Hepatocyte nuclear factor 4α in the intestinal epithelial cells protects against inflammatory bowel disease

Inflammatory Bowel Diseases

Volumn 14, Issue 7, 2008, Pages 908-920

  Ahn, Sung Hoon ^a   Shah, Yatrik M ^a   Inoue, Junko ^a   Morimura, Keiichirou ^b   Kim, Insook ^a   Yim, SunHee ^a   Lambert, Gilles ^c,d   Kurotani, Reiko ^a,e   Nagashima, Kunio ^f   Gonzalez, Frank J ^a   Inoue, Yusuke ^a,g  

^a NATIONAL CANCER INSTITUTE   (United States)

^b OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c UNIVERSITÉ DE NANTES   (France)

^d HEART RESEARCH INSTITUTE   (Australia)

^e YOKOHAMA CITY UNIVERSITY   (Japan)

^f NATIONAL CANCER INSTITUTE   (United States)

^g GUNMA UNIVERSITY   (Japan)

Author keywords

Colitis; Hepatocyte nuclear factor 4 ; HNF4 ; Intestinal epithelial cell; Nuclear receptors

Indexed keywords

DEXTRAN SULFATE; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; MESSENGER RNA; MUCIN;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROL GROUP; CONTROLLED STUDY; CROHN DISEASE; ENTERITIS; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; INTESTINE BIOPSY; INTESTINE EPITHELIUM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENE; ULCERATIVE COLITIS; WEIGHT REDUCTION;

ADULT; AGED; ANIMALS; AQUAPORINS; BLOTTING, NORTHERN; BLOTTING, WESTERN; COLITIS, ULCERATIVE; COLON; CROHN DISEASE; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION; HEPATOCYTE NUCLEAR FACTOR 4; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINES; MALE; MICE; MIDDLE AGED; MUCINS; POLYMERASE CHAIN REACTION; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, MESSENGER; THIOPRONINE;

EID: 47949083278     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.20413     Document Type: Article

References (75)

1. Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347:417-429.
2. Bouma G, Strober W. The immunological and genetic basis of inflammatory bowel disease. Nat Rev Immunol. 2003;3:521-533.
3. Froicu M, Weaver V, Wynn TA, et al. A crucial role for the vitamin D receptor in experimental inflammatory bowel diseases. Mol Endocrinol. 2003;17:2386-2392.
4. Lim WC, Hanauer SB, Li YC. Mechanisms of disease: vitamin D and inflammatory bowel disease. Nat Clin Pract Gastroenterol Hepatol. 2005;2:308-315.
5. Dubuquoy L, Jansson EA, Deeb S, et al. Impaired expression of peroxisome proliferator-activated receptor gamma in ulcerative colitis. Gastroenterology. 2003;124:1265-1276.
6. Katayama K, Wada K, Nakajima A, et al. A novel PPAR gamma gene therapy to control inflammation associated with inflammatory bowel disease in a murine model. Gastroenterology. 2003;124:1315-1324.
7. Adachi M, Kurotani R, Morimura K, et al. Peroxisome proliferator activated receptor gamma in colonic epithelial cells protects against experimental inflammatory bowel disease. Gut. 2006;55:1104-1113.
8. Cuzzocrea S, Di Paola R, Mazzon E, et al. Role of endogenous and exogenous ligands for the peroxisome proliferators activated receptors alpha (PPAR-alpha) in the development of inflammatory bowel disease in mice. Lab Invest. 2004;84:1643-1654.
9. Bassaganya-Riera J, Reynolds K, Martino-Catt S, et al. Activation of PPAR gamma and delta by conjugated linoleic acid mediates protection from experimental inflammatory bowel disease. Gastroenterology. 2004;127:777-791.
10. Langmann T, Moehle C, Mauerer R, et al. Loss of detoxification in inflammatory bowel disease: dysregulation of pregnane X receptor target genes. Gastroenterology. 2004;127:26-40.
11. Shah YM, Ma X, Morimura K, et al. Pregnane X receptor activation ameliorates DSS-induced inflammatory bowel disease via inhibition of NF-kappaB target gene expression. Am J Physiol Gastrointest Liver Physiol. 2007;292:G1114-1122.
12. Schottelius A, Wedel S, Weltrich R, et al. Higher expression of glucocorticoid receptor in peripheral mononuclear cells in inflammatory bowel disease. Am J Gastroenterol. 2000;95:1994-1999.
13. Stange EF. Glucocorticoid receptor activity in inflammatory bowel disease: hindsight or foresight? Eur J Clin Invest. 1999;29:278-279.
14. Sladek FM, Zhong WM, Lai E, et al. Liver-enriched transcription factor HNF-4 is a novel member of the steroid hormone receptor superfamily. Genes Dev. 1990;4:2353-2365.
15. Schrem H, Klempnauer J, Borlak J. Liver-enriched transcription factors in liver function and development. Part I. The hepatocyte nuclear factor network and liver-specific gene expression. Pharmacol Rev. 2002;54:129-158.
16. Drewes T, Senkel S, Holewa B, et al. Human hepatocyte nuclear factor 4 isoforms are encoded by distinct and differentially expressed genes. Mol Cell Biol. 1996;16:925-931.
17. Jiang S, Tanaka T, Iwanari H, et al. Expression and localization of P1 promoter-driven hepatocyte nuclear factor-4alpha (HNF4alpha) isoforms in human and rats. Nucl Recept. 2003;1:5.
18. Chen WS, Manova K, Weinstein DC, et al. Disruption of the HNF-4 gene, expressed in visceral endoderm, leads to cell death in embryonic ectoderm and impaired gastrulation of mouse embryos. Genes Dev. 1994;8:2466-2477.
19. Hayhurst GP, Lee YH, Lambert G, et al. Hepatocyte nuclear factor 4alpha (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol Cell Biol. 2001;21:1393-1403.
20. Inoue Y, Hayhurst GP, Inoue J, et al. Defective ureagenesis in mice carrying a liver-specific disruption of hepatocyte nuclear factor 4alpha (HNF4alpha). HNF4alpha regulates ornithine transcarbamylase in vivo. J Biol Chem. 2002;277:25257-25265.
21. Rhee J, Inoue Y, Yoon JC, et al. Regulation of hepatic fasting response by PPARgamma coactivator-1alpha (PGC-1): requirement for hepatocyte nuclear factor 4alpha in gluconeogenesis. Proc Natl Acad Sci U S A. 2003;100:4012-4017.
22. Kamiya A, Inoue Y, Kodama T, et al. Hepatocyte nuclear factors 1 alpha and 4alpha control expression of proline oxidase in adult liver. FEBS Lett. 2004;578:63-68.
23. Inoue Y, Yu AM, Yim SH, et al. Regulation of bile acid biosynthesis by hepatocyte nuclear factor 4alpha. J Lipid Res. 2006;47:215-227.
24. Inoue Y, Peters LL, Yim SH, et al. Role of hepatocyte nuclear factor 4alpha in control of blood coagulation factor gene expression. J Mol Med. 2006;84:334-344.
25. Miura A, Yamagata K, Kakei M, et al. Hepatocyte nuclear factor-4alpha is essential for glucose-stimulated insulin secretion by pancreatic beta-cells. J Biol Chem. 2006;281:5246-5257.
26. Gupta RK, Vatamaniuk MZ, Lee CS, et al. The MODY1 gene HNF-4alpha regulates selected genes involved in insulin secretion. J Clin Invest. 2005;115:1006-1015.
27. Ginsburg GS, Ozer J, Karathanasis SK. Intestinal apolipoprotein AI gene transcription is regulated by multiple distinct DNA elements and is synergistically activated by the orphan nuclear receptor, hepatocyte nuclear factor 4. J Clin Invest. 1995;96:528-538.
28. Ochoa A, Bovard-Houppermans S, Zakin MM. Human apolipoprotein A-IV gene expression is modulated by members of the nuclear hormone receptor superfamily. Biochim Biophys Acta. 1993;1210:41-47.
29. Antes TJ, Levy-Wilson B. HNF-3 beta, C/EBP beta, and HNF-4 act in synergy to enhance transcription of the human apolipoprotein B gene in intestinal cells. DNA Cell Biol. 2001;20:67-74.
30. Swenson ES, Mann EA, Jump ML, et al. Hepatocyte nuclear factor-4 regulates intestinal expression of the guanylin/heat-stable toxin receptor. Am J Physiol. 1999;276:G728-736.
31. Tegude H, Schnabel A, Zanger UM, et al. Molecular mechanism of basal CYP3A4 regulation by hepatocyte nuclear factor 4{alpha}: evidence for direct regulation in the intestine. Drug Metab Dispos. 2007;35:946-954.
32. Olsen L, Bressendorff S, Troelsen JT, et al. Differentiation-dependent activation of the human intestinal alkaline phosphatase promoter by HNF-4 in intestinal cells. Am J Physiol Gastrointest Liver Physiol. 2005;289:G220-226.
33. Stegmann A, Hansen M, Wang Y, et al. Metabolome, transcriptome, and bioinformatic cis-element analyses point to HNF-4 as a central regulator of gene expression during enterocyte differentiation. Physiol Genomics. 2006;27:141-155.
34. Garrison WD, Battle MA, Yang C, et al. Hepatocyte nuclear factor 4alpha is essential for embryonic development of the mouse colon. Gastroenterology. 2006;130:1207-1220.
35. Madison BB, Dunbar L, Qiao XT, et al. Cis elements of the villin gene control expression in restricted domains of the vertical (crypt) and horizontal (duodenum, cecum) axes of the intestine. J Biol Chem. 2002;277:33275-33283.
36. Cooper HS, Murthy SN, Shah RS, et al. Clinicopathologic study of dextran sulfate sodium experimental murine colitis. Lab Invest. 1993;69:238-249.
37. Shah YM, Morimura K, Gonzalez FJ. Expression of peroxisome proliferator-activated receptor-gamma in macrophage suppresses experimentally induced colitis. Am J Physiol Gastrointest Liver Physiol. 2007;292:G657-666.
38. Bond JS, Matters GL, Banerjee S, et al. Meprin metalloprotease expression and regulation in kidney, intestine, urinary tract infections and cancer. FEBS Lett. 2005;579:3317-3322.
39. King LS, Kozono D, Agre P. From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol. 2004;5:687-698.
40. Verkman AS, Mitra AK. Structure and function of aquaporin water channels. Am J Physiol Renal Physiol. 2000;278:F13-28.
41. Jass JR, Walsh MD. Altered mucin expression in the gastrointestinal tract: a review. J Cell Mol Med. 2001;5:327-351.
42. Byrd JC, Bresalier RS. Mucins and mucin binding proteins in colorectal cancer. Cancer Metastasis Rev. 2004;23:77-99.
43. Amasheh S, Barmeyer C, Koch CS, et al. Cytokine-dependent transcriptional down-regulation of epithelial sodium channel in ulcerative colitis. Gastroenterology. 2004;126:1711-1720.
44. Takahashi KI, Fukushima K, Sasano H, et al. Type II 11beta-hydroxysteroid dehydrogenase expression in human colonic epithelial cells of inflammatory bowel disease. Dig Dis Sci. 1999;44:2516-2522.
45. Seril DN, Liao J, Yang GY, et al. Oxidative stress and ulcerative colitis-associated carcinogenesis: studies in humans and animal models. Carcinogenesis. 2003;24:353-362.
46. Sartor RB. Current concepts of the etiology and pathogenesis of ulcerative colitis and Crohn's disease. Gastroenterol Clin North Am. 1995;24:475-507.
47. Lugering N, Kucharzik T, Stoll R, et al. Current concept of the role of monocytes/macrophages in inflammatory bowel disease - balance of proinflammatory and immunosuppressive mediators. Ital J Gastroenterol Hepatol. 1998;30:338-344.
48. Papadakis KA, Targan SR. Role of cytokines in the pathogenesis of inflammatory bowel disease. Annu Rev Med. 2000;51:289-298.
49. Brynskov J, Tvede N, Andersen CB, et al. Increased concentrations of interleukin 1 beta, interleukin-2, and soluble interleukin-2 receptors in endoscopical mucosal biopsy specimens with active inflammatory bowel disease. Gut. 1992;33:55-58.
50. Cappello M, Keshav S, Prince C, et al. Detection of mRNAs for macrophage products in inflammatory bowel disease by in situ hybridisation. Gut. 1992;33:1214-1219.
51. Reinecker HC, Steffen M, Witthoeft T, et al. Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1 beta by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn's disease. Clin Exp Immunol. 1993;94:174-181.
52. De Bosscher K, Vanden Berghe W, Haegeman G. Cross-talk between nuclear receptors and nuclear factor kappaB. Oncogene. 2006;25:6868-6886.
53. Guo H, Wei J, Inoue Y, et al. Serine/threonine phosphorylation regulates HNF-4alpha-dependent redox-mediated iNOS expression in hepatocytes. Am J Physiol Cell Physiol. 2003;284:C1090-1099.
54. Nikolaidou-Neokosmidou V, Zannis VI, Kardassis D. Inhibition of hepatocyte nuclear factor 4 transcriptional activity by the nuclear factor kappaB pathway. Biochem J. 2006;398:439-450.
55. Moniaux N, Escande F, Porchet N, et al. Structural organization and classification of the human mucin genes. Front Biosci. 2001;6:D1192-1206.
56. Satsangi J, Parkes M, Louis E, et al. Two stage genome-wide search in inflammatory bowel disease provides evidence for susceptibility loci on chromosomes 3, 7 and 12. Nat Genet. 1996;14:199-202.
57. Kyo K, Parkes M, Takei Y, et al. Association of ulcerative colitis with rare VNTR alleles of the human intestinal mucin gene, MUC3. Hum Mol Genet. 1999;8:307-311.
58. Nakamori S, Ota DM, Cleary KR, et al. MUC1 mucin expression as a marker of progression and metastasis of human colorectal carcinoma. Gastroenterology. 1994;106:353-361.
59. Baldus SE, Monig SP, Hanisch FG, et al. Comparative evaluation of the prognostic value of MUC1, MUC2, sialyl-Lewis(a) and sialyl-Lewis(x) antigens in colorectal adenocarcinoma. Histopathology. 2002;40:440-449.
60. Yamamoto M, Bharti A, Li Y, et al. Interaction of the DF3/MUC1 breast carcinoma-associated antigen and beta-catenin in cell adhesion. J Biol Chem. 1997;272:12492-12494.
61. Li Y, Bharti A, Chen D, et al. Interaction of glycogen synthase kinase 3beta with the DF3/MUC1 carcinoma-associated antigen and beta-catenin. Mol Cell Biol. 1998;18:7216-7224.
62. Beatty PL, Plevy SE, Sepulveda AR, et al. Cutting edge: transgenic expression of human MUC1 in 1L-10-/- mice accelerates inflammatory bowel disease and progression to colon cancer. J Immunol. 2007;179:735-739.
63. Monti P, Leone BE, Zerbi A, et al. Tumor-derived MUC1 mucins interact with differentiating monocytes and induce IL-10highIL-12low regulatory dendritic cell. J Immunol. 2004;172:7341-7349.
64. Hiltbold EM, Vlad AM, Ciborowski P, et al. The mechanism of unresponsiveness to circulating tumor antigen MUC1 is a block in intracellular sorting and processing by dendritic cells. J Immunol. 2000;165:3730-3741.
65. Herbert LM, Grosso JF, Dorsey M Jr, et al. A unique mucin immunoenhancing peptide with antitumor properties. Cancer Res. 2004;64:8077-8084.
66. Ma T, Verkman AS. Aquaporin water channels in gastrointestinal physiology. J Physiol. 1999;517(Pt 2):317-326.
67. Koyama Y, Yamamoto T, Kondo D, et al. Molecular cloning of a new aquaporin from rat pancreas and liver. J Biol Chem. 1997;272:30329-30333.
68. Yang B, Song Y, Zhao D, et al. Phenotype analysis of aquaporin-8 null mice. Am J Physiol Cell Physiol. 2005;288:C1161-1170.
69. Hardin JA, Wallace LE, Wong JF, et al. Aquaporin expression is downregulated in a murine model of colitis and in patients with ulcerative colitis, Crohn's disease and infectious colitis. Cell Tissue Res. 2004;318:313-323.
70. Fischer H, Stenling R, Rubio C, et al. Differential expression of aquaporin 8 in human colonic epithelial cells and colorectal tumors. BMC Physiol. 2001;1:1.
71. Bertenshaw GP, Turk BE, Hubbard SJ, et al. Marked differences between metalloproteases meprin A and B in substrate and peptide bond specificity. J Biol Chem. 2001;276:13248-13255.
72. Kruse MN, Becker C, Lottaz D, et al. Human meprin alpha and beta homo-oligomers: cleavage of basement membrane proteins and sensitivity to metalloprotease inhibitors. Biochem J. 2004;378:383-389.
73. Lottaz D, Maurer CA, Hahn D, et al. Nonpolarized secretion of human meprin alpha in colorectal cancer generates an increased proteolytic potential in the stroma. Cancer Res. 1999;59:1127-1133.
74. Matters GL, Bond JS. Expression and regulation of the meprin beta gene in human cancer cells. Mol Carcinog. 1999;25:169-178.
75. Norman LP, Jiang W, Han X, et al. Targeted disruption of the meprin beta gene in mice leads to underrepresentation of knockout mice and changes in renal gene expression profiles. Mol Cell Biol. 2003;23:1221-1230.