B, Gaudet F, Eggan K, Humpherys D, Mastrangelo MA, Jun Z, Walter J, Jaenisch R. Dnmt1 overexpression causes genomic hypermethylation, loss of imprinting, and embryonic lethality. Mol Cell Biol 2002;22:2124-35.
44. Januchowski R, Dabrowski M, Ofori H, Jagodzinski PP. Trichostatin A down-regulate DNA methyltransferase 1 in Jurkat T cells. Cancer Lett 2007;246:313-7.
45. Yang X, Phillips DL, Ferguson AT, Nelson WG, Herman JG, Davidson NE. Synergistic activation of functional estrogen receptor (ER)-alpha by DNA methyltransferase and histone deacetylase inhibition in human ER-alpha-negative breast cancer cells. Cancer Res 2001;61:7025-9.
46. Jung JW, Cho SD, Ahn NS, Yang SR, Park JS, Jo EH, Hwang JW, Jung JY, Kim SH, Kang KS, Lee YS. Ras/MAP kinase pathways are involved in Ras specific apoptosis induced by sodium butyrate. Cancer Lett 2005;225:199-206.
47. Park WH, Jung CW, Park JO, Kim K, Kim WS, Im YH, Lee MH, Kang WK, Park K. Trichostatin inhibits the growth of ACHN renal cell carcinoma cells via cell cycle arrest in association with p27, or apoptosis. Int J Oncol 2003;22:1129-34.