Cooperative interaction between hepatocyte nuclear factor 4α and GATA transcription factors regulates ATP-binding cassette sterol transporters ABCG5 and ABCG8

Molecular and Cellular Biology

Volumn 27, Issue 12, 2007, Pages 4248-4260

  Sumi, Koichi ^a,e   Tanaka, Toshiya ^a   Uchida, Aoi ^a   Magoori, Kenta ^a   Urashima, Yasuyo ^a   Ohashi, Riuko ^b   Ohguchi, Hiroto ^a   Okamura, Masashi ^a   Kudo, Hiromi ^a   Daigo, Kenji ^a   Maejima, Takashi ^a   Kojima, Noriaki ^a   Sakakibara, Iori ^a   Jiang, Shuying ^b   Hasegawa, Go ^b   Kim, Insook ^c   Osborne, Timothy F ^d   Naito, Makoto ^b   Gonzalez, Frank J ^c   Hamakubo, Takao ^a   Kodama, Tatsuhiko ^a   Sakai, Juro ^a   more..

^a UNIVERSITY OF TOKYO   (Japan)

^b NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^c NATIONAL CANCER INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e Nippon Bio Rad Laboratories   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABCG5 TRANSPORTER; ABCG8 TRANSPORTER; BILE ACID; HEPATOCYTE NUCLEAR FACTOR 4ALPHA; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR GATA 6; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL CULTURE; CELL NUCLEUS; CELL STRAIN HEPG2; CHOLESTEROL METABOLISM; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; CULTURE MEDIUM; DNA RESPONSIVE ELEMENT; GENE EXPRESSION; HOMEOSTASIS; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REPORTER GENE;

ADENOVIRIDAE; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ATP-BINDING CASSETTE TRANSPORTERS; BASE SEQUENCE; BINDING SITES; CARCINOMA, HEPATOCELLULAR; CELL LINE; CELL LINE, TUMOR; CONSENSUS SEQUENCE; CONSERVED SEQUENCE; GATA4 TRANSCRIPTION FACTOR; GATA6 TRANSCRIPTION FACTOR; GENE DELETION; GENES, REPORTER; HEPATOCYTE NUCLEAR FACTOR 4; HUMANS; LIPOPROTEINS; LIVER NEOPLASMS; LUCIFERASES; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 34250173805     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01894-06     Document Type: Article

References (55)

1. Arceci, R. J., A. A. King, M. C. Simon, S. H. Orkin, and D. B. Wilson. 1993. Mouse GATA-4: a retinoic acid-inducible GATA-binding transcription factor expressed in endodermally derived tissues and heart. Mol. Cell. Biol. 13:2235-2246.
2. Berge, K. E., H. Tian, G. A. Graf, L. Yu, N. V. Grishin, J. Schultz, P. Kwiterovich, B. Shan, R. Barnes, and H. H. Hobbs. 2000. Accumulation of dietary cholesterol in sitosterolemia caused by mutations in adjacent ABC transporters. Science 290:1771-1775.
3. Chiang, J. Y. 2002. Bile acid regulation of gene expression: roles of nuclear hormone receptors. Endocr. Rev. 23:443-463.
4. Duncan, S. A., A. Nagy, and W. Chan. 1997. Murine gastrulation requires HNF-4 regulated gene expression in the visceral endoderm: tetraploid rescue of Hnf-4(-/-) embryos. Development 124:279-287.
5. Francis, G. A., E. Fayard, F. Picard, and J. Auwerx. 2003. Nuclear receptors and the control of metabolism. Annu. Rev. Physiol. 65:261-311.
6. Freeman, L. A., A. Kennedy, J. Wu, S. Bark, A. T. Remaley, S. Santamarina-Fojo, and H. B. Brewer, Jr. 2004. The orphan nuclear receptor LRH-1 activates the ABCG5/ABCG8 intergenic promoter. J. Lipid Res. 45:1197-1206.
7. Glass, C. K., and M. G. Rosenfeld. 2000. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 14:121-141.
8. Goodwin, B., S. A. Jones, R. R. Price, M. A. Watson, D. D. McKee, L. B. Moore, C. Galardi, J. G. Wilson, M. C. Lewis, M. E. Roth, P. K. Maloney, T. M. Willson, and S. A. Kliewer. 2000. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol. Cell 6:517-526.
9. Gregg, R. E., W. E. Connor, D. S. Lin, and H. B. Brewer, Jr. 1986. Abnormal metabolism of shellfish sterols in a patient with sitosterolemia and xanthomatosis. J. Clin. Investig. 77:1864-1872.
10. Hayhurst, G. P., Y.-H. Lee, G. Lambert, J. M. Ward, and F. J. Gonzalez. 2001. Hepatocyte nuclear factor 4α (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol. Cell. Biol. 21:1393-1403.
11. Horton, J. D., J. L. Goldstein, and M. S. Brown. 2002. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J. Clin. Investig. 109:1125-1131.
12. Iguchi, H., Y. Ikeda, M. Okamura, T. Tanaka, Y. Urashima, H. Ohguchi, S. Takayasu, N. Kojima, S. Iwasaki, R. Ohashi, S. Jiang, G. Hasegawa, R. X. Ioka, K. Magoori, K. Sumi, T. Maejima, A. Uchida, M. Naito, T. F. Osborne, M. Yanagisawa, T. T. Yamamoto, T. Kodama, and J. Sakai. 2005. SOX6 attenuates glucose-stimulated insulin secretion by repressing PDX1 transcriptional activity and is down-regulated in hyperinsulinemic obese mice. J. Biol. Chem. 280:37669-37680.
13. Ikeda, Y., J. Yamamoto, M. Okamura, T. Fujino, S. Takahashi, K. Takeuchi, T. F. Osborne, T. T. Yamamoto, S. Ito, and J. Sakai. 2001. Transcriptional regulation of the murine acetyl-CoA synthetase 1 gene through multiple clustered binding sites for sterol regulatory element-binding proteins and a single neighboring site for Sp1. J. Biol. Chem. 276:34259-34269.
14. Jiang, S., T. Tanaka, H. Iwanari, H. Hotta, H. Yamashita, J. Kumakura, Y. Watanabe, Y. Uchiyama, H. Aburatani, T. Hamakubo, T. Kodama, and M. Naito. 2003. Expression and localization of P1 promoter-driven hepatocyte nuclear factor-4alpha (HNF4alpha) isoforms in human and rats. Nucl. Recept. 1:5.
15. Kelley, C., H. Blumberg, L. I. Zon, and T. Evans. 1993. GATA-4 is a novel transcription factor expressed in endocardium of the developing heart. Development 118:817-827.
16. Kuo, C. J., P. B. Conley, L. Chen, F. M. Sladek, J. E. Darnell, Jr., and G. R. Crabtree. 1992. A transcriptional hierarchy involved in mammalian cell-type specification. Nature 355:457-461.
17. Kuo, C. T., E. E. Morrisey, R. Anandappa, K. Sigrist, M. M. Lu, M. S. Parmacek, C. Soudais, and J. M. Leiden. 1997. GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev. 11:1048-1060.
18. Ladias, J. A., M. Hadzopoulou-Cladaras, D. Kardassis, P. Cardot, J. Cheng, V. Zannis, and C. Cladaras. 1992. Transcriptional regulation of human apolipoprotein genes ApoB, ApoCIII, and ApoAII by members of the steroid hormone receptor superfamily HNF-4, ARP-1, EAR-2, and EAR-3. J. Biol. Chem. 267:15849-15860.
19. Laverriere, A. C., C. MacNeill, C. Mueller, R. E. Poelmann, J. B. Burch, and T. Evans. 1994. GATA-4/5/6, a subfamily of three transcription factors transcribed in developing heart and gut. J. Biol. Chem. 269:23177-23184.
20. Lee, M. H., K. Lu, S. Hazard, H. Yu, S. Shulenin, H. Hidaka, H. Kojima, R. Allikmets, N. Sakuma, R. Pegoraro, A. K. Srivastava, G. Salen, M. Dean, and S. B. Patel. 2001. Identification of a gene, ABCG5, important in the regulation of dietary cholesterol absorption. Nat. Genet. 27:79-83.
21. Lee, M. H., K. Lu, and S. B. Patel. 2001. Genetic basis of sitosterolemia. Curr. Opin. Lipidol. 12:141-149.
22. Li, J., G. Ning, and S. A. Duncan. 2000. Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha. Genes Dev. 14:464-474.
23. Liu, C., S. W. Glasser, H. Wan, and J. A. Whitsett. 2002. GATA-6 and thyroid transcription factor-1 directly interact and regulate surfactant protein-C gene expression. J. Biol. Chem. 277:4519-4525.
24. Lu, K., M. H. Lee, S. Hazard, A. Brooks-Wilson, H. Hidaka, H. Kojima, L. Ose, A. F. Stalenhoef, T. Mietinnen, I. Bjorkhem, E. Bruckert, A. Pandya, H. B. Brewer, Jr., G. Salen, M. Dean, A. Srivastava, and S. B. Patel. 2001. Two genes that map to the STSL locus cause sitosterolemia: genomic structure and spectrum of mutations involving sterolin-1 and sterolin-2, encoded by ABCG5 and ABCG8, respectively. Am. J. Hum. Genet. 69:278-290.
25. Lu, K., M. H. Lee, and S. B. Patel. 2001. Dietary cholesterol absorption; more than just bile. Trends Endocrinol. Metab. 12:314-320.
26. Lu, T. T., M. Makishima, J. J. Repa, K. Schoonjans, T. A. Kerr, J. Auwerx, and D. J. Mangelsdorf. 2000. Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol. Cell 6:507-515.
27. Lu, T. T., J. J. Repa, and D. J. Mangelsdorf. 2001. Orphan nuclear receptors as eLiXiRs and FiXeRs of sterol metabolism. J. Biol. Chem. 276:37735-37738.
28. Molkentin, J. D., Q. Lin, S. A. Duncan, and E. N. Olson. 1997. Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev. 11:1061-1072.
29. Morrisey, E. E., H. S. Ip, M. M. Lu, and M. S. Parmacek. 1996. GATA-6: a zinc finger transcription factor that is expressed in multiple cell lineages derived from lateral mesoderm. Dev. Biol. 177:309-322.
30. Morrisey, E. E., Z. Tang, K. Sigrist, M. M. Lu, F. Jiang, H. S. Ip, and M. S. Parmacek. 1998. GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev. 12:3579-3590.
31. Odom, D. T., N. Zizlsperger, D. B. Gordon, G. W. Bell, N. J. Rinaldi, H. L. Murray, T. L. Volkert, J. Schreiber, P. A. Rolfe, D. K. Gifford, E. Fraenkel, G. I. Bell, and R. A. Young. 2004. Control of pancreas and liver gene expression by HNF transcription factors. Science 303:1378-1381.
32. Orkin, S. H., R. A. Shivdasani, Y. Fujiwara, and M. A. McDevitt. 1998. Transcription factor GATA-1 in megakaryocyte development. Stem Cells 16(Suppl. 2):79-83.
33. Remaley, A. T., S. Bark, A. D. Walts, L. Freeman, S. Shulenin, T. Annilo, E. Elgin, H. E. Rhodes, C. Joyce, and M. Dean. 2002. Comparative genome analysis of potential regulatory elements in the ABCG5-ABCG8 gene cluster. Biochem. Biophys. Res. Commun. 295:276-282.
34. Repa, J. J., K. E. Berge, C. Pomajzl, J. A. Richardson, H. Hobbs, and D. J. Mangelsdorf. 2002. Regulation of ATP-binding cassette sterol transporters ABCG5 and ABCG8 by the liver X receptors alpha and beta. J. Biol. Chem. 277:18793-18800.
35. Ruse, M. D., Jr., M. L. Privalsky, and F. M. Sladek. 2002. Competitive cofactor recruitment by orphan receptor hepatocyte nuclear factor 4α1: modulation by the F domain. Mol. Cell. Biol. 22:1626-1638.
36. Sakai, J., E. A. Duncan, R. B. Rawson, X. Hua, M. S. Brown, and J. L. Goldstein. 1996. Sterol-regulated release of SREBP-2 from cell membranes requires two sequential cleavages, one within a transmembrane segment. Cell 85:1037-1046.
37. Sakai, J., A. Nohturfft, J. L. Goldstein, and M. S. Brown. 1998. Cleavage of sterol regulatory element-binding proteins (SREBPs) at site-1 requires interaction with SREBP cleavage-activating protein. Evidence from in vivo competition studies. J. Biol. Chem. 273:5785-5793.
38. Sakai, J., and R. B. Rawson. 2001. The sterol regulatory element-binding protein pathway: control of lipid homeostasis through regulated intracellular transport. Curr. Opin. Lipidol. 12:261-266.
39. Sakai, J., R. B. Rawson, P. J. Espenshade, D. Cheng, A. C. Seegmiller, J. L. Goldstein, and M. S. Brown. 1998. Molecular identification of the sterol-regulated luminal protease that cleaves SREBPs and controls lipid composition of animal cells. Mol. Cell 2:505-514.
40. Salen, G., S. Shefer, L. Nguyen, G. C. Ness, G. S. Tint, and V. Shore. Sitosterolemia. 1992. J. Lipid Res. 33:945-955.
41. Shulenin, S., L. M. Schriml, A. T. Remaley, S. Fojo, B. Brewer, R. Allikmets, and M. Dean. 2001. An ATP-binding cassette gene (ABCG5) from the ABCG (White) gene subfamily maps to human chromosome 2p21 in the region of the Sitosterolemia locus. Cytogenet. Cell Genet. 92:204-208.
42. Sladek, F. M., M. D. Ruse, Jr., L. Nepomuceno, S. M. Huang, and M. R. Stallcup. 1999. Modulation of transcriptional activation and coactivator interaction by a splicing variation in the F domain of nuclear receptor hepatocyte nuclear factor 4α1. Mol. Cell. Biol. 19:6509-6522.
43. Sladek, F. M., W. M. Zhong, E. Lai, and J. E. Darnell, Jr. 1990. Liver-enriched transcription factor HNF-4 is a novel member of the steroid hormone receptor superfamily. Genes Dev. 4:2353-2365.
44. Sladek, R., and V. Giguere. 2000. Orphan nuclear receptors: an emerging family of metabolic regulators. Adv. Pharmacol. 47:23-87.
45. Soudais, C., M. Bielinska, M. Heikinheimo, C. A. MacArthur, N. Narita, J. E. Saffitz, M. C. Simon, J. M. Leiden, and D. B. Wilson. 1995. Targeted mutagenesis of the transcription factor GATA-4 gene in mouse embryonic stem cells disrupts visceral endoderm differentiation in vitro. Development 121:3877-3888.
46. Suzuki, E., T. Evans, J. Lowry, L. Truong, D. W. Bell, J. R. Testa, and K. Walsh. 1996. The human GATA-6 gene: structure, chromosomal location, and regulation of expression by tissue-specific and mitogen-responsive signals. Genomics 38:283-290.
47. Tanaka, T., S. Jiang, H. Hotta, K. Takano, H. Iwanari, K. Sumi, K. Daigo, R. Ohashi, M. Sugai, C. Ikegame, H. Umezu, Y. Hirayama, Y. Midorikawa, Y. Hippo, A. Watanabe, Y. Uchiyama, G. Hasegawa, P. Reid, H. Aburatani, T. Hamakubo, J. Sakai, M. Naito, and T. Kodama. 2006. Dysregulated expression of P1 and P2 promoter-driven hepatocyte nuclear factor-4alpha in the pathogenesis of human cancer. J. Pathol. 208:662-672.
48. Tanaka, T., J. Yamamoto, S. Iwasaki, H. Asaba, H. Hamura, Y. Ikeda, M. Watanabe, K. Magoori, R. X. Ioka, K. Tachibana, Y. Watanabe, Y. Uchiyama, K. Sumi, H. Iguchi, S. Ito, T. Doi, T. Hamakubo, M. Naito, J. Auwerx, M. Yanagisawa, T. Kodama, and J. Sakai. 2003. Activation of peroxisome proliferator-activated receptor delta induces fatty acid beta-oxidation in skeletal muscle and attenuates metabolic syndrome. Proc. Natl. Acad. Sci. USA 100:15924-15929.
49. Tauscher, A., and R. Kuver. 2003. ABCG5 and ABCG8 are expressed in gallbladder epithelial cells. Biochem. Biophys. Res. Commun. 307:1021-1028.
50. van Wering, H. M., I. L. Huibregtse, S. M. van der Zwan, M. S. de Bie, L. N. Dowling, F. Boudreau, E. H. H. M. Rings, R. J. Grand, and S. D. Krasinski. 2002. Physical interaction between GATA-5 and hepatocyte nuclear factor-1alpha results in synergistic activation of the human lactase-phlorizin hydrolase promoter. J. Biol. Chem. 277:27659-27667.
51. Yamagata, K., H. Furuta, N. Oda, P. J. Kaisaki, S. Menzel, N. J. Cox, S. S. Fajans, S. Signorini, M. Stoffel, and G. I. Bell. 1996. Mutations in the hepatocyte nuclear factor-4α gene in maturity-onset diabetes of the young (MODY1). Nature 384:458-460.
52. Yamamoto, J., Y. Ikeda, H. Iguchi, T. Fujino, T. Tanaka, H. Asaba, S. Iwasaki, R. X. Ioka, I. W. Kaneko, K. Magoori, S. Takahashi, T. Mori, H. Sakaue, T. Kodama, M. Yanagisawa, T. T. Yamamoto, S. Ito, and J. Sakai. 2004. A Kruppel-like factor KLF15 contributes fasting-induced transcriptional activation of mitochondrial acetyl-CoA synthetase gene AceCS2. J. Biol. Chem. 279:16954-16962.
53. Yu, L., R. E. Hammer, J. Li-Hawkins, K. Von Bergmann, D. Lutjohann, J. C. Cohen, and H. H. Hobbs. 2002. Disruption of Abcg5 and Abcg8 in mice reveals their crucial role in biliary cholesterol secretion. Proc. Natl. Acad. Sci. USA 99:16237-16242.
54. Yu, L., J. Li-Hawkins, R. E. Hammer, K. E. Berge, J. D. Horton, J. C. Cohen, and H. H. Hobbs. 2002. Overexpression of ABCG5 and ABCG8 promotes biliary cholesterol secretion and reduces fractional absorption of dietary cholesterol. J. Clin. Investig. 110:671-680.
55. Zhang, M., and J. Y. Chiang. 2001. Transcriptional regulation of the human sterol I2alpha-hydroxylase gene (CYP8B1): roles of hepatocyte nuclear factor 4alpha in mediating bile acid repression. J. Biol. Chem. 276:41690-41699.