Inactivation of adenomatous polyposis coli reduces bile acid/farnesoid X receptor expression through FXR gene cpgmethylation in mouse colon tumors and human colon cancer cells

Journal of Nutrition

Volumn 146, Issue 2, 2016, Pages 236-242

  Selmin, Ornella I ^a,b   Fang, Changming ^b   Lyon, Adam M ^a   Doetschman, Tom C ^b   Thompson, Patricia A ^b   Martinez, Jesse D ^b   Smith, Jeffrey W ^c   Lance, Peter M ^b   Romagnolo, Donato F ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c BURNHAM INSTITUTE   (United States)

Author keywords

Adenomatous polyposis coli; Bile acid metabolism; Colon cancer; CpG methylation; Deoxycholic acid; Epigenetics; Farnesoid X receptor; Inflammation

Indexed keywords

BILE ACID; FARNESOID X RECEPTOR; GENOMIC DNA; RNA; CELL RECEPTOR; CYCLOOXYGENASE 2; FARNESOID X-ACTIVATED RECEPTOR; MYC PROTEIN; MYC PROTEIN, HUMAN; NUCLEAR RECEPTOR SUBFAMILY 0, GROUP B, MEMBER 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL LINE; COLON CANCER; COLON MUCOSA; COLON POLYPOSIS; COLON TUMOR; CPG ISLAND; CYCLOOXYGENASE 2 GENE; DNA METHYLATION; FARNESOID X RECEPTOR GENE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; ILEAL BILE ACID BINDING PROTEIN GENE; IN VITRO STUDY; MALE; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; SMALL HETERODIMER PARTNER GENE; ADENOCARCINOMA; ANIMAL; C57BL MOUSE; COLON; GENE SILENCING; GENETICS; HCT116 CELL LINE; HT 29 CELL LINE; METABOLISM; PROMOTER REGION; TUMOR SUPPRESSOR GENE;

ADENOCARCINOMA; ADENOMATOUS POLYPOSIS COLI; ANIMALS; BILE ACIDS AND SALTS; COLON; COLONIC NEOPLASMS; CYCLOOXYGENASE 2; DNA METHYLATION; GENE EXPRESSION; GENE SILENCING; GENES, APC; HCT116 CELLS; HT29 CELLS; HUMANS; MICE, INBRED C57BL; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-MYC; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84959301201     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.115.216580     Document Type: Article

References (48)

1. Modica S, Gadaleta RM, Moschetta A. Deciphering the nuclear bile acid receptor FXR paradigm. Nucl Recept Signal 2010;8:e005.
2. De Gottardi A, Touri F, Maurer CA, Perez A, Maurhofer O, Ventre G, Bentzen CL, Niesor EJ, Dufour JF. The bile acid nuclear receptor FXR and the bile acid binding protein IBABP are differently expressed in colon cancer. Dig Dis Sci 2004;49:982-9.
3. Lax S, Schauer G, Prein K, Kapitan M, Silbert D, Berghold A, Berger A, Trauner M. Expression of the nuclear bile acid receptor/farnesoid X receptor is reduced in human colon carcinoma compared to nonneoplastic mucosa independent from site and may be associated with adverse prognosis. Int J Cancer 2012;130:2232-9.
4. Maran RR, Thomas A, Roth M, Sheng Z, Esterly N, Pinson D, Gao X, Zhang Y, Ganapathy V, Gonzalez FJ, et al. Farnesoid X receptor deficiency in mice leads to increased intestinal epithelial cell proliferation and tumor development. J Pharmacol Exp Ther 2009;328:469-77.
5. Modica S, Murzilli S, Salvatore L, Schmidt DR, Moschetta A. Nuclear bile acid receptor FXR protects against intestinal tumorigenesis. Cancer Res 2008;68:9589-94.
6. Imray CH, Radley S, Davis A, Barker G, Hendrickse CW, Donovan IA, Lawson AM, Baker PR, Neoptolemos JP. Faecal unconjugated bile acids in patients with colorectal cancer or polyps. Gut 1992;33:1239-45.
7. Bayerdörffer E, Mannes GA, Richter WO, Ochsenkühn T, Wiebecke B, Köpcke W, Paumgartner G. Increased serum deoxycholic acid levels in men with colorectal adenomas. Gastroenterology 1993;104:145-51.
8. Reddy BS, Watanabe K, Weisburger JH, Wynder EL. Promoting effect of bile acids in colon carcinogenesis in germ-free and conventional F344 rats. Cancer Res 1977;37:3238-42.
9. Rainey JB, Maeda M, Williams C, Williamson RC. The cocarcinogenic effect of intrarectal deoxycholate in rats is reduced by oral metronidazole. Br J Cancer 1984;49:631-6.
10. Flynn C, Montrose DC, Swank DL, Nakanishi M, Ilsley JN, Rosenberg DW. Deoxycholic acid promotes the growth of colonic aberrant crypt foci. Mol Carcinog 2007;46:60-70.
11. Powell SM, Zilz N, Beazer-Barclay Y, Bryan TM, Hamilton SR, Thibodeau SN, Vogelstein B, Kinzler KW. APC mutations occur early during colorectal tumorigenesis. Nature 1992;359:235-7.
12. Kinzler KW, Nilbert MC, Su LK, Vogelstein B, Bryan TM, Levy DB, Smith KJ, Preisinger AC, Hedge P, McKechnie D, et al. Identification of FAP locus genes from chromosome 5q21. Science 1991;253:661-5.
13. Korinek V, Barker N, Morin PJ, van Wichen D, de Weger R, Kinzler KW, Vogelstein B, Clevers H. Constitutive transcriptional activation by a betacatenin-Tcf complex in APC-/-colon carcinoma. Science 1997;275:1784-7.
14. Morin PJ, Sparks AB, Korinek V, Barker N, Clevers H, Vogelstein B, Kinzler KW. Activation of beta-catenin-Tcf signaling in colon cancer by mutations in beta-catenin or APC. Science 1997;275:1787-90.
15. Tetsu O, McCormick F. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 1999;398:422-6.
16. Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R, Ben-Ze'ev A. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci USA 1999;96:5522-7.
17. He TC, Sparks AB, Rago C, Hermeking H, Zawel L, da Costa LT, Morin PJ, Vogelstein B, Kinzler KW. Identification of c-MYC as a target of the APC pathway. Science 1998;281:1509-12.
18. McCart AE, Vickaryous NK, Silver A. Apc mice: models, modifiers and mutants. Pathol Res Pract 2008;204:479-90.
19. Yamada Y, Mori H. Multistep carcinogenesis of the colon in Apc(Min/+) mouse. Cancer Sci 2007;98:6-10.
20. Ilyas M, Tomlinson IP, Rowan A, Pignatelli M, Bodmer WF. Betacatenin mutations in cell lines established from human colorectal cancers. Proc Natl Acad Sci USA 1997;94:10330-4.
21. Stenman LK, Holma R, Korpela R. High-fat-induced intestinal permeability dysfunction associated with altered fecal bile acids. World J Gastroenterol 2012;18:923-9.
22. Bianchini F, Caderni G, Dolara P, Fantetti L, Kriebel D. Effect of dietary fat, starch and cellulose on fecal bile acids in mice. J Nutr 1989;119:1617-24.
23. Suzuki R, Miyamoto S, Yasui Y, Sugie S, Tanaka T. Global gene expression analysis of the mouse colonic mucosa treated with azoxymethane and dextran sodium sulfate. BMC Cancer 2007;7:84.
24. Sinal CJ, Tohkin M, Miyata M, Ward JM, Lambert G, Gonzalez FJ. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 2000;102:731-44.
25. Kemp MQ, Jeffy BD, Romagnolo DF. Conjugated linoleic acid inhibits cell proliferation through a p53-dependent mechanism: effects on the expression of G1-restriction points in breast and colon cancer cells. J Nutr 2003;133:3670-7.
26. Kellermayer R, Dowd SE, Harris RA, Balasa A, Schaible TD, Wolcott RD, Tatevian N, Szigeti R, Li Z, Versalovic J, et al. Colonic mucosal DNA methylation, immune response, and microbiome patterns in Tolllike receptor 2-knockout mice. FASEB J 2011;25:1449-60.
27. Papoutsis AJ, Lamore SD, Wondrak GT, Selmin OI, Romagnolo DF. Resveratrol prevents epigenetic silencing of BRCA-1 by the aromatic hydrocarbon receptor in human breast cancer cells. J Nutr 2010;140: 1607-14.
28. Papoutsis AJ, Selmin OI, Borg JL, Romagnolo DF. Gestational exposure to theAhR agonist 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin induces BRCA-1 promoterhypermethylation and reduces BRCA-1 expression in mammary tissue of ratoffspring: Preventive effects of resveratrol. Mol Carcinog 2015;54:261-9.
29. Niho N, Takahashi M, Kitamura T, Shoji Y, Itoh M, Noda T, Sugimura T, Wakabayashi K. Concomitant suppression of hyperlipidemia and intestinal polyp formation in Apc-deficient mice by peroxisome proliferator-activated receptor ligands. Cancer Res 2003;63:6090-5.
30. Sano H, Kawahito Y, Wilder RL, Hashiramoto A, Mukai S, Asai K, Kimura S, Kato H, Kondo M, Hla T. Expression of cyclooxygenase-1 and-2 in human colorectal cancer. Cancer Res 1995;55:3785-9.
31. National Cancer Institute. Surveillance, epidemiology, and end results program [cited 2015 Apr 23]. Available from: http://seer.cancer.gov.
32. Modica S, Petruzzelli M, Bellafante E, Murzilli S, Salvatore L, Celli N, Di Tullio G, Palasciano G, Moustafa T, Halilbasic E, et al. Selective activation of nuclear bile acid receptor FXR in the intestine protects mice against cholestasis. Gastroenterology 2012;142:355-65.e1-4.
33. Wang YD, Chen WD, Wang M, Yu D, Forman BM, Huang W. Farnesoid X receptor antagonizes nuclear factor kappaB in hepatic inflammatory response. Hepatology 2008;48:1632-43.
34. Silviera ML, Smith BP, Powell J, Sapienza C. Epigenetic differences in normal colon mucosa of cancer patients suggest altered dietary metabolic pathways. Cancer Prev Res (Phila) 2012;5:374-84.
35. Bailey AM, Zhan L, Maru D, Shureiqi I, Pickering CR, Kiriakova G, Izzo J, He N, Wei C, Baladandayuthapani V, et al. FXR silencing in human colon cancer by DNA methylation and KRAS signaling. Am J Physiol Gastrointest Liver Physiol 2014;306:G48-58.
36. Zhang Y, Kast-Woelbern HR, Edwards PA. Natural structural variants of the nuclear receptor farnesoid X receptor affect transcriptional activation. J Biol Chem 2003;278:104-10.
37. Huber RM, Murphy K, Miao B, Link JR, Cunningham MR, Rupar MJ, Gunyuzlu PL, Haws TF, Kassam A, Powell F, et al. Generation of multiple farnesoid-X-receptor isoforms through the use of alternative promoters. Gene 2002;290:35-43.
38. Senda T, Iizuka-Kogo A, Onouchi T, Shimomura A. Adenomatous polyposis coli (APC) plays multiple roles in the intestinal and colorectal epithelia. Med Mol Morphol 2007;40:68-81.
39. Degirolamo C, Modica S, Palasciano G, Moschetta A. Bile acids and colon cancer: solving the puzzle with nuclear receptors. Trends Mol Med 2011;17:564-72.
40. Parks DJ, Blanchard SG, Bledsoe RK, Chandra G, Consler TG, Kliewer SA, Stimmel JB, Willson TM, Zavacki AM, Moore DD, et al. Bile acids: natural ligands for an orphan nuclear receptor. Science 1999;284:1365-8.
41. Smith DL, Keshavan P, Avissar U, Ahmed K, Zucker SD. Sodium taurocholate inhibits intestinal adenoma formation in APCMin/+ mice, potentially through activation of the farnesoid X receptor. Carcinogenesis 2010;31:1100-9.
42. Tang FY, Pai MH, Chiang EP. Consumption of high-fat diet induces tumor progression and epithelial-mesenchymal transition of colorectal cancer in a mouse xenograft model. J Nutr Biochem 2012;23:1302-13.
43. Mai V, Colbert LH, Perkins SN, Schatzkin A, Hursting SD. Intestinal microbiota: a potential diet-responsive prevention target in ApcMin mice. Mol Carcinog 2007;46:42-8.
44. Grimm C, Chavez L, Vilardell M, Farrall AL, Tierling S, Böhm JW, Grote P, Lienhard M, Dietrich J, Timmermann B, et al. DNAmethylome analysis of mouse intestinal adenoma identifies a tumourspecific signature that is partly conserved in human colon cancer. PLoS Genet 2013;9:e1003250.
45. Forn M, Díez-Villanueva A, Merlos-Suárez A, Muñoz M, Lois S, Carriò E, Jordà M, Bigas A, Batlle E, Peinado MA. Overlapping DNA methylation dynamics in mouse intestinal cell differentiation and early stages of malignant progression. PLoS One 2015;10:e0123263.
46. Mills SC, Windsor AC, Knight SC. The potential interactions between polyunsaturated fatty acids and colonic inflammatory processes. Clin Exp Immunol 2005;142:216-28.
47. Tjonneland A, Overvad K, Bergmann MM, Nagel G, Linseisen J, Hallmans G, Palmqvist R, Sjodin H, Hagglund G, Berglund G, et al. Linoleic acid, a dietary n-6 polyunsaturated fatty acid, and the aetiology of ulcerative colitis: a nested case-control study within a European prospective cohort study. Gut 2009;58:1606-11.
48. Day SD, Enos RT, McClellan JL, Steiner JL, Velázquez KT, Murphy EA. Linking inflammation to tumorigenesis in a mouse model of high-fatdiet-enhanced colon cancer. Cytokine 2013;64:454-62.