Bile acids and colon cancer: Solving the puzzle with nuclear receptors

Trends in Molecular Medicine

Volumn 17, Issue 10, 2011, Pages 564-572

  Degirolamo, Chiara ^a   Modica, Salvatore ^a,c   Palasciano, Giuseppe ^b   Moschetta, Antonio ^a,b  

^a Santa Maria Imbaro   (Italy)

^b UNIVERSITY OF BARI   (Italy)

^c ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; BILE ACID; CARBONATE DEHYDRATASE XII; CELL NUCLEUS RECEPTOR; CHENODEOXYCHOLIC ACID; CHOLIC ACID; CONSTITUTIVE ANDROSTANE RECEPTOR; CYTOCHROME C; DEOXYCHOLIC ACID; EPIDERMAL GROWTH FACTOR RECEPTOR; FARNESOID X RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 18; LITHOCHOLIC ACID; PREGNANE X RECEPTOR; PROTEIN KINASE C; SATURATED FATTY ACID; URSODEOXYCHOLIC ACID; VITAMIN D RECEPTOR; WNT PROTEIN;

ANEUPLOIDY; APOPTOSIS; CANCER GROWTH; CANCER RISK; CANCER SUSCEPTIBILITY; CELL CYCLE ARREST; CELL DEATH; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CHOLESTEROL METABOLISM; CHROMOSOMAL INSTABILITY; COLON CARCINOGENESIS; COLORECTAL CANCER; CRYPT CELL; DETOXIFICATION; DNA DAMAGE; ENZYME ACTIVATION; FRUIT; GARLIC; GLUCOSE HOMEOSTASIS; HOMEOSTASIS; HYDROPHOBICITY; INFLAMMATION; INTESTINE CELL; INTESTINE EPITHELIUM; LIFESTYLE; LIVER CELL CARCINOMA; METAPHASE; MITOSIS; NONHUMAN; OVERALL SURVIVAL; POINT MUTATION; PROTEIN EXPRESSION; RED MEAT; REVIEW; SIGNAL TRANSDUCTION; THERMOGENESIS; TUMOR GENE; VEGETABLE;

ANIMALS; BILE ACIDS AND SALTS; COLON; COLONIC NEOPLASMS; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTESTINAL MUCOSA; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 80052771111     PISSN: 14714914     EISSN: 1471499X     Source Type: Journal    
DOI: 10.1016/j.molmed.2011.05.010     Document Type: Review

References (79)

1. Karsa L.V., et al. The dimensions of the CRC problem. Best Pract. Res. Clin. Gastroenterol. 2010, 24:381-396.
2. Pearson J.R., et al. Diet, fecal water, and colon cancer - development of a biomarker. Nutr. Rev. 2009, 67:509-526.
3. Berg A. Nutrition, development, and population growth. Popul. Bull. 1973, 29:3-37.
4. Chao A., et al. Meat consumption and risk of colorectal cancer. JAMA 2005, 293:172-182.
5. Kirkegaard H., et al. Association of adherence to lifestyle recommendations and risk of colorectal cancer: a prospective Danish cohort study. BMJ 2010, 341:c5504.
6. Bajor A., et al. Bile acids: short and long term effects in the intestine. Scand. J. Gastroenterol. 2010, 45:645-664.
7. McGarr S.E., et al. Diet, anaerobic bacterial metabolism, and colon cancer: a review of the literature. J. Clin. Gastroenterol. 2005, 39:98-109.
8. Bernstein, C. et al. Carcinogenicity of deoxycholate, a secondary bile acid. Arch. Toxicol. (in press).
9. Schmidt D.R., Mangelsdorf D.J. Nuclear receptors of the enteric tract: guarding the frontier. Nutr. Rev. 2008, 66:S88-S97.
10. Modica S., et al. The intestinal nuclear receptor signature with epithelial localization patterns and expression modulation in tumors. Gastroenterology 2010, 138:636-648. 648.e1-12.
11. Barker N., et al. Identification of stem cells in small intestine and colon by marker gene Lgr5. Nature 2007, 449:1003-1007.
12. Snippert H.J., et al. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell 2010, 143:134-144.
13. Schneikert J., Behrens J. The canonical Wnt signalling pathway and its APC partner in colon cancer development. Gut 2007, 56:417-425.
14. D'Errico I., Moschetta A. Nuclear receptors, intestinal architecture and colon cancer: an intriguing link. Cell. Mol. Life Sci. 2008, 65:1523-1543.
15. Clarke A.R. Wnt signalling in the mouse intestine. Oncogene 2006, 25:7512-7521.
16. van Es J.H., Clevers H. Notch and Wnt inhibitors as potential new drugs for intestinal neoplastic disease. Trends Mol. Med. 2005, 11:496-502.
17. Krause W.F., DuBois R.N. The molecular basis for prevention of colorectal cancer. Clin. Colorectal Cancer 2001, 1:47-54.
18. Kinzler K.W., Vogelstein B. Lessons from hereditary colorectal cancer. Cell 1996, 87:159-170.
19. Janssen K.P., et al. APC and oncogenic KRAS are synergistic in enhancing Wnt signaling in intestinal tumor formation and progression. Gastroenterology 2006, 131:1096-1109.
20. Williams B.R., et al. Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science 2008, 322:703-709.
21. Hofmann A.F. The enterohepatic circulation of bile acids in mammals: form and functions. Front Biosci. 2009, 14:2584-2598.
22. Watanabe M., et al. Bile acids induce energy expenditure by promoting intracellular thyroid hormone activation. Nature 2006, 439:484-489.
23. Keitel V., et al. Endocrine and paracrine role of bile acids. World J. Gastroenterol. 2008, 14:5620-5629.
24. Ma K., et al. Farnesoid X receptor is essential for normal glucose homeostasis. J. Clin. Invest. 2006, 116:1102-1109.
25. Thomas C., et al. TGR5-mediated bile acid sensing controls glucose homeostasis. Cell Metab. 2009, 10:167-177.
26. Thomas C., et al. Targeting bile-acid signalling for metabolic diseases. Nat. Rev. Drug Discov. 2008, 7:678-693.
27. Chiang J.Y. Bile acids: regulation of synthesis. J. Lipid Res. 2009, 50:1955-1966.
28. Miyake J.H., et al. Bile acid induction of cytokine expression by macrophages correlates with repression of hepatic cholesterol 7alpha-hydroxylase. J. Biol. Chem. 2000, 275:21805-21808.
29. Hofmann A.F. Detoxification of lithocholic acid, a toxic bile acid: relevance to drug hepatotoxicity. Drug Metab. Rev. 2004, 36:703-722.
30. Perez M.J., Briz O. Bile-acid-induced cell injury and protection. World J. Gastroenterol. 2009, 15:1677-1689.
31. Uppal H., et al. Combined loss of orphan receptors PXR and CAR heightens sensitivity to toxic bile acids in mice. Hepatology 2005, 41:168-176.
32. Nomoto M., et al. Bile acid-induced elevated oxidative stress in the absence of farnesoid X receptor. Biol. Pharm. Bull. 2009, 32:172-178.
33. Nagengast F.M., et al. Role of bile acids in colorectal carcinogenesis. Eur. J. Cancer 1995, 31A:1067-1070.
34. Cheng K., Raufman J.P. Bile acid-induced proliferation of a human colon cancer cell line is mediated by transactivation of epidermal growth factor receptors. Biochem. Pharmacol. 2005, 70:1035-1047.
35. Jean-Louis S., et al. Deoxycholic acid induces intracellular signaling through membrane perturbations. J. Biol. Chem. 2006, 281:14948-14960.
36. Zeng H., et al. Deoxycholic acid and selenium metabolite methylselenol exert common and distinct effects on cell cycle, apoptosis, and MAP kinase pathway in HCT116 human colon cancer cells. Nutr. Cancer 2010, 62:85-92.
37. Yui S., et al. Biphasic regulation of cell death and survival by hydrophobic bile acids in HCT116 cells. Nutr. Cancer 2009, 61:374-380.
38. Bernstein C., et al. A bile acid-induced apoptosis assay for colon cancer risk and associated quality control studies. Cancer Res. 1999, 59:2353-2357.
39. Amaral J.D., et al. Bile acids: regulation of apoptosis by ursodeoxycholic acid. J. Lipid Res. 2009, 50:1721-1734.
40. Yui S., et al. Deoxycholic acid can induce apoptosis in the human colon cancer cell line HCT116 in the absence of Bax. Nutr. Cancer 2008, 60:91-96.
41. Katona B.W., et al. Characterization of enantiomeric bile acid-induced apoptosis in colon cancer cell lines. J. Biol. Chem. 2009, 284:3354-3364.
42. Payne C.M., et al. Deoxycholate induces mitochondrial oxidative stress and activates NF-kappaB through multiple mechanisms in HCT-116 colon epithelial cells. Carcinogenesis 2007, 28:215-222.
43. Payne C.M., et al. Hydrophobic bile acid-induced micronuclei formation, mitotic perturbations, and decreases in spindle checkpoint proteins: relevance to genomic instability in colon carcinogenesis. Nutr. Cancer 2010, 62:825-840.
44. Kim N.D., et al. Modulation of the cell cycle and induction of apoptosis in human cancer cells by synthetic bile acids. Curr. Cancer Drug Targets 2006, 6:681-689.
45. Chawla A., et al. Nuclear receptors and lipid physiology: opening the X-files. Science 2001, 294:1866-1870.
46. Makishima M., et al. Identification of a nuclear receptor for bile acids. Science 1999, 284:1362-1365.
47. Parks D.J., et al. Bile acids: natural ligands for an orphan nuclear receptor. Science 1999, 284:1365-1368.
48. Wang H., et al. Endogenous bile acids are ligands for the nuclear receptor FXR/BAR. Mol. Cell 1999, 3:543-553.
49. Sinal C.J., et al. Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 2000, 102:731-744.
50. Kok T., et al. Enterohepatic circulation of bile salts in farnesoid X receptor-deficient mice: efficient intestinal bile salt absorption in the absence of ileal bile acid-binding protein. J. Biol. Chem. 2003, 278:41930-41937.
51. Gadaleta R.M., et al. Bile acids and their nuclear receptor FXR: relevance for hepatobiliary and gastrointestinal disease. Biochim. Biophys. Acta 2010, 1801:683-692.
52. Inagaki T., et al. Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab. 2005, 2:217-225.
53. Dawson P.A., et al. The heteromeric organic solute transporter alpha-beta, Ostalpha-Ostbeta, is an ileal basolateral bile acid transporter. J. Biol. Chem. 2005, 280:6960-6968.
54. Ballatori N., et al. OSTalpha-OSTbeta: a major basolateral bile acid and steroid transporter in human intestinal, renal, and biliary epithelia. Hepatology 2005, 42:1270-1279.
55. Inagaki T., et al. Regulation of antibacterial defense in the small intestine by the nuclear bile acid receptor. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:3920-3925.
56. Stedman C., et al. Feed-forward regulation of bile acid detoxification by CYP3A4: studies in humanized transgenic mice. J. Biol. Chem. 2004, 279:11336-11343.
57. Makishima M., et al. Vitamin D receptor as an intestinal bile acid sensor. Science 2002, 296:1313-1316.
58. Xie W., et al. Humanized xenobiotic response in mice expressing nuclear receptor SXR. Nature 2000, 406:435-439.
59. Kliewer S.A., et al. An orphan nuclear receptor activated by pregnanes defines a novel steroid signaling pathway. Cell 1998, 92:73-82.
60. Zhou J., et al. The antiapoptotic role of pregnane X receptor in human colon cancer cells. Mol. Endocrinol. 2008, 22:868-880.
61. Owen B.M., et al. Intestinal detoxification limits the activation of hepatic pregnane X receptor by lithocholic acid. Drug Metab. Dispos. 2010, 38:143-149.
62. Yang F., et al. Spontaneous development of liver tumors in the absence of the bile acid receptor farnesoid X receptor. Cancer Res. 2007, 67:863-867.
63. Kim I., et al. Spontaneous hepatocarcinogenesis in farnesoid X receptor-null mice. Carcinogenesis 2007, 28:940-946.
64. De Gottardi A., et al. The bile acid nuclear receptor FXR and the bile acid binding protein IBABP are differently expressed in colon cancer. Dig. Dis. Sci. 2004, 49:982-989.
65. Modica S., et al. Nuclear bile acid receptor FXR protects against intestinal tumorigenesis. Cancer Res. 2008, 68:9589-9594.
66. Maran R.R., et al. Farnesoid X receptor deficiency in mice leads to increased intestinal epithelial cell proliferation and tumor development. J. Pharmacol. Exp. Ther. 2009, 328:469-477.
67. Schneider H. A factor in the increased risk of colorectal cancer due to ingestion of animal fat is inhibition of colon epithelial cell glutathione S-transferase, an enzyme that detoxifies mutagens. Med. Hypotheses 1992, 39:119-122.
68. Schmidt D.R., et al. AKR1B7 is induced by the farnesoid X receptor and metabolizes bile acids. J. Biol. Chem. 2011, 286:2425-2432.
69. Hamilton J.P., et al. Human cecal bile acids: concentration and spectrum. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293:G256-G263.
70. Gadaleta R.M., et al. Farnesoid X receptor activation inhibits inflammation and preserves the intestinal barrier in inflammatory bowel disease. Gut 2011, 60:463-472.
71. Clevers H. The cancer stem cell: premises, promises and challenges. Nat. Med. 2011, 17:313-319.
72. Min+/- mice, potentially through activation of the farnesoid X receptor. Carcinogenesis 2010, 31:1100-1109.
73. Barker N., et al. Crypt stem cells as the cells-of-origin of intestinal cancer. Nature 2009, 457:608-611.
74. Zhu L., et al. Prominin 1 marks intestinal stem cells that are susceptible to neoplastic transformation. Nature 2009, 457:603-607.
75. Sangiorgi E., Capecchi M.R. Bmi1 is expressed in vivo in intestinal stem cells. Nat. Genet. 2008, 40:915-920.
76. Spence J.R., et al. Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro. Nature 2011, 470:105-109.
77. Maruyama T., et al. Identification of membrane-type receptor for bile acids (M-BAR). Biochem. Biophys. Res. Commun. 2002, 298:714-719.
78. Hong J., et al. Role of a novel bile acid receptor TGR5 in the development of oesophageal adenocarcinoma. Gut 2010, 59:170-180.
79. Yasuda H., et al. Involvement of membrane-type bile acid receptor M-BAR/TGR5 in bile acid-induced activation of epidermal growth factor receptor and mitogen-activated protein kinases in gastric carcinoma cells. Biochem. Biophys. Res. Commun. 2007, 354:154-159.