Obesity, rather than diet, drives epigenomic alterations in colonic epithelium resembling cancer progression

Cell Metabolism

Volumn 19, Issue 4, 2014, Pages 702-711

  Li, Ruifang ^a   Grimm, Sara A ^a   Chrysovergis, Kaliopi ^a   Kosak, Justin ^a   Wang, Xingya ^a   Du, Ying ^a   Burkholder, Adam ^a   Janardhan, Kyathanahalli ^b   Mav, Deepak ^c   Shah, Ruchir ^c   Eling, Thomas E ^a   Wade, Paul A ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b ILS Inc   (United States)

^c SRA International Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE;

ACETYLATION; ANIMAL EXPERIMENT; ARTICLE; CANCER GROWTH; CANCER RISK; CARCINOGENESIS; CHROMATIN IMMUNOPRECIPITATION; COLON MUCOSA; ENHANCER REGION; EPIGENETICS; FEMALE; GENE EXPRESSION; HISTONE ACETYLATION; HISTONE MODIFICATION; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROMOTER REGION; ANIMAL; COLORECTAL TUMOR; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; INTESTINE MUCOSA; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE;

ANIMALS; BASE SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; COLORECTAL NEOPLASMS; DIET, HIGH-FAT; ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONES; INTESTINAL MUCOSA; MICE; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; OBESITY; SIGNAL TRANSDUCTION;

EID: 84897480129     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2014.03.012     Document Type: Article

References (37)

1. B. Akhtar-Zaidi, R. Cowper-Sal-lari, O. Corradin, A. Saiakhova, C.F. Bartels, D. Balasubramanian, L. Myeroff, J. Lutterbaugh, A. Jarrar, and M.F. Kalady et al. Epigenomic enhancer profiling defines a signature of colon cancer Science 336 2012 736 739
2. S.J. Baek, R. Okazaki, S.H. Lee, J. Martinez, J.S. Kim, K. Yamaguchi, Y. Mishina, D.W. Martin, A. Shoieb, M.F. McEntee, and T.E. Eling Nonsteroidal anti-inflammatory drug-activated gene-1 over expression in transgenic mice suppresses intestinal neoplasia Gastroenterology 131 2006 1553 1560
3. M. Bardou, A.N. Barkun, and M. Martel Obesity and colorectal cancer Gut 62 2013 933 947
4. Cancer Genome Atlas Network Comprehensive molecular characterization of human colon and rectal cancer Nature 487 2012 330 337
5. A.L. Cattin, J. Le Beyec, F. Barreau, S. Saint-Just, A. Houllier, F.J. Gonzalez, S. Robine, M. Pinçon-Raymond, P. Cardot, M. Lacasa, and A. Ribeiro Hepatocyte nuclear factor 4alpha, a key factor for homeostasis, cell architecture, and barrier function of the adult intestinal epithelium Mol. Cell. Biol. 29 2009 6294 6308
6. F. De Sousa E Melo, X. Wang, M. Jansen, E. Fessler, A. Trinh, L.P. de Rooij, J.H. de Jong, O.J. de Boer, R. van Leersum, and M.F. Bijlsma et al. Poor-prognosis colon cancer is defined by a molecularly distinct subtype and develops from serrated precursor lesions Nat. Med. 19 2013 614 618
7. J.R. Dixon, S. Selvaraj, F. Yue, A. Kim, Y. Li, Y. Shen, M. Hu, J.S. Liu, and B. Ren Topological domains in mammalian genomes identified by analysis of chromatin interactions Nature 485 2012 376 380
8. T.E. Eling, S.J. Baek, M. Shim, and C.H. Lee NSAID activated gene (NAG-1), a modulator of tumorigenesis J. Biochem. Mol. Biol. 39 2006 649 655
9. J. Ernst, P. Kheradpour, T.S. Mikkelsen, N. Shoresh, L.D. Ward, C.B. Epstein, X. Zhang, L. Wang, R. Issner, and M. Coyne et al. Mapping and analysis of chromatin state dynamics in nine human cell types Nature 473 2011 43 49
10. J. Ferlay, H.R. Shin, F. Bray, D. Forman, C. Mathers, and D.M. Parkin Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008 Int. J. Cancer 127 2010 2893 2917
11. N. Gao, P. White, and K.H. Kaestner Establishment of intestinal identity and epithelial-mesenchymal signaling by Cdx2 Dev. Cell 16 2009 588 599
12. W.D. Garrison, M.A. Battle, C. Yang, K.H. Kaestner, F.M. Sladek, and S.A. Duncan Hepatocyte nuclear factor 4alpha is essential for embryonic development of the mouse colon Gastroenterology 130 2006 1207 1220
13. A.M. Ghaleb, B.B. McConnell, K.H. Kaestner, and V.W. Yang Altered intestinal epithelial homeostasis in mice with intestine-specific deletion of the Krüppel-like factor 4 gene Dev. Biol. 349 2011 310 320
14. F.G. Giancotti, and E. Ruoslahti Integrin signaling Science 285 1999 1028 1032
15. S. Heinz, C. Benner, N. Spann, E. Bertolino, Y.C. Lin, P. Laslo, J.X. Cheng, C. Murre, H. Singh, and C.K. Glass Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities Mol. Cell 38 2010 576 589
16. J. Hess, P. Angel, and M. Schorpp-Kistner AP-1 subunits: quarrel and harmony among siblings J. Cell Sci. 117 2004 5965 5973
17. A. Hryniuk, S. Grainger, J.G. Savory, and D. Lohnes Cdx function is required for maintenance of intestinal identity in the adult Dev. Biol. 363 2012 426 437
18. J.P. Katz, N. Perreault, B.G. Goldstein, C.S. Lee, P.A. Labosky, V.W. Yang, and K.H. Kaestner The zinc-finger transcription factor Klf4 is required for terminal differentiation of goblet cells in the colon Development 129 2002 2619 2628
19. S.C. Larsson, and A. Wolk Meat consumption and risk of colorectal cancer: a meta-analysis of prospective studies Int. J. Cancer 119 2006 2657 2664
20. C.Y. McLean, D. Bristor, M. Hiller, S.L. Clarke, B.T. Schaar, C.B. Lowe, A.M. Wenger, and G. Bejerano GREAT improves functional interpretation of cis-regulatory regions Nat. Biotechnol. 28 2010 495 501
21. A.A. Moghaddam, M. Woodward, and R. Huxley Obesity and risk of colorectal cancer: a meta-analysis of 31 studies with 70,000 events Cancer Epidemiol. Biomarkers Prev. 16 2007 2533 2547
22. J.P. Moorman, D. Luu, J. Wickham, D.A. Bobak, and C.S. Hahn A balance of signaling by Rho family small GTPases RhoA, Rac1 and Cdc42 coordinates cytoskeletal morphology but not cell survival Oncogene 18 1999 47 57
23. B.S. Reddy, K. Watanabe, and J.H. Weisburger Effect of high-fat diet on colon carcinogenesis in F344 rats treated with 1,2-dimethylhydrazine, methylazoxymethanol acetate, or methylnitrosourea Cancer Res. 37 1977 4156 4159
24. W.E. Roediger, and S.C. Truelove Method of preparing isolated colonic epithelial cells (colonocytes) for metabolic studies Gut 20 1979 484 488
25. A.E. Russ, J.S. Peters, W.C. McNabb, M.P. Barnett, R.C. Anderson, Z. Park, S. Zhu, P. Maclean, W. Young, G.W. Reynolds, and N.C. Roy Gene expression changes in the colon epithelium are similar to those of intact colon during late inflammation in interleukin-10 gene deficient mice PLoS ONE 8 2013 e63251
26. A. Sadanandam, C.A. Lyssiotis, K. Homicsko, E.A. Collisson, W.J. Gibb, S. Wullschleger, L.C. Ostos, W.A. Lannon, C. Grotzinger, and M. Del Rio et al. A colorectal cancer classification system that associates cellular phenotype and responses to therapy Nat. Med. 19 2013 619 625
27. A. Sanyal, B.R. Lajoie, G. Jain, and J. Dekker The long-range interaction landscape of gene promoters Nature 489 2012 109 113
28. J. Schug, W.P. Schuller, C. Kappen, J.M. Salbaum, M. Bucan, and C.J. Stoeckert Jr. Promoter features related to tissue specificity as measured by Shannon entropy Genome Biol. 6 2005 R33
29. S. Schwitalla, A.A. Fingerle, P. Cammareri, T. Nebelsiek, S.I. Göktuna, P.K. Ziegler, O. Canli, J. Heijmans, D.J. Huels, and G. Moreaux et al. Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties Cell 152 2013 25 38
30. R.E. Thurman, E. Rynes, R. Humbert, J. Vierstra, M.T. Maurano, E. Haugen, N.C. Sheffield, A.B. Stergachis, H. Wang, and B. Vernot et al. The accessible chromatin landscape of the human genome Nature 489 2012 75 82
31. I. Tuominen, L. Al-Rabadi, D. Stavrakis, I. Karagiannides, C. Pothoulakis, and J.M. Bugni Diet-induced obesity promotes colon tumor development in azoxymethane-treated mice PLoS ONE 8 2013 e60939
32. M.P. Verzi, H. Shin, H.H. He, R. Sulahian, C.A. Meyer, R.K. Montgomery, J.C. Fleet, M. Brown, X.S. Liu, and R.A. Shivdasani Differentiation-specific histone modifications reveal dynamic chromatin interactions and partners for the intestinal transcription factor CDX2 Dev. Cell 19 2010 713 726
33. M.P. Verzi, H. Shin, L.L. Ho, X.S. Liu, and R.A. Shivdasani Essential and redundant functions of caudal family proteins in activating adult intestinal genes Mol. Cell. Biol. 31 2011 2026 2039
34. M.P. Verzi, H. Shin, A.K. San Roman, X.S. Liu, and R.A. Shivdasani Intestinal master transcription factor CDX2 controls chromatin access for partner transcription factor binding Mol. Cell. Biol. 33 2013 281 292
35. H.S. Wasan, M. Novelli, J. Bee, and W.F. Bodmer Dietary fat influences on polyp phenotype in multiple intestinal neoplasia mice Proc. Natl. Acad. Sci. USA 94 1997 3308 3313
36. S. Yoshimoto, T.M. Loo, K. Atarashi, H. Kanda, S. Sato, S. Oyadomari, Y. Iwakura, K. Oshima, H. Morita, and M. Hattori et al. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome Nature 499 2013 97 101
37. C. Zang, D.E. Schones, C. Zeng, K. Cui, K. Zhao, and W. Peng A clustering approach for identification of enriched domains from histone modification ChIP-Seq data Bioinformatics 25 2009 1952 1958