The Foxa family of transcription factors in development and metabolism

Cellular and Molecular Life Sciences

Volumn 63, Issue 19-20, 2006, Pages 2317-2328

  Friedman, J R ^a   Kaestner, K H ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Development; Diabetes; Metabolism; Organogenesis; Transcription factors

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 3ALPHA; HEPATOCYTE NUCLEAR FACTOR 3BETA; HEPATOCYTE NUCLEAR FACTOR 3GAMMA; HORMONE RECEPTOR; TRANSCRIPTION FACTOR;

ADIPOSE TISSUE; DEVELOPMENTAL BIOLOGY; EMBRYO DEVELOPMENT; ENDODERM; GASTRULATION; GENE TARGETING; GENETIC ANALYSIS; HOMEOSTASIS; KIDNEY FUNCTION; LIVER DEVELOPMENT; LUNG DEVELOPMENT; MAMMAL; METABOLIC RATE; MORPHOGENESIS; NEURAL TUBE; NONHUMAN; NOTOCHORD; ORGANOGENESIS; PERINATAL PERIOD; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW;

ANIMALS; EMBRYONIC DEVELOPMENT; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GLUCOSE; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HEPATOCYTE NUCLEAR FACTOR 3-BETA; HEPATOCYTE NUCLEAR FACTOR 3-GAMMA; MICE; MULTIGENE FAMILY; ORGANOGENESIS; PROTEIN STRUCTURE, TERTIARY;

MAMMALIA;

EID: 33750438123     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-006-6095-6     Document Type: Review

References (134)

1. Weigel, D., Jurgens, G., Kuttner, F., Seifert, E. and Jackle, H. (1989) The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57, 645-658.
2. Carlsson, P. and Mahlapuu, M. (2002) Forkhead transcription factors: key players in development and metabolism. Dev. Biol. 250, 1-23.
3. Kaestner, K. H., Knochel, W. and Martinez, D. E. (2000) Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14, 142-146.
4. Herbst, R. S., Nielsch, U., Sladek, F., Lai, E., Babiss, L. E. and Darnell, J. E. Jr (1991) Differential regulation of hepatocyte-enriched transcription factors explains changes in albumin and transthyretin gene expression among hepatoma cells. New Biol. 3, 289-296.
5. Lai, E., Prezioso, V. R., Smith, E., Litvin, O., Costa, R. H. and Darnell, J. E. Jr (1990) HNF-3A, a hepatocyte-enriched transcription factor of novel structure is regulated transcriptionally. Genes Dev. 4, 1427-1436.
6. Clark, K. L., Halay, E. D., Lai, E. and Burley, S. K. (1993) Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature 364, 412-420.
7. Cirillo, L. A., Lin, F. R., Cuesta, I., Friedman, D., Jarnik, M. and Zaret, K. S. (2002) Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol. Cell 9, 279-289.
8. Holmqvist, P. H., Belikov, S., Zaret, K. S. and Wrange, O. (2005) FoxA1 binding to the MMTV LTR modulates chromatin structure and transcription. Exp. Cell Res. 304, 593-603.
9. Qian, X. and Costa, R. H. (1995) Analysis of hepatocyte nuclear factor-3 beta protein domains required for transcriptional activation and nuclear targeting. Nucleic Acids Res. 23, 1184-1191.
10. Pani, L., Overdier, D. G., Porcella, A., Qian, X., Lai, E. and Costa, R. H. (1992) Hepatocyte nuclear factor 3 beta contains two transcriptional activation domains, one of which is novel and conserved with the Drosophila fork head protein. Mol. Cell Biol. 12, 3723-3732.
11. Lai, E., Prezioso, V. R., Tao, W. F., Chen, W. S. and Darnell, J. E. Jr. (1991) Hepatocyte nuclear factor 3 alpha belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Dev. 5, 416-427.
12. Kaestner, K. H., Lee, K. H., Schlondorff, J., Hiemisch, H., Monaghan, A. P. and Schutz, G. (1993) Six members of the mouse forkhead gene family are developmentally regulated. Proc. Natl. Acad. Sci. USA 90, 7628-7631.
13. Monaghan, A. P., Kaestner, K. H., Grau, E. and Schutz, G. (1993) Postimplantation expression patterns indicate a role for the mouse forkhead/HNF-3 alpha, beta and gamma genes in determination of the definitive endoderm, chordamesoderm and neuroectoderm. Development 119, 567-578.
14. Sasaki, H. and Hogan, B. L. (1993) Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118, 47-59.
15. Kaestner, K. H., Hiemisch, H., Luckow, B. and Schutz, G. (1994) The HNF-3 gene family of transcription factors in mice: gene structure, cDNA sequence, and mRNA distribution. Genomics 20, 377-385.
16. Sasaki, H. and Hogan, B. L. (1994) HNF-3 beta as a regulator of floor plate development. Cell 76, 103-115.
17. Clevidence, D. E., Overdier, D. G., Tao, W., Qian, X., Pani, L., Lai, E. and Costa, R. H. (1993) Identification of nine tissue-specific transcription factors of the hepatocyte nuclear factor 3/forkhead DNA-binding-domain family. Proc. Natl. Acad. Sci. USA 90, 3948-3952.
18. Sasaki, H. and Hogan, B. L. (1996) Enhancer analysis of the mouse HNF-3 beta gene: regulatory elements for node/notochord and floor plate are independent and consist of multiple sub-elements. Genes Cells 1, 59-72.
19. Yasui, K., Sasaki, H., Arakaki, R. and Uemura, M. (1997) Distribution pattern of HNF-3beta proteins in developing embryos of two mammalian species, the house shrew and the mouse. Dev. Growth Differ. 39, 667-676.
20. Mirosevich, J., Gao, N. and Matusik, R. J. (2005) Expression of Foxa transcription factors in the developing and adult murine prostate. Prostate 62, 339-352.
21. Besnard, V., Wert, S. E., Hull, W. M. and Whitsett, J. A. (2004) Immunohistochemical localization of Foxa1 and Foxa2 in mouse embryos and adult tissues. Gene Expr. Patterns 5, 193-208.
22. Ang, S. L., Wierda, A., Wong, D., Stevens, K. A., Cascio, S., Rossant, J. and Zaret, K. S. (1993) The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119, 1301-1315.
23. Besnard, V., Wert, S. E., Kaestner, K. H. and Whitsett, J. A. (2005) Stage-specific regulation of respiratory epithelial cell differentiation by Foxa1. Am. J. Physiol. Lung Cell Mol. Physiol. 289, L750-759.
24. Peterson, R. S., Clevidence, D. E., Ye, H. and Costa, R. H. (1997) Hepatocyte nuclear factor-3 alpha promoter regulation involves recognition by cell-specific factors, thyroid transcription factor-1, and autoactivation. Cell Growth Differ. 8, 69-82.
25. Weinstein, D. C., Ruiz i Altaba, A., Chen, W. S., Hoodless, P., Prezioso, V. R., Jessell, T. M. and Darnell, J. E. Jr (1994) The winged-helix transcription factor HNF-3 beta is required for notochord development in the mouse embryo. Cell 78, 575-588.
26. Epstein, D. J., McMahon, A. P. and Joyner, A. L. (1999) Regionalization of Sonic hedgehog transcription along the anteroposterior axis of the mouse central nervous system is regulated by Hnf3-dependent and -independent mechanisms. Development 126, 281-292.
27. Filosa, S., Rivera-Perez, J. A., Gomez, A. P., Gansmuller, A., Sasaki, H., Behringer, R. R. and Ang, S. L. (1997) Goosecoid and HNF-3beta genetically interact to regulate neural tube patterning during mouse embryogenesis. Development 124, 2843-2854.
28. Shen, W., Scearce, L. M., Brestelli, J. E., Sund, N. J. and Kaestner, K. H. (2001) Foxa3 (hepatocyte nuclear factor 3gamma) is required for the regulation of hepatic GLUT2 expression and the maintenance of glucose homeostasis during a prolonged fast. J. Biol. Chem. 276, 42812-42817.
29. Kaestner, K. H., Katz, J., Liu, Y., Drucker, D. J. and Schutz, G. (1999) Inactivation of the winged helix transcription factor HNF3alpha affects glucose homeostasis and islet glucagon gene expression in vivo. Genes Dev. 13, 495-504.
30. Lee, C. S., Friedman, J. R., Fulmer, J. T. and Kaestner, K. H. (2005) The initiation of liver development is dependent on Foxa transcription factors. Nature 435, 944-947.
31. Sund, N. J., Ang, S. L., Sackett, S. D., Shen, W., Daigle, N., Magnuson, M. A. and Kaestner, K. H. (2000) Hepatocyte nuclear factor 3beta (Foxa2) is dispensable for maintaining the differentiated state of the adult hepatocyte. Mol. Cell Biol. 20, 5175-5183.
32. Ashizawa, S., Brunicardi, F. C. and Wang, X. P. (2004) PDX-1 and the pancreas. Pancreas 28, 109-120.
33. Lee, C. S., Sund, N. J., Behr, R., Herrera, P. L. and Kaestner, K. H. (2005) Foxa2 is required for the differentiation of pancreatic alpha-cells. Dev. Biol. 278, 484-495.
34. Wan, H., Dingle, S., Xu, Y., Besnard, V., Kaestner, K. H., Ang, S. L., Wert, S., Stahlman, M. T. and Whitsett, J. A. (2005) Compensatory roles of Foxa1 and Foxa2 during lung morphogenesis. J. Biol. Chem. 280, 13809-13816.
35. Shih, D. Q., Navas, M. A., Kuwajima, S., Duncan, S. A. and Stoffel, M. (1999) Impaired glucose homeostasis and neonatal mortality in hepatocyte nuclear factor 3alpha-deficient mice. Proc. Natl. Acad. Sci. USA 96, 10152-10157.
36. Wan, H., Kaestner, K. H., Ang, S. L., Ikegami, M., Finkelman, F. D., Stahlman, M. T., Fulkerson, P. C., Rothenberg, M. E. and Whitsett, J. A. (2004) Foxa2 regulates alveolarization and goblet cell hyperplasia. Development 131, 953-964.
37. Gao, N., Zhang, J., Rao, M. A., Case, T. C., Mirosevich, J., Wang, Y., Jin, R., Gupta, A., Rennie, P. S. and Matusik, R. J. (2003) The role of hepatocyte nuclear factor-3 alpha (Forkhead Box A1) and androgen receptor in transcriptional regulation of prostatic genes. Mol. Endocrinol. 17, 1484-1507.
38. Gao, N., Ishii, K., Mirosevich, J., Kuwajima, S., Oppenheimer, S. R., Roberts, R. L., Jiang, M., Yu, X., Shappell, S. B., Caprioli, R. M., Stoffel, M., Hayward, S. W. and Matusik, R. J. (2005) Forkhead box A1 regulates prostate ductal morphogenesis and promotes epithelial cell maturation. Development 132, 3431-3443.
39. Behr, R., Brestelli, J., Fulmer, J. T., Miyawaki, N., Kleyman, T. R. and Kaestner, K. H. (2004) Mild nephrogenic diabetes insipidus caused by Foxa1 deficiency. J. Biol. Chem. 279, 41936-41941.
40. Kaestner, K. H., Hiemisch, H. and Schutz, G. (1998) Targeted disruption of the gene encoding hepatocyte nuclear factor 3gamma results in reduced transcription of hepatocyte-specific genes. Mol. Cell Biol. 18, 4245-4251.
41. Lantz, K. A., Vatamaniuk, M. Z., Brestelli, J. E., Friedman, J. R., Matschinsky, F. M. and Kaestner, K. H. (2004) Foxa2 regulates multiple pathways of insulin secretion. J. Clin. Invest. 114, 512-520.
42. Lantz, K. A. and Kaestner, K. H. (2005) Winged-helix transcription factors and pancreatic development. Clin. Sci. (Lond) 108, 195-204.
43. Hussain, K., Clayton, P. T., Krywawych, S., Chatziandreou, I., Mills, P., Ginbey, D. W., Geboers, A. J., Berger, R., van den Berg, I. E. and Eaton, S. (2005) Hyperinsulinism of infancy associated with a novel splice site mutation in the SCHAD gene. J. Pediatr. 146, 706-708.
44. Molven, A., Matre, G. E., Duran, M., Wanders, R. J., Rishaug, U., Njolstad, P. R., Jellum, E. and Sovik, O. (2004) Familial hyperinsulinemic hypoglycemia caused by a defect in the SCHAD enzyme of mitochondrial fatty acid oxidation. Diabetes 53, 221-227.
45. Clayton, P. T., Eaton, S., Aynsley-Green, A., Edginton, M., Hussain, K., Krywawych, S., Datta, V., Malingre, H. E., Berger, R. and van den Berg, I. E. (2001) Hyperinsulinism in short-chain L-3-hydroxyacyl-CoA dehydrogenase deficiency reveals the importance of beta-oxidation in insulin secretion. J. Clin. Invest. 108, 457-465.
46. Zhang, L., Rubins, N. E., Ahima, R. S., Greenbaum, L. E. and Kaestner, K. H. (2005) Foxa2 integrates the transcriptional response of the hepatocyte to fasting. Cell Metab. 2, 141-148.
47. Wolfrum, C., Shih, D. Q., Kuwajima, S., Norris, A. W., Kahn, C. R. and Stoffel, M. (2003) Role of Foxa-2 in adipocyte metabolism and differentiation. J. Clin. Invest. 112, 345-356.
48. Wolfrum, C., Asilmaz, E., Luca, E., Friedman, J. M. and Stoffel, M. (2004) Foxa2 regulates lipid metabolism and ketogenesis in the liver during fasting and in diabetes. Nature 432, 1027-1032.
49. Wolfrum, C., Besser, D., Luca, E. and Stoffel, M. (2003) Insulin regulates the activity of forkhead transcription factor Hnf-3beta/Foxa-2 by Akt-mediated phosphorylation and nuclear/cytosolic localization. Proc. Natl. Acad. Sci. USA 100, 11624-11629.
50. Steneberg, P., Rubins, N., Bartoov-Shifman, R., Walker, M. D. and Edlund, H. (2005) The FFA receptor GPR40 links hyperinsulinemia, hepatic steatosis, and impaired glucose homeostasis in mouse. Cell Metab. 1, 245-258.
51. Bossard, P. and Zaret, K. S. (2000) Repressive and restrictive mesodermal interactions with gut endoderm: possible relation to Meckel's Diverticulum. Development 127, 4915-4923.
52. Zaret, K. (1999) Developmental competence of the gut endoderm: genetic potentiation by GATA and HNF3/fork head proteins. Dev. Biol. 209, 1-10.
53. Chaya, D., Hayamizu, T., Bustin, M. and Zaret, K. S. (2001) Transcription factor FoxA (HNF3) on a nucleosome at an enhancer complex in liver chromatin. J. Biol. Chem. 276, 44385-44389.
54. Cirillo, L. A. and Zaret, K. S. (1999) An early developmental transcription factor complex that is more stable on nucleosome core particles than on free DNA. Mol. Cell 4, 961-969.
55. Cirillo, L. A., McPherson, C. E., Bossard, P., Stevens, K., Cherian, S., Shim, E. Y., Clark, K. L., Burley, S. K. and Zaret, K. S. (1998) Binding of the winged-helix transcription factor HNF3 to a linker histone site on the nucleosome. EMBO J. 17, 244-254.
56. Shim, E. Y., Woodcock, C. and Zaret, K. S. (1998) Nucleosome positioning by the winged helix transcription factor HNF3. Genes Dev. 12, 5-10.
57. Carroll, J. S., Liu, X. S., Brodsky, A. S., Li, W., Meyer, C. A., Szary, A. J., Eeckhoute, J., Shao, W., Hestermann, E. V., Geistlinger, T. R., Fox, E. A., Silver, P. A. and Brown, M. (2005) Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122, 33-43.
58. Laganiere, J., Deblois, G., Lefebvre, C., Bataille, A. R., Robert, F. and Giguere, V. (2005) From the Cover: Location analysis of estrogen receptor alpha target promoters reveals that FOXA1 defines a domain of the estrogen response. Proc. Natl. Acad. Sci. USA 102, 11651-11656.
59. Lacroix, M. and Leclercq, G. (2004) About GATA3, HNF3A, and XBP1, three genes co-expressed with the oestrogen receptor-alpha gene (ESR1) in breast cancer. Mol. Cell. Endocrinol. 219, 1-7.
60. Huang, M. C., Li, K. K. and Spear, B. T. (2002) The mouse alpha-fetoprotein promoter is repressed in HepG2 hepatoma cells by hepatocyte nuclear factor-3 (FOXA). DNA Cell Biol. 21, 561-569.
61. Crowe, A. J., Sang, L., Li, K. K., Lee, K. C., Spear, B. T. and Barton, M. C. (1999) Hepatocyte nuclear factor 3 relieves chromatin-mediated repression of the alpha-fetoprotein gene. J. Biol. Chem. 274, 25113-25120.
62. Millonig, J. H., Emerson, J. A., Levorse, J. M. and Tilghman, S. M. (1995) Molecular analysis of the distal enhancer of the mouse alpha-fetoprotein gene. Mol. Cell. Biol. 15, 3848-3856.
63. Groupp, E. R., Crawford, N. and Locker, J. (1994) Characterization of the distal alpha-fetoprotein enhancer, a strong, long distance, liver-specific activator. J. Biol. Chem. 269, 22178-22187.
64. Scassa, M. E., Guberman, A. S., Ceruti, J. M. and Canepa, E. T. (2004) Hepatic nuclear factor 3 and nuclear factor 1 regulate 5-aminolevulinate synthase gene expression and are involved in insulin repression. J. Biol. Chem. 279, 28082-28092.
65. Schoneveld, O. J., Gaemers, I. C., Das, A. T., Hoogenkamp, M., Renes, J., Ruijter, J. M. and Lamers, W. H. (2004) Structural requirements of the glucocorticoid-response unit of the carbamoyl-phosphate synthase gene. Biochem. J. 382, 463-470.
66. Costa, R. H., Grayson, D. R., Xanthopoulos, K. G. and Darnell, J. E. Jr (1988) A liver-specific DNA-binding protein recognizes multiple nucleotide sites in regulatory regions of transthyretin, alpha 1-antitrypsin, albumin, and simian virus 40 genes. Proc. Natl. Acad. Sci. USA 85, 3840-3844.
67. Vallet, V., Antoine, B., Chafey, P., Vandewalle, A. and Kahn, A. (1995) Overproduction of a truncated hepatocyte nuclear factor 3 protein inhibits expression of liver-specific genes in hepatoma cells. Mol. Cell. Biol. 15, 5453-5460.
68. Gregori, C., Kahn, A. and Pichard, A. L. (1994) Activity of the rat liver-specific aldolase B promoter is restrained by HNF3. Nucleic Acids Res. 22, 1242-1246.
69. Gregori, C., Kahn, A. and Pichard, A. L. (1993) Competition between transcription factors HNF1 and HNF3, and alternative cell-specific activation by DBP and C/EBP contribute to the regulation of the liver-specific aldolase B promoter. Nucleic Acids Res. 21, 897-903.
70. Raymondjean, M., Pichard, A. L., Gregori, C., Ginot, F. and Kahn, A. (1991) Interplay of an original combination of factors: C/EBP, NFY, HNF3, and HNF1 in the rat aldolase B gene promoter. Nucleic Acids Res. 19, 6145-6153.
71. Harnish, D. C., Malik, S., Kilbourne, E., Costa, R. and Karathanasis, S. K. (1996) Control of apolipoprotein AI gene expression through synergistic interactions between hepatocyte nuclear factors 3 and 4. J. Biol. Chem. 271, 13621-13628.
72. Harnish, D. C., Malik, S. and Karathanasis, S. K. (1994) Activation of apolipoprotein AI gene transcription by the liver-enriched factor HNF-3. J. Biol. Chem. 269, 28220-28226.
73. Paulweber, B., Sandhofer, F. and Levy-Wilson, B. (1993) The mechanism by which the human apolipoprotein B gene reducer operates involves blocking of transcriptional activation by hepatocyte nuclear factor 3. Mol. Cell. Biol. 13, 1534-1546.
74. Arenzana, N. and Rodriguez de Cordoba, S. (1996) Promoter region of the human gene coding for beta-chain of C4b binding protein. Hepatocyte nuclear factor-3 and nuclear factor-I/CTF transcription factors are required for efficient expression of C4BPB in HepG2 cells. J. Immunol. 156, 168-175.
75. Williamson, E. A., Wolf, I., O'Kelly, J., Bose, S., Tanosaki, S. and Koeffler, H. P. (2005) BRCA1 and FOXA1 proteins coregulate the expression of the cell cycle-dependent kinase inhibitor p27(Kip1). Oncogene 25, 1391-1399.
76. Christoffels, V. M., Habets, P. E., Das, A. T., Clout, D. E., van Roon, M. A., Moorman, A. F. and Lamers, W. H. (2000) A single regulatory module of the carbamoylphosphate synthetase I gene executes its hepatic program of expression. J. Biol. Chem. 275, 40020-40027.
77. Christoffels, V. M., Grange, T., Kaestner, K. H., Cole, T. J., Darlington, G. J., Croniger, C. M. and Lamers, W. H. (1998) Glucocorticoid receptor, C/EBP, HNF3, and protein kinase A coordinately activate the glucocorticoid response unit of the carbamoylphosphate synthetase I gene. Mol. Cell. Biol. 18, 6305-6315.
78. Wiwi, C. A. and Waxman, D. J. (2005) Role of hepatocyte nuclear factors in transcriptional regulation of male-specific CYP2A2. J. Biol. Chem. 280, 3259-3268.
79. Park, S. H. and Waxman, D. J. (2001) Inhibitory cross-talk between STAT5b and liver nuclear factor HNF3beta: impact on the regulation of growth hormone pulse-stimulated, male-specific liver cytochrome P-450 gene expression. J. Biol. Chem. 276, 43031-43039.
80. Delesque-Touchard, N., Park, S. H. and Waxman, D. J. (2000) Synergistic action of hepatocyte nuclear factors 3 and 6 on CYP2C12 gene expression and suppression by growth hormone-activated STAT5b. Proposed model for female specific expression of CYP2C12 in adult rat liver. J. Biol. Chem. 275, 34173-34182.
81. Shaw, P. M., Weiss, M. C. and Adesnik, M. (1994) Hepatocyte nuclear factor 3 is a major determinant of CYP2C6 promoter activity in hepatoma cells. Mol Pharmacol. 46, 79-87.
82. Dogra, S. C. and May, B. K. (1997) Liver-enriched transcription factors, HNF-1, HNF-3, and C/EBP, are major contributors to the strong activity of the chicken CYP2H1 promoter in chick embryo hepatocytes. DNA Cell Biol. 16, 1407-1418.
83. Ceelie, H., Spaargaren-Van Riel, C. C., De Jong, M., Bertina, R. M. and Vos, H. L. (2003) Functional characterization of transcription factor binding sites for HNF1-alpha, HNF3-beta (FOXA2), HNF4-alpha, Sp1 and Sp3 in the human prothrombin gene enhancer. J. Thromb. Haemost. 1, 1688-1698.
84. Lin, B., Morris, D. W. and Chou, J. Y. (1997) The role of HN-F1alpha, HNF3gamma, and cyclic AMP in glucose-6-phosphatase gene activation. Biochemistry 36, 14096-14106.
85. Wang, H., Gauthier, B. R., Hagenfeldt-Johansson, K. A., Iezzi, M. and Wollheim, C. B. (2002) Foxa2 (HNF3beta) controls multiple genes implicated in metabolism-secretion coupling of glucose-induced insulin release. J. Biol. Chem. 277, 17564-17570.
86. Shih, D. Q., Heimesaat, M., Kuwajima, S., Stein, R., Wright, C. V. and Stoffel, M. (2002) Profound defects in pancreatic beta-cell function in mice with combined heterozygous mutations in Pdx-1, Hnf-1alpha, and Hnf-3beta. Proc. Natl. Acad. Sci. USA 99, 3818-3823.
87. Cha, J. Y., Kim, H. I., Im, S. S., Li, T. Z. and Ahn, Y. H. (2001) HNF1 and/or HNF3 may contribute to the tissue specific expression of glucokinase gene. Exp. Mol. Med. 33, 59-63.
88. Banks, K. E., Anderson, A. L., Tang, H., Hughes, D. E., Costa, R. H. and McLachlan, A. (2002) Hepatocyte nuclear factor 3beta inhibits hepatitis B virus replication in vivo. J. Virol. 76, 12974-12980.
89. Fukai, K., Takada, S., Yokosuka, O., Saisho, H., Omata, M. and Koike, K. (1997) Characterization of a specific region in the hepatitis B virus enhancer I for the efficient expression of X gene in the hepatic cell. Virology 236, 279-287.
90. Ori, A. and Shaul, Y. (1995) Hepatitis B virus enhancer binds and is activated by the hepatocyte nuclear factor 3. Virology 207, 98-106.
91. Johnson, J. L., Raney, A. K. and McLachlan, A. (1995) Characterization of a functional hepatocyte nuclear factor 3 binding site in the hepatitis B virus nucleocapsid promoter. Virology 208, 147-158.
92. Chen, M., Hieng, S., Qian, X., Costa, R. and Ou, J. H. (1994) Regulation of hepatitis B virus ENI enhancer activity by hepatocyte-enriched transcription factor HNF3. Virology 205, 127-132.
93. Allander, S. V., Durham, S. K., Scheimann, A. O., Wasserman, R. M., Suwanichkul, A. and Powell, D. R. (1997) Hepatic nuclear factor 3 and high mobility group I/Y proteins bind the insulin response element of the insulin-like growth factor-binding protein-1 promoter. Endocrinology 138, 4291-4300.
94. Unterman, T. G., Fareeduddin, A., Harris, M. A., Goswami, R. G., Porcella, A., Costa, R. H. and Lacson, R. G. (1994) Hepatocyte nuclear factor-3 (HNF-3) binds to the insulin response sequence in the IGF binding protein-1 (IGFBP-1) promoter and enhances promoter function. Biochem. Biophys. Res. Commun. 203, 1835-1841.
95. Lee, C. S., Sund, N. J., Vatamaniuk, M. Z., Matschinsky, F. M., Stoffers, D. A. and Kaestner, K. H. (2002) Foxa2 controls Pdx1 gene expression in pancreatic beta-cells in vivo. Diabetes 51, 2546-2551.
96. Ben-Shushan, E., Marshak, S., Shoshkes, M., Cerasi, E. and Melloul, D. (2001) A pancreatic beta -cell-specific enhancer in the human PDX-1 gene is regulated by hepatocyte nuclear factor 3beta (HNF-3beta), HNF-1alpha, and SPs transcription factors. J. Biol. Chem. 276, 17533-17540.
97. Wu, K. L., Gannon, M., Peshavaria, M., Offield, M. F., Henderson, E., Ray, M., Marks, A., Gamer, L. W., Wright, C. V. and Stein, R. (1997) Hepatocyte nuclear factor 3beta is involved in pancreatic beta-cell-specific transcription of the pdx-1 gene. Mol. Cell. Biol. 17, 6002-6013.
98. Wang, J. C., Stromstedt, P. E., O'Brien, R. M. and Granner, D. K. (1996) Hepatic nuclear factor 3 is an accessory factor required for the stimulation of phosphoenolpyruvate carboxykinase gene transcription by glucocorticoids. Mol. Endocrinol. 10, 794-800.
99. O'Brien, R. M., Noisin, E. L., Suwanichkul, A., Yamasaki, T., Lucas, P. C., Wang, J. C., Powell, D. R. and Granner, D. K. (1995) Hepatic nuclear factor 3- and hormone-regulated expression of the phosphoenolpyruvate carboxykinase and insulin-like growth factor-binding protein 1 genes. Mol. Cell. Biol. 15, 1747-1758.
100. Ip, Y. T., Poon, D., Stone, D., Granner, D. K. and Chalkley, R. (1990) Interaction of a liver-specific factor with an enhancer 4.8 kilobases upstream of the phosphoenolpyruvate carboxykinase gene. Mol. Cell. Biol. 10, 3770-3781.
101. Tsay, W., Lee, Y. M., Lee, S. C., Shen, M. C. and Chen, P. J. (1997) Synergistic transactivation of HNF-1alpha, HNF-3, and NF-I contributes to the activation of the liver-specific protein C gene. DNA Cell Biol. 16, 569-577.
102. Bingle, C. D., Hackett, B. P., Moxley, M., Longmore, W. and Gitlin, J. D. (1995) Role of hepatocyte nuclear factor-3 alpha and hepatocyte nuclear factor-3 beta in Clara cell secretory protein gene expression in the bronchiolar epithelium. Biochem. J. 308, 197-202.
103. Sawaya, P. L. and Luse, D. S. (1994) Two members of the HNF-3 family have opposite effects on a lung transcriptional element; HNF-3 alpha stimulates and HNF-3 beta inhibits activity of region I from the Clara cell secretory protein (CCSP) promoter. J. Biol. Chem. 269, 22211-22216.
104. Bohinski, R. J., Di Lauro, R. and Whitsett, J. A. (1994) The lung-specific surfactant protein B gene promoter is a target for thyroid transcription factor 1 and hepatocyte nuclear factor 3, indicating common factors for organ-specific gene expression along the foregut axis. Mol. Cell. Biol. 14, 5671-5681.
105. Bingle, C. D. and Gitlin, J. D. (1993) Identification of hepatocyte nuclear factor-3 binding sites in the Clara cell secretory protein gene. Biochem. J. 295, 227-232.
106. Costa, R. H., Grayson, D. R. and Darnell, J. E. Jr (1989) Multiple hepatocyte-enriched nuclear factors function in the regulation of transthyretin and alpha 1-antitrypsin genes. Mol. Cell. Biol. 9, 1415-1425.
107. Grayson, D. R., Costa, R. H. and Darnell, J. E. (1989) Regulation of hepatocyte-specific gene expression. Ann N Y Acad Sci 557, 243-255, discussion 255-246.
108. Grayson, D. R., Costa, R. H., Xanthopoulos, K. G. and Darnell, J. E. Jr (1988) A cell-specific enhancer of the mouse alpha 1-antitrypsin gene has multiple functional regions and corresponding protein-binding sites. Mol. Cell. Biol. 8, 1055-1066.
109. Grayson, D. R., Costa, R. H., Xanthopoulos, K. G. and Darnell, J. E. (1988) One factor recognizes the liver-specific enhancers in alpha 1-antitrypsin and transthyretin genes. Science 239, 786-788.
110. Yoshimi, T., Nakamura, N., Shimada, S., Iguchi, K., Hashimoto, F., Mochitate, K., Takahashi, Y. and Miura, T. (2005) Homeobox B3, FoxA1 and FoxA2 interactions in epithelial lung cell differentiation of the multipotent M3E3/C3 cell line. Eur. J. Cell Biol. 84, 555-566.
111. Wan, H., Xu, Y., Ikegami, M., Stahlman, M. T., Kaestner, K. H., Ang, S. L. and Whitsett, J. A. (2004) Foxa2 is required for transition to air breathing at birth. Proc. Natl. Acad. Sci. USA 101, 14449-14454.
112. He, Y., Crouch, E. C., Rust, K., Spaite, E. and Brody, S. L. (2000) Proximal promoter of the surfactant protein D gene: regulatory roles of AP-1, forkhead box, and GT box binding proteins. J. Biol. Chem. 275, 31051-31060.
113. Jeong, Y. and Epstein, D. J. (2003) Distinct regulators of Shh transcription in the floor plate and notochord indicate separate origins for these tissues in the mouse node. Development 130, 3891-3902.
114. Tan, Y., Costa, R. H., Kovesdi, I. and Reichel, R. R. (2001) Adenovirus-mediated increase of HNF-3 levels stimulates expression of transthyretin and sonic hedgehog, which is associated with F9 cell differentiation toward the visceral endoderm lineage. Gene Expr. 9, 237-248.
115. Jung, D., Hagenbuch, B., Fried, M., Meier, P. J. and Kullak-Ublick, G. A. (2004) Role of liver-enriched transcription factors and nuclear receptors in regulating the human, mouse, and rat NTCP gene. Am. J. Physiol. Gastrointest. Liver Physiol. 286, G752-761.
116. Rausa, F. M., Tan, Y., Zhou, H., Yoo, K. W., Stolz, D. B., Watkins, S. C., Franks, R. R., Unterman, T. G. and Costa, R. H. (2000) Elevated levels of hepatocyte nuclear factor 3beta in mouse hepatocytes influence expression of genes involved in bile acid and glucose homeostasis. Mol. Cell. Biol. 20, 8264-8282.
117. Cha, J. Y., Kim, H., Kim, K. S., Hur, M. W. and Ahn, Y. (2000) Identification of transacting factors responsible for the tissue-specific expression of human glucose transporter type 2 isoform gene. Cooperative role of hepatocyte nuclear factors 1alpha and 3beta. J. Biol. Chem. 275, 18358-18365.
118. Roux, J., Pictet, R. and Grange, T. (1995) Hepatocyte nuclear factor 3 determines the amplitude of the glucocorticoid response of the rat tyrosine aminotransferase gene. DNA Cell Biol. 14, 385-396.
119. Nitsch, D. and Schutz, G. (1993) The distal enhancer implicated in the developmental regulation of the tyrosine aminotransferase gene is bound by liver-specific and ubiquitous factors. Mol. Cell. Biol. 13, 4494-4504.
120. Nitsch, D., Boshart, M. and Schutz, G. (1993) Extinction of tyrosine aminotransferase gene activity in somatic cell hybrids involves modification and loss of several essential transcriptional activators. Genes Dev. 7, 308-319.
121. Beck, S., Sommer, P., dos Santos Silva, E., Blin, N. and Gott, P. (1999) Hepatocyte nuclear factor 3 (winged helix domain) activates trefoil factor gene TFF1 through a binding motif adjacent to the TATAA box. DNA Cell Biol. 18, 157-164.
122. Ikeda, K., Shaw-White, J. R., Wert, S. E. and Whitsett, J. A. (1996) Hepatocyte nuclear factor 3 activates transcription of thyroid transcription factor 1 in respiratory epithelial cells. Mol. Cell. Biol. 16, 3626-3636.
123. Auge-Gouillou, C., Petropoulos, I. and Zakin, M. M. (1993) Liver-enriched HNF-3 alpha and ubiquitous factors interact with the human transferrin gene enhancer. FEBS Lett. 323, 4-10.
124. Costa, R. H. and Grayson, D. R. (1991) Site-directed mutagenesis of hepatocyte nuclear factor (HNF) binding sites in the mouse transthyretin (TTR) promoter reveal synergistic interactions with its enhancer region. Nucleic Acids Res. 19, 4139-4145.
125. Costa, R. H., Lai, E., Grayson, D. R. and Darnell, J. E. Jr. (1988) The cell-specific enhancer of the mouse transthyretin (prealbumin) gene binds a common factor at one site and a liver-specific factor(s) at two other sites. Mol. Cell. Biol. 8, 81-90.
126. Robyr, D., Gegonne, A., Wolffe, A. P. and Wahli, W. (2000) Determinants of vitellogenin B1 promoter architecture. HNF3 and estrogen responsive transcription within chromatin. J. Biol. Chem. 275, 28291-28300.
127. Marilley, D., Robyr, D., Schild-Poulter, C. and Wahli, W. (1998) Regulation of the vitellogenin gene B1 promoter after transfer into hepatocytes in primary cultures. Mol. Cell. Endocrinol. 141, 79-93.
128. Cardinaux, J. R., Chapel, S. and Wahli, W. (1994) Complex organization of CTF/NF-I, C/EBP, and HNF3 binding sites within the promoter of the liver-specific vitellogenin gene. J. Biol. Chem. 269, 32947-32956.
129. Drewes, T., Klein-Hitpass, L. and Ryffel, G. U. (1991) Liver specific transcription factors of the HNF3-, C/EBP- and LFB1-families interact with the A-activator binding site. Nucleic Acids Res. 19, 6383-6389.
130. Shimizu, S., Kondo, M., Miyamoto, Y. and Hayashi, M. (2002) Foxa (HNF3) up-regulates vitronectin expression during retinoic acid-induced differentiation in mouse neuroblastoma Neuro2a cells. Cell Struct. Funct. 27, 181-188.
131. Shimizu, S., Miyamoto, Y. and Hayashi, M. (2002) Cell-type dependency of two Foxa/HNF3 sites in the regulation of vitronectin promoter activity. Biochim. Biophys. Acta 1574, 337-344.
132. Sund, N. J., Vatamaniuk, M. Z., Casey, M., Ang, S. L., Magnuson, M. A., Stoffers, D. A., Matschinsky, F. M. and Kaestner, K. H. (2001) Tissue-specific deletion of Foxa2 in pancreatic beta cells results in hyperinsulinemic hypoglycemia. Genes Dev. 15, 1706-1715.
133. Stroud, J. C., Wu, Y., Bates, D. L., Han, A., Nowick, K., Paabo, S., Tong, H. and Chen, L. (2006) Structure of the forkhead domain of FOXP2 bound to DNA. Structure 14, 159-166.
134. Chen, J., Anderson, J. B., DeWeese-Scott, C., Fedorova, N. D., Geer, L. Y., He, S., Hurwitz, D. I., Jackson, J. D., Jacobs, A. R., Lanczycki, C. J., Liebert, C. A., Liu, C., Madej, T., Marchler-Bauer, A., Marchler, G. H., Mazumder, R., Nikolskaya, A. N., Rao, B. S., Panchenko, A. R., Shoemaker, B. A., Simonyan, V., Song, J. S., Thiessen, P. A., Vasudevan, S., Wang, Y., Yamashita, R. A., Yin, J. J. and Bryant, S. H. (2003) MMDB: Entrez's 3D-structure database. Nucleic Acids Res. 31, 474-477.