Hepatocyte nuclear factor-4 mediates apolipoprotein A-IV transcriptional regulation by fatty acid in newborn swine enterocytes

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 293, Issue 2, 2007, Pages

  Leng, Shuangying ^a   Lu, Song ^a   Yao, Ying ^a   Kan, Zhisheng ^a   Morris, Gabriel S ^a   Stair, Brad R ^a   Cherny, Mathew A ^a   Black, Dennis D ^a,b  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^b LE BONHEUR CHILDREN'S MEDICAL CENTER   (United States)

Author keywords

Apo B; IPEC 1 cells; Lipid absorption; Microsomal triglyceride transfer protein; Neonate; Oleic acid

Indexed keywords

APOLIPOPROTEIN A4; APOLIPOPROTEIN C3; DOXYCYCLINE; FATTY ACID; HEPATOCYTE NUCLEAR FACTOR 4; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; MESSENGER RNA; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; OLEIC ACID;

ANIMAL CELL; ARTICLE; ENZYME ACTIVITY; FAT INTAKE; FATTY ACID METABOLISM; GENETIC TRANSCRIPTION; INTESTINE CELL; LIPID ABSORPTION; LIPID METABOLISM; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PIGLET; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REPORTER GENE; TRANSACTIVATION; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, NEWBORN; APOLIPOPROTEINS A; CARRIER PROTEINS; CELL LINE; CHYLOMICRONS; DIETARY FATS; DNA, INTERGENIC; ENTEROCYTES; FEMALE; GENES, REPORTER; HEPATOCYTE NUCLEAR FACTOR 4; JEJUNUM; LUCIFERASES; MOLECULAR SEQUENCE DATA; OLEIC ACID; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUS SCROFA; TRANSCRIPTION, GENETIC; TRANSFECTION; UP-REGULATION;

EID: 34547900621     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00072.2007     Document Type: Article

References (50)

1. Apfelbaum TF, Davidson NO, Glickman RM. Apolipoprotein A-IV synthesis in the rat small intestine: regulation by dietary triglyceride. Am J Physiol Gastrointest Liver Physiol 252: G662-G666, 1987.
2. Archer A, Sauvaget D, Chauffeton V, Bouchet PE, Chambaz J, Pincon-Raymond M, Cardot P, Ribeiro A, Lacasa M. Intestinal apolipoprotein A-IV gene transcription is controlled by two hormone-responsive elements: a role for hepatic nuclear factor-4 isoforms. Mol Endocrinol 19: 2320-2334, 2005.
3. Black DD. Regulation of intestinal apolipoprotein gene expression. In: Intestinal Lipid Metabolism, edited by Mansbach CM, Tso P, and Kuksis A. New York: Kluwer Academic/Plenum, 2001, p. 263-284.
4. Black DD, Rohwer-Nutter PL. Intestinal apolipoprotein synthesis in the newborn piglet. Pediatr Res 29: 32-38, 1991.
5. Black DD, Rohwer-Nutter PL, Davidson NO. Intestinal apo A-IV gene expression in the piglet. J Lipid Res 31: 497-505, 1990.
6. Black DD, Wang H, Hunter F, Zhan R. Intestinal expression of apolipoprotein A-IV and C-III is coordinately regulated by dietary lipid in newborn swine. Biochem Biophys Res Commun 221: 619-624, 1996.
7. Bogan AA, Dallas-Yang Q, Ruse MD Jr, Maeda Y, Jiang G, Nepomuceno L, Scanlan TS, Cohen FE, Sladek FM. Analysis of protein dimerization and ligand binding of orphan receptor HNF-4alpha. J Mol Biol 302: 831- 851, 2000.
8. Carrier JC, Deblois G, Champigny C, Levy E, Giguere V. Estrogen-related receptor alpha (ERRalpha) is a transcriptional regulator of apolipoprotein A-IV and controls lipid handling in the intestine. J Biol Chem 279: 52052-52058, 2004.
9. Carriere V, Vidal R, Lazou K, Lacasa M, Delers F, Ribeiro A, Rousset M, Chambaz J, Lacorte JM. HNF-4-dependent induction of apolipoprotein A-IV gene transcription by an apical supply of lipid micelles in intestinal cells. J Biol Chem 280: 5406-5413, 2005.
10. Dhe-Paganon S, Duda K, Iwamoto M, Chi YI, Shoelson SE. Crystal structure of the HNF-4 alpha ligand binding domain in complex with endogenous fatty acid ligand. J Biol Chem 277: 37973-37976, 2002.
11. Duverger N, Tremp G, Gaillaud JM, Emmanuel F, Castro G, Fruchart JC, Steinmetz A, Denefle P. Protection against atherogenesis in mice mediated by human apolipoprotein A-IV. Science 273: 966-968, 1996.
12. Dvorin E, Gorder NL, Benson DM, Gotto AM. Apolipoprotein A-IV: a determinate for binding and uptake of high-density lipoproteins by rat hepatocytes. J Biol Chem 261: 15714-15718, 1986.
13. Eeckhoute J, Moerman E, Bouckenooghe T, Lukoviak B, Pattou F, Formstecher P, Kerr-Conte J, Vandewalle B, Laine B. Hepatocyte nuclear factor-4 alpha isoforms originated from the P1 promoter are expressed in human pancreatic beta-cells and exhibit stronger transcriptional potentials than P2 promoter-driven isoforms. Endocrinology 144: 1686-1694, 2003.
14. Fujimoto K, Cardelli JA, Tso P. Increased apolipoprotein A-IV in rat mesenteric lymph after lipid meal acts as a physiological signal for satiation. Am J Physiol Gastrointest Liver Physiol 262: G1002-G1006, 1992.
15. Gonzalez-Vallina R, Wang H, Zhan R, Berschneider HM, Lee RM, Davidson NO, Black DD. Lipoprotein and apolipoprotein secretion by a newborn piglet intestinal cell line (IPEC-1). Am J Physiol Gastrointest Liver Physiol 271: G249-G259, 1996.
16. Hanniman EA, Lambert G, Inoue Y, Gonzalez FJ, Sinal CJ. Apolipoprotein A-IV is regulated by nutritional and metabolic stress: involvement of glucocorticoids, HNF-4 alpha, and PGC-1 alpha. J Lipid Res 47: 2503-2514, 2006.
17. Hayhurst GP, Lee YH, Lambert G, Ward JM, Gonzalez FJ. Hepatocyte nuclear factor-4alpha (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol Cell Biol 21: 1393-1403, 2001.
18. Hertz R, Magenheim J, Berman I, Bar-Tana J. Fatty acyl-CoA thioesters are ligands of hepatic nuclear factor-4 alpha. Nature 392: 512-516, 1998.
19. Hertz R, Sheena V, Kalderon B, Berman I, Bar-Tana J. Suppression of hepatocyte nuclear factor-4alpha by acyl-CoA thioesters of hypolipidemic peroxisome proliferators. Biochem Pharmacol 61: 1057-1062, 2001.
20. Hsu KT. Fatty acid transfer from liver and intestinal fatty acid-binding proteins to membranes occurs by different mechanisms. J Biol Chem 271: 13317-13323, 1996.
21. Jump DB. Fatty acid regulation of gene transcription. Crit Rev Clin Lab Sci 41: 41-78, 2004.
22. Kalogeris TJ, Rodriguez MD, Tso P. Control of synthesis and secretion of intestinal apolipoprotein A-IV by lipid. J Nutr 127: 537S-543S, 1997.
23. Karathanasis SK. Apolipoprotein multigene family: tandem organization of human apolipoprotein AI, CIII, and AIV genes. Proc Natl Acad Sci USA 82: 6374-6378, 1985.
24. Ktistaki E, Ktistakis NT, Papadogeorgaki E, Talianidis I. Recruitment of hepatocyte nuclear factor-4 into specific intranuclear compartments depends on tyrosine phosphorylation that affects its DNA-binding and transactivation potential. Proc Natl Acad Sci USA 92: 9876-9880, 1995.
25. Ktistaki E, Lacorte JM, Katrakili N, Zannis VI, Talianidis I. Transcriptional regulation of the apolipoprotein A-IV gene involves synergism between a proximal orphan receptor response element and a distant enhancer located in the upstream promoter region of the apolipoprotein A-IV gene. Nucleic Acids Res 22: 4689-4696, 1994.
26. Le Beyec J, Chauffeton V, Kan HY, Janvier PL, Cywiner-Golenzer C, Chatelet FP, Kalopissis AD, Zannis V, Chambaz J, Pincon-Raymond M, Cardot P. The -700/-310 fragment of the apolipoprotein A-IV gene combined with the -890/-500 apolipoprotein C-III enhancer is sufficient to direct a pattern of gene expression similar to that for the endogenous apolipoprotein A-IV gene. J Biol Chem 274: 4954-4961, 1999.
27. Lu S, Huffman M, Yao Y, Mansbach CM, Cheng X, Black DD. Regulation of microsomal triglyceride transfer protein expression in developing swine. J Lipid Res 43: 1303-1311, 2002.
28. Lu S, Yao Y, Cheng X, Mitchell S, Leng S, Meng S, Gallagher JW, Shelness GS, Morris GS, Mahan J, Frase S, Mansbach CM, Weinberg RB, Black DD. Overexpression of apolipoprotein A-IV enhances lipid secretion in IPEC-1 cells by increasing chylomicron size. J Biol Chem 281: 3473-3483, 2006.
29. Lu S, Yao Y, Meng S, Cheng X, Black DD. Overexpression of apolipoprotein A-IV enhances lipid transport in newborn swine intestinal epithelial cells. J Biol Chem 277: 31929-31937, 2002.
30. Lu S, Yao Y, Wang H, Meng S, Cheng X, Black DD. Regulation of apo A-IV transcription by lipid in newborn swine is associated with a promoter DNA-binding protein. Am J Physiol Gastrointest Liver Physiol 284: G248-G254, 2003.
31. Magenheim J, Hertz R, Berman I, Nousbeck J, Bar-Tana J. Negative autoregulation of HNF-4alpha gene expression by HNF-4alpha1. Biochem J 388: 325-332, 2005.
32. Peignon G, Thenet S, Schreider C, Fouquet S, Ribeiro A, Dussaulx E, Chambaz J, Cardot P, Pincon-Raymond M, Le Beyec J. E-cadherin-dependent transcriptional control of apolipoprotein A-IV gene expression in intestinal epithelial cells: a role for the hepatic nuclear factor-4. J Biol Chem 281: 3560-3568, 2006.
33. Qin X, Swertfeger DK, Zheng S, Hui DY, Tso P. Apolipoprotein A-IV: A potent endogenous inhibitor of lipid oxidation. Am J Physiol Heart Circ Physiol 274: H1836-H1840, 1998.
34. Rhee J, Ge H, Yang W, Fan M, Handschin C, Cooper M, Lin J, Li C, Spiegelman BM. Partnership of PGC-1alpha and HNF-4alpha in the regulation of lipoprotein metabolism. J Biol Chem 281: 14683-14690, 2006.
35. Rhee J, Inoue Y, Yoon JC, Puigserver P, Fan M, Gonzalez FJ, Spiegelman BM. Regulation of hepatic fasting response by PPARgamma coactivator-1alpha (PGC-1): requirement for hepatocyte nuclear factor-4alpha in gluconeogenesis. Proc Natl Acad Sci USA 100: 4012-4017, 2003.
36. Rowley CW, Staloch LJ, Divine JK, McCaul SP, Simon TC. Mechanisms of mutual functional interactions between HNF-4alpha and HNF-1alpha revealed by mutations that cause maturity onset diabetes of the young. Am J Physiol Gastrointest Liver Physiol 290: G466-G475, 2006.
37. Sauvaget D, Chauffeton V, Citadelle D, Chatelet FP, Cywiner-Golenzer C, Chambaz J, Pincon-Raymond M, Cardot P, Le Beyec J, Ribeiro A. Restriction of apolipoprotein A-IV gene expression to the intestine villus depends on a hormone-responsive element and parallels differential expression of the hepatic nuclear factor-4alpha and gamma isoforms. J Biol Chem 277: 34540 -34548, 2002.
38. Seda O, Sedova L. New apolipoprotein A-V: comparative genomics meets metabolism. Physiol Res 52: 141-146, 2003.
39. Sheena V, Hertz R, Nousbeck J, Berman I, Magenheim J, Bar-Tana J. Transcriptional regulation of human microsomal triglyceride transfer protein by hepatocyte nuclear factor-4alpha. J Lipid Res 46: 328-341, 2005.
40. Shelness GS, Ledford AS. Evolution and mechanism of apolipoprotein B-containing lipoprotein assembly. Curr Opin Lipidol 16: 325-332, 2005.
41. Shimamoto Y, Ishida J, Yamagata K, Saito T, Kato H, Matsuoka T, Hirota K, Daitoku H, Nangaku M, Yamagata K, Fujii H, Takeda J, Fukamizu A. Inhibitory effect of the small heterodimer partner on hepatocyte nuclear factor-4 mediates bile acid-induced repression of the human angiotensinogen gene. J Biol Chem 279: 7770-7776, 2004.
42. Sladek FM, Seidel SD. Hepatocyte nuclear factor-4 alpha. In: Nuclear Receptors and Genetic Disease, edited by Burris TB and McCabe ERB. San Diego, CA: Academic, 2001, p. 309-361.
43. Stegmann A, Hansen M, Wang Y, Larsen JB, Lund LR, Ritie L, Nicholson JK, Quistorff B, Simon-Assmann P, Troelsen JT, Olsen J. Metabolome, transcriptome, and bioinformatic cis-element analyses point to HNF-4 as a central regulator of gene expression during enterocyte differentiation. Physiol Genomics 27: 141-155, 2006.
44. Thomas H, Jaschkowitz K, Bulman M, Frayling TM, Mitchell SM, Roosen S, Lingott-Frieg A, Tack CJ, Ellard S, Ryffel GU, Hattersley AT. A distant upstream promoter of the HNF-4alpha gene connects the transcription factors involved in maturity-onset diabetes of the young. Hum Mol Genet 10: 2089-2097, 2001.
45. Vowinkel T, Mori M, Krieglstein CF, Russell J, Saijo F, Bharwani S, Turnage RH, Davidson WS, Tso P, Granger DN, Kalogeris TJ. Apolipoprotein A-IV inhibits experimental colitis. J Clin Invest 114: 260-269, 2004.
46. Wisely G, Miller A, Davis R, Thornquest A, Johnson R, Spitzer T, Sefler A, Shearer B, Moore J, Willson T, Williams S. Hepatocyte nuclear factor-4 is a transcription factor that constitutively binds fatty acids. Structure 10: 1225-1234, 2002.
47. Yamamoto T, Shimano H, Nakagawa Y, Ide T, Yahagi N, Matsuzaka T, Nakakuki M, Takahashi A, Suzuki H, Sone H, Toyoshima H, Sato R, Yamada N. SREBP-1 interacts with hepatocyte nuclear factor-4 alpha and interferes with PGC-1 recruitment to suppress hepatic gluconeogenic genes. J Biol Chem 279: 12027-12035, 2004.
48. Yoon JC, Puigserver P, Chen G, Donovan J, Wu Z, Rhee J, Adelmant G, Stafford J, Kahn CR, Granner DK, Newgard CB, Spiegelman BM. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413: 131-138, 2001.
49. Zannis VI, Kan HY, Kritis A, Zanni E, Kardassis D. Transcriptional regulation of the human apolipoprotein genes. Front Biosci 6: 456-501, 2001.
50. Zhong W, Mirkovitch J, Darnell JE Jr. Tissue-specific regulation of mouse hepatocyte nuclear factor-4 expression. Mol Cell Biol 14: 7276-7284, 1994.