Hepatocyte nuclear factor-1α is required for expression but dispensable for histone acetylation of the lactase-phlorizin hydrolase gene in vivo

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 290, Issue 5, 2006, Pages

  Bosse, Tjalling ^a   Van Wering, Herbert M ^b   Gielen, Marieke ^a   Dowling, Lauren N ^c   Fialkovich, John J ^c   Piaseckyj, Christina M ^c   Gonzalez, Frank J ^d   Akiyama, Taro E ^e   Montgomery, Robert K ^c,f   Grand, Richard J ^c,f   Krasinski, Stephen D ^c,f,g  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e MERCK RESEARCH LABORATORIES   (United States)

^f HARVARD MEDICAL SCHOOL   (United States)

^g TUFTS UNIVERSITY   (United States)

Author keywords

Chromatin modification; Intestinal gene expression; Liver fatty acid binding protein; Sucrase isomaltase

Indexed keywords

GLYCOSYLCERAMIDASE; HEPATOCYTE NUCLEAR FACTOR 1ALPHA; HISTONE; HISTONE ACETYLTRANSFERASE; LACTASE; MESSENGER RNA; SUCRASE ISOMALTASE;

ACETYLATION; ANIMAL CELL; ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DIFFERENTIATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE TARGETING; JEJUNUM; LIVER; MOUSE; NEWBORN; NONHUMAN; PANCREAS; PRIORITY JOURNAL; PROMOTER REGION; REGULATORY MECHANISM; WILD TYPE;

ACETYLATION; ANIMALS; GENE EXPRESSION REGULATION; GENES, REPORTER; GLYCOSYLCERAMIDASE; HEPATOCYTE NUCLEAR FACTOR 1; HISTONES; INTESTINES; JEJUNUM; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PROMOTER REGIONS (GENETICS); SUCRASE-ISOMALTASE COMPLEX; TRANSCRIPTION FACTORS;

EID: 33645893199     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00359.2005     Document Type: Article

References (56)

1. Akiyama TE, Ward JM, and Gonzalez FJ. Regulation of the liver fatty acid-binding protein gene by hepatocyte nuclear factor 1α (HNF1α). Alterations in fatty acid homeostasis in HNF1α-deficient mice. J Biol Chem 275: 27117-27122, 2000.
2. Baumhueter S, Courtois G, Morgan JG, and Crabtree GR. The role of HNF-1 in liver-specific gene expression. Am NY Acad Sci 557: 272-278, 1989.
3. Baumhueter S, Mendel DB, Conley PB, Kuo CJ, Turk C, Graves MK, Edwards CA, Courtois G, and Crabtree GR. HNF-1 shares three sequence motifs with the POU domain proteins and is identical to LF-B1 and APF. Genes Dev 4: 372-379, 1990.
4. Boudreau F, Rings EH, van Wering HM, Kim RK, Swain GP, Krasinski SD, Moffett J, Grand RJ, Suh ER, and Traber PG. Hepatocyte nuclear factor-1α, GATA-4, and caudal related homeodomain protein Cdx2 interact functionally to modulate intestinal gene transcription. Implication for the developmental regulation of the sucrase-isomaltase gene. J Biol Chem 277: 31909-31917, 2002.
5. Boudreau F, Rings EHHM, Swain GP, Sinclair AM, Suh ER, Silberg DG, Scheuermann RH, and Traber PG. A Novel Colonic Repressor Element Regulates Intestinal Gene Expression by Interacting with Cux/CDP. Mol Cell Biol 22: 5467-5478, 2002.
6. Boudreau F, Zhu Y, and Traber PG. Sucrase-isomaltase gene transcription requires the hepatocyte nuclear factor-1 (HNF-1) regulatory element and is regulated by the ratio of HNF-1α to HNF-1β. J Biol Chem 276: 32122-32128, 2001.
7. Cereghini S, Blumenfeld M, and Yaniv M. A liver-specific factor essential for albumin transcription differs between differentiated and dedifferentiated rat hepatoma cells. Genes Dev 2: 957-974, 1988.
8. Courtois G, Morgan JG, Campbell LA, Fourel G, and Crabtree GR. Interaction of a liver-specific nuclear factor with the fibrinogen and α1-antitrypsin promoters. Science 238: 688-692, 1987.
9. Divine JK, McCaul SP, and Simon TC. HNF-1α and endodermal transcription factors cooperatively activate Fabpl: MODY3 mutations abrogate cooperativity. Am J Physiol Gastrointest Liver Physiol 285: G62-G72, 2003.
10. Divine JK, Staloch LJ, Haveri H, Jacobsen CM, Wilson DB, Heikinheimo M, and Simon TC. GATA-4, GATA-5, and GATA-6 activate the rat liver fatty acid binding protein gene in concert with HNF-1α. Am J Physiol Gastrointest Liver Physiol 287: G1086-G1099, 2004.
11. Gerrish K, Cissell MA, and Stein R. The role of hepatic nuclear factor 1α and PDX-1 in transcriptional regulation of the pdx-1 gene. J Biol Chem 276: 47775-47784, 2001.
12. Hatzis P and Talianidis I. Regulatory mechanisms controlling human hepatocyte nuclear factor 4α gene expression. Mol Cell Biol 21: 7320-7330, 2001.
13. Henning SJ. Postnatal development: coordination of feeding, digestion, and metabolism. Am J Physiol Gastrointest Liver Physiol 241: G199-G214, 1981.
14. Hochman JA, Sciaky D, Whitaker TL, Hawkins JA, and Cohen MB. Hepatocyte nuclear factor-1α regulates transcription of the guanylin gene. Am J Physiol Gastrointest Liver Physiol 273: G833-G841, 1997.
15. Hu C and Perlmutter DH. Regulation of α1-antitrypsin gene expression in human intestinal epithelial cell line caco-2 by HNF-1α and HNF-4. Am J Physiol Gastrointest Liver Physiol 276: G1181-G1194, 1999.
16. Krasinski SD, Estrada G, Yeh KY, Yeh M, Traber PG, Rings EH, Buller HA, Verhave M, Montgomery RK, and Grand RJ. Transcriptional regulation of intestinal hydrolase biosynthesis during postnatal development in rats. Am J Physiol Gastrointest Liver Physiol 267: G584-G594, 1994.
17. Krasinski SD, Upchurch BH, Irons SJ, June RM, Mishra K, Grand RJ, and Verhave M. Rat lactase-phlorizin hydrolase/human growth hormone transgene is expressed on small intestinal villi in transgenic mice. Gastroenterology 113: 844-855, 1997.
18. Krasinski SD, van Wering HM, Tannemaat MR, and Grand RJ. Differential activation of intestinal gene promoters: demonstration of functional interactions between GATA-5 and HNF-1α. Am J Physiol Gastrointest Liver Physiol 281: G69-G84, 2001.
19. Kuo CJ, Conley PB, Hsieh CL, Francke U, and Crabtree GR. Molecular cloning, functional expression, and chromosomal localization of mouse hepatocyte nuclear factor 1. Proc Natl Acad Sci 87: 9838-9842, 1990.
20. Lambert M, Colnot S, Suh E, FLH, Blin C, Calliot ME, Raymondjean M, Thomasset M, Traber PG, and Perret C. cis-Acting elements and transcription factors involved in the intestinal specific expression of the rat calbindin-D9k gene: binding of the intestine-specific transcription factor Cdx-2 to the Tata box. Eur J Biochem 236: 778-788, 1996.
21. Lee YH, Sauer B, and Gonzalez FJ. Laron dwarfism and non-insulin- dependent diabetes mellitus in the Hnf-1α knockout mouse. Mol Cell Biol 18: 3059-3068, 1998.
22. Markowitz AJ, Wu GD, Birkenmeier EH, and Traber PG. The human sucrase-isomaltase gene directs complex patterns of gene expression in transgenic mice. Am J Physiol Gastrointest Liver Physiol 265: G526-G539, 1993.
23. +-glucose cotransporter gene, SGLT1, by HNF-1 and Sp1. Am J Physiol Gastrointest Liver Physiol 278: G591-G603, 2000.
24. Mitchelmore C, Troelsen JT, Sjostrom H, and Noren O. The HOXC11 homeodomain protein interacts with the lactase-phlorizin hydrolase promoter and stimulates HNF1α-dependent transcription. J Biol Chem 273: 13297-13306, 1998.
25. Mitchelmore C, Troelsen JT, Spodsberg N, Sjostrom H, and Noren O. Interaction between the homeodomain proteins Cdx2 and HNF1α mediates expression of the lactase-phlorizin hydrolase gene. Biochem J 346: 529-535, 2000.
26. Miyamoto KHK, Taketani Y, Minami H, Oka T, Nakabou Y, and Hagihira H. Diabetes and glucose transporter gene expression reat small intestine. Biochem Biophys Res Commun 181: 1110-1117, 1991.
27. Mouchel N, Henstra SA, McCarthy VA, Williams SH, Phylactides M, and Harris A. HNF1α is involved in tissue-specific regulation of CFTR gene expression. Biochem J 378: 909-918, 2004.
28. Olsen WA, Perchellet E, and Malinowski RL. Intestinal mucosa in diabetes: synthesis of total proteins and sucrase-isomaltase. Am J Physiol Gastrointest Liver Physiol 250: G788-G793, 1986.
29. Parrizas M, Maestro MA, Boj SF, Paniagua A, Casamitjana R, Gomis R, Rivera F, and Ferrer J. Hepatic nuclear factor 1-α directs nucleosomal hyperacetylation to its tissue-specific transcriptional targets. Mol Cell Biol 21: 3234-3243, 2001.
30. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucl Acids Res 29: e45, 2001.
31. Pontoglio M, Barra J, Hadchouel M, Doyen A, Kress C, Bach JP, Babinet C, and Yaniv M. Hepatocyte nuclear factor 1 inactivation results in hepatic dysfunction, phenylketonuria, and renal Fanconi syndrome. Cell 84: 575-585, 1996.
32. Pontoglio M, Faust DM, Doyen A, Yaniv M, and Weiss MC. Hepatocyte nuclear factor 1α gene inactivation impairs chromatin remodeling and demethylation of the phenylalanine hydroxylase gene. Mol Cell Biol 17: 4948-4956, 1997.
33. Pontoglio M, Prie D, Cheret C, Doyen A, Leroy C, Froguel P, Velho G, Yaniv M, and Friedlander G. HNF1α controls renal glucose reabsorption in mouse and man. EMBO Reports 1: 359-365, 2000.
34. +/glucose cotransporter 1 mRNA levels is transcriptionally regulated. J Biol Chem 273: 9510-9516, 1998.
35. Rings EH, de Boer PA, Moorman AF, van Beers EH, Dekker J, Montgomery RK, Grand RJ, and Buller HA. Lactase gene expression during early development of rat small intestine. Gastroenterology 103: 1154-1161, 1992.
36. Rings EH, Krasinski SD, van Beers EH, Moorman AF, Dekker J, Montgomery RK, Grand RJ, and Buller HA. Restriction of lactase gene expression along the proximal-to-distal axis of rat small intestine occurs during postnatal development. Gastroenterology 106: 1223-1232, 1994.
37. Sakaguchi T, Gu X, Golden HM, Suh ER, Rhoads DB, and Reinecker HC. Cloning of the human claudin-2 5′-flanking region revealed a TATA-less promoter with conserved binding sites in mouse and human for caudal-related homeodomain proteins and hepatocyte nuclear factor-1a. J Biol Chem 277: 21361-21370, 2002.
38. Schjerven H, Brandtzaeg P, and Johansen FE. Hepatocyte NF-1 and STAT6 cooperate with additional DNA-binding factors to activate transcription of the human polymeric Ig receptor gene in response to IL-4. J Immunol 170: 6048-6056, 2003.
39. Serfas MS and Tyner AL. HNF-1 α and HNF-1 beta expression in mouse intestinal crypts. Am J Physiol Gastrointest Liver Physiol 265: G506-G513, 1993.
40. Shih DQ, Bussen M, Sehayek E, Ananthanarayanan M, Shneider BL, Suchy FJ, Shefer S, Bollileni JS, Gonzalez FJ, Breslow JL, and Stoffel M. Hepatocyte nuclear factor-1α is an essential regulator of bile acid and plasma cholesterol metabolism. Nat Genet 27: 375-382, 2001.
41. Shih DQ, Screenan S, Munoz KN, Philipson L, Pontoglio M, Yaniv M, Polonsky KS, and Stoffel M. Loss of HNF-1α function in mice leads to abnormal expression of genes involved in pancreatic islet development and metabolism. Diabetes 50: 2472-2480, 2001.
42. Shivdasani RA. Molecular and transcriptional regulation of megakaryocyte differentiation. Stem Cells 19: 397-407, 2001.
43. Spodsberg N, Troelsen JT, Carlsson P, Enerback S, Sjostrom H, and Noren O. Transcriptional regulation of pig lactase-phlorizin hydrolase: involvement of HNF-1 and FREACs. Gastroenterology 116: 842-854, 1999.
44. Suh E and Traber PG. An intestine-specific homeobox gene regulates proliferation and differentiation. Mol Cell Biol 16: 619-625, 1996.
45. Tandon RK, Srivastava LM, and Pandey SC. Increased disaccharidase activity in human diabetics. Am J Clin Nutr 28: 621-625, 1975.
46. Traber PG and Silberg DG. Intestine-specific gene transcription. Ann Rev Physiol 58: 275-297, 1996.
47. Troelsen JT. Adult-type hypolactasia and regulation of lactase expression. Biochim Biophys Acta 1723: 19-32, 2005.
48. Vallet V, Bens M, Antoine B, Levrat F, Miquerol L, Kahn A, and Vandewalle A. Transcription factors and aldolase B gene expression in microdissected renal proximal tubules and derived cell lines. Exp Cell Res 216: 363-370, 1995.
49. Van Wering HM, Bosse T, Musters A, de Jong E, de Jong N, Hogen Esch CE, Boudreau F, Swain GP, Dowling LN, Montgomery RK, Grand RJ, and Krasinski SD. Complex regulation of the lactase-phlorizin hydrolase promoter by GATA-4. Am J Physiol Gastrointest Liver Physiol 287: G899-G909, 2004.
50. Van Wering HM, Huibregtse IL, van der Zwan SM, de Bie MS, Dowling LN, Boudreau F, Rings EH, Grand RJ, and Krasinski SD. Physical interaction between GATA-5 and hepatocyte nuclear factor-1α results in synergistic activation of the human lactase-phlorizin hydrolase promoter. J Biol Chem 277: 27659-27667, 2002.
51. Viollet B, Yaniv M, and Pontoglio M. Embryonic but not postnatal reexpression of hepatocyte nuclear factor 1α (HNF1α) can reactivate the silent phenylalanine hydroxylase gene in HNF1α-deficient hepatocytes. Mol Cell Biol 21: 3662-3670, 2001.
52. Wang L, Klopot A, Freund JN, Dowling LN, Krasinski SD, and Fleet JC. Control of differentiation-induced calbindin-D9k gene expression in Caco-2 cells by cdx-2 and HNF-1α. Am J Physiol Gastrointest Liver Physiol 287: G943-G953, 2004.
53. Wang Z, Fang R, Olds LC, and Sibley E. Transcriptional regulation of the lactase-phlorizin hydrolase promoter by PDX-1. Am J Physiol Gastrointest Liver Physiol 287: G555-G561, 2004.
54. Wu GD, Chen L, Forslund K, and Traber PG. Hepatocyte nuclear factor-1 α (HNF-1 α) and HNF-1 beta regulate transcription via two elements in an intestine-specific promoter. J Biol Chem 269: 17080-17085, 1994.
55. Wu GD, Wang W, and Traber PG. Isolation and characterization of the human sucrase-isomaltase gene and demonstration of intestine-specific transcriptional elements. J Biol Chem 267: 7863-7870, 1992.
56. Younoszai MK and Schedl HP. Effect of diabetes on intestinal disaccharidase activities. J Lab Clin Med 79: 579-586, 1972.