Class I and III HDACs and loss of active chromatin features contribute to epigenetic silencing of CDX1 and EPHB tumor suppressor genes in colorectal cancer

Epigenetics

Volumn 6, Issue 5, 2011, Pages 610-622

  Rönsch, Kerstin ^a   Jäger, Marcel ^a   Schöpflin, Anja ^b   Danciu, Mihai ^b,c   Laßmann, Silke ^b   Hecht, Andreas ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

^c GRIGORE T POPA UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

Author keywords

CDX1; Colorectal cancer; DNA methylation; EphB receptors; HDACs; Transcriptional repression; catenin

Indexed keywords

BETA CATENIN; DNA; DNA METHYLTRANSFERASE INHIBITOR; EPHRIN RECEPTOR B2; EPHRIN RECEPTOR B3; EPHRIN RECEPTOR B4; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; TRANSCRIPTION FACTOR CDX1; WNT PROTEIN;

ARTICLE; CARCINOGENESIS; CARCINOMA CELL; CHROMATIN; CLINICAL ARTICLE; COLON MUCOSA; COLORECTAL ADENOMA; COLORECTAL CANCER; COLORECTAL CARCINOMA; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE LOCUS; GENE SILENCING; GENETIC HETEROGENEITY; HISTONE MODIFICATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INVASIVE CARCINOMA; RECEPTOR GENE; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE; UPREGULATION;

EID: 79957536067     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.6.5.15300     Document Type: Article

References (51)

1. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006; 127: 469-80.
2. Merlos-Suarez A, Batlle E. Eph-ephrin signalling in adult tissues and cancer. Curr Op Cell Biol 2008; 20: 194-200.
3. Cortina C, Palomo-Ponce S, Iglesias M, Fernandez-Masip JL, Vivancos A, Whissell G, et al. EphB-ephrin-B interactions suppress colorectal cancer progression by compartmentalizing tumor cells. Nature Genetics 2007; 39: 1376-83.
4. Batlle E, Bacani J, Begthel H, Jonkheer S, Gregorieff A, van de Born M, et al. EphB receptor activity suppresses colorectal cancer progression. Nature 2005; 435: 1126-30.
5. Chiu ST, Chang KJ, Ting CH, Shen HC, Li H, Hsieh FJ. Overexpression of EphB3 enhances cell-cell contacts and suppresses tumor growth in HT-29 human colon cancer cells. Carcinogenesis 2009; 30: 1475-86.
6. Guo DL, Zhang J, Yuen ST, Tsui WY, Chan AS, Ho C, et al. Reduced expression of EphB2 that parallels invasion and metastasis in colorectal tumours. Carcinogenesis 2006; 27: 454-64.
7. Fu T, Li P, Wang H, He Y, Luo D, Zhang A, et al. c-Rel is a transcriptional repressor of EPHB2 in colorectal cancer. J Pathol 2009; 219: 103-13.
8. Jubb AM, Zhong F, Bheddah S, Grabsch HI, Frantz GD, Mueller W, et al. EphB2 is a prognostic factor in colorectal cancer. Clin Cancer Res 2005; 11: 5181-7.
9. Lugli A, Spichtin H, Maurer R, Mirlacher M, Kiefer J, Huusko P, et al. EphB2 expression across 138 human tumor types in a tissue microarray: high levels of expression in gastrointestinal cancers. Clin Cancer Res 2005; 11: 6450-8.
10. Davalos V, Dopeso H, Castano J, Wilson AJ, Vilardell F, Romero-Gimenez J, et al. EPHB4 and survival of colorectal cancer patients. Cancer Res 2006; 66: 8943-8.
11. Mallo GV, Rechreche H, Frigerio JM, Rocha D, Zweibaum A, Lacasa M, et al. Molecular cloning, sequencing and expression of the mRNA encoding human Cdx1 and Cdx2 homeobox. Downregulation of Cdx1 and Cdx2 mRNA expression during colorectal carcinogenesis. Int J Cancer 1997; 74: 35-44.
12. Crissey MA, Guo RJ, Fogt F, Li H, Katz JP, Silberg DG, et al. The homeodomain transcription factor Cdx1 does not behave as an oncogene in normal mouse intestine. Neoplasia 2008; 10: 8-19.
13. Pilozzi E, Onelli MR, Ziparo V, Mercantini P, Ruco L. CDX1 expression is reduced in colorectal carcinoma and is associated with promoter hypermethylation. J Pathol 2004; 204: 289-95.
14. Guo RJ, Huang E, Ezaki T, Patel N, Sinclair K, Wu J, et al. Cdx1 inhibits human colon cancer cell proliferation by reducing beta-catenin/T-cell factor transcriptional activity. J Biol Chem 2004; 279: 36865-75.
15. Alazzouzi H, Davalos V, Kokko A, Domingo E, Woerner SM, Wilson AJ, et al. Mechanisms of inactivation of the receptor tyrosine kinase EPHB2 in colorectal tumors. Cancer Res 2005; 65: 10170-3.
16. Kumar SR, Scehnet JS, Ley EJ, Singh J, Krasnoperov V, Liu R, et al. Preferential induction of EphB4 over EphB2 and its implication in colorectal cancer progression. Cancer Res 2009; 69: 3736-45.
17. Wu Q, Lind GE, Aasheim HC, Micci F, Silins I, Trope CG, et al. The EPH receptor Bs (EPHBs) promoters are unmethylated in colon and ovarian cancers. Epigenetics 2007; 2: 237-43.
18. Esteller M. Cancer epigenomics: DNA methylomes and histone-modification maps. Nat Rev Genet 2007; 8: 286-98.
19. Cedar H, Bergman Y. Linking DNA methylation and histone modification: patterns and paradigms. Nat Rev Genet 2009; 10: 295-304.
20. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J 2003; 22: 5323-35.
21. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, et al. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002; 419: 624-9.
22. Wilson AJ, Byun DS, Popova N, Murray LB, L'Italien K, Sowa Y, et al. Histone deacetylase 3 (HDAC3) and other class I HDACs regulate colon cell maturation and p21 expression and are deregulated in human colon cancer. J Biol Chem 2006; 281: 13548-58.
23. Linhart HG, Lin H, Yamada Y, Moran E, Steine EJ, Gokhale S, et al. Dnmt3b promotes tumorigenesis in vivo by gene-specific de novo methylation and transcriptional silencing. Genes Dev 2007; 21: 3110-22.
24. Vire E, Brenner C, Deplus R, Blanchon L, Fraga M, Didelot C, et al. The Polycomb group protein EZH2 directly controls DNA methylation. Nature 2006; 439: 871-4.
25. Bai S, Ghoshal K, Datta J, Majumder S, Yoon SO, Jacob ST. DNA methyltransferase 3b regulates nerve growth factor-induced differentiation of PC12 cells by recruiting histone deacetylase 2. Mol Cell Biol 2005; 25: 751-66.
26. Suh ER, Ha CS, Rankin EB, Toyota M, Traber PG. DNA methylation downregulates CDX1 gene expression in colorectal cancer cell lines. J Biol Chem 2002; 277: 35795-800.
27. Wong NA, Britton MP, Choi GS, Stanton TK, Bicknell DC, Wilding JL, et al. Loss of CDX1 expression in colorectal carcinoma: promoter methylation, mutation and loss of heterozygosity analyses of 37 cell lines. Proc Natl Acad Sci USA 2004; 101: 574-9.
28. Lassmann S, Danciu M, Muller M, Weis R, Makowiec F, Schulte-Monting J, et al. Aurora A is differentially expressed and regulated in chromosomal and microsatellite instable sporadic colorectal cancers. Mod Pathol 2009; 22: 1385-97.
29. Koinuma K, Yamashita Y, Liu W, Hatanaka H, Kurashina K, Wada T, et al. Epigenetic silencing of AXIN2 in colorectal carcinoma with microsatellite instability. Oncogene 2006; 25: 139-46.
30. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, et al. High-resolution profiling of histone methylations in the human genome. Cell 2007; 129: 823-37.
31. Bedalov A, Gatbonton T, Irvine WP, Gottschling DE, Simon JA. Identification of a small molecule inhibitor of Sir2p. Proc Natl Acad Sci USA 2001; 98: 15113-8.
32. Blackwell L, Norris J, Suto CM, Janzen WP. The use of diversity profiling to characterize chemical modulators of the histone deacetylases. Life Sciences 2008; 82: 1050-8.
33. WAF1 involves changes in promoter-associated proteins, including HDAC1. Proc Natl Acad Sci USA 2004; 101: 1241-6.
34. Marks PA, Xu WS. Histone deacetylase inhibitors: Potential in cancer therapy. J Cell Biochem 2009; 107: 600-8.
35. Saito A, Yamashita T, Mariko Y, Nosaka Y, Tsuchiya K, Ando T, et al. A synthetic inhibitor of histone deacetylase, MS-27-275, with marked in vivo antitumor activity against human tumors. Proc Natl Acad Sci USA 1999; 96: 4592-7.
36. Cip1/WAF1 expression, independent of histone deacetylase 1. Cell Death Diff 2005; 12: 395-404.
37. Zhu P, Martin E, Mengwasser J, Schlag P, Janssen KP, Gottlicher M. Induction of HDAC2 expression upon loss of APC in colorectal tumorigenesis. Cancer Cell 2004; 5: 455-63.
38. Batlle E, Henderson JT, Beghtel H, van den Born MM, Sancho E, Huls G, et al. Beta-catenin and TCF mediate cell positioning in the intestinal epithelium by controlling the expression of EphB/ephrinB. Cell 2002; 111: 251-63.
39. Wohrle S, Wallmen B, Hecht A. Differential control of Wnt target genes involves epigenetic mechanisms and selective promoter occupancy by T-cell factors. Mol Cell Biol 2007; 27: 8164-77.
40. Ohm JE, McGarvey KM, Yu X, Cheng L, Schuebel KE, Cope L, et al. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nature Genetics 2007; 39: 237-42.
41. Schlesinger Y, Straussman R, Keshet I, Farkash S, Hecht M, Zimmerman J, et al. Polycomb-mediated methylation on Lys27 of histone H3 pre-marks genes for de novo methylation in cancer. Nature Genet 2007; 39: 232-6.
42. Widschwendter M, Fiegl H, Egle D, Mueller-Holzner E, Spizzo G, Marth C, et al. Epigenetic stem cell signature in cancer. Nature Genet 2007; 39: 157-8.
43. Wang P, Lin C, Smith ER, Guo H, Sanderson BW, Wu M, et al. Global analysis of H3K4 methylation defines MLL family member targets and points to a role for MLLl-mediated H3K4 methylation in the regulation of transcriptional initiation by RNA polymerase II. Mol Cell Biol 2009; 29: 6074-85.
44. Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, et al. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 2009; 138: 1019-31.
45. Ropero S, Esteller M. The role of histone deacetylases (HDACs) in human cancer. Mol Oncol 2007; 1: 19-25.
46. Peinado H, Ballestar E, Esteller M, Cano A. Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol Cell Biol 2004; 24: 306-19.
47. McDonel P, Costello I, Hendrich B. Keeping things quiet: roles of NuRD and Sin3 co-repressor complexes during mammalian development. Intl J Biochem Cell Biol 2009; 41: 108-16.
48. Ashburner BP, Westerheide SD, Baldwin AS Jr. The p65 (RelA) subunit of NFkappaB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol Cell Biol 2001; 21: 7065-77.
49. Gerlach U, Kayser G, Walch A, Hopt U, Schulte-Monting J, Werner M, et al. Centrosome-, chromosomal-passenger-and cell cycle-associated mRNAs are differentially regulated in the development of sporadic colorectal cancer. J Pathol 2006; 208: 462-72.
50. Dydensborg AB, Herring E, Auclair J, Tremblay E, Beaulieu JF. Normalizing genes for quantitative RT-PCR in differentiating human intestinal epithelial cells and adenocarcinomas of the colon. American J Physiol 2006; 290: 1067-74.
51. Weise A, Bruser K, Elfert S, Wallmen B, Wittel Y, Wohrle S, et al. Alternative splicing of Tcf7l2 transcripts generates protein variants with differential promoter-binding and transcriptional activation properties at Wnt/beta-catenin targets. Nucleic Acids Res 2010; 38: 1964-81.