45
Views
35
CrossRef citations to date
0
Altmetric
Article

Hepatocyte Nuclear Factor 4α Contributes to Thyroid Hormone Homeostasis by Cooperatively Regulating the Type 1 Iodothyronine Deiodinase Gene with GATA4 and Krüppel-Like Transcription Factor 9

, , , , , , , , , , , , , , & show all
Pages 3917-3931 | Received 04 Dec 2007, Accepted 05 Apr 2008, Published online: 27 Mar 2023

REFERENCES

  • Amma, L. L., A. Campos-Barros, Z. Wang, B. Vennstrom, and D. Forrest. 2001. Distinct tissue-specific roles for thyroid hormone receptors β and α1 in regulation of type 1 deiodinase expression. Mol. Endocrinol. 15:467–475.
  • Anderson, K. P., C. B. Kern, S. C. Crable, and J. B. Lingrel. 1995. Isolation of a gene encoding a functional zinc finger protein homologous to erythroid Krüppel-like factor: identification of a new multigene family. Mol. Cell. Biol. 15:5957–5965.
  • 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.
  • Battle, M. A., G. Konopka, F. Parviz, A. L. Gaggl, C. Yang, F. M. Sladek, and S. A. Duncan. 2006. Hepatocyte nuclear factor 4α orchestrates expression of cell adhesion proteins during the epithelial transformation of the developing liver. Proc. Natl. Acad. Sci. USA 103:8419–8424.
  • Berry, M. J., L. Banu, Y. Y. Chen, S. J. Mandel, J. D. Kieffer, J. W. Harney, and P. R. Larsen. 1991. Recognition of UGA as a selenocysteine codon in type I deiodinase requires sequences in the 3′ untranslated region. Nature 353:273–276.
  • Berry, M. J., L. Banu, and P. R. Larsen. 1991. Type I iodothyronine deiodinase is a selenocysteine-containing enzyme. Nature 349:438–440.
  • Berry, M. J., D. Grieco, B. A. Taylor, A. L. Maia, J. D. Kieffer, W. Beamer, E. Glover, A. Poland, and P. R. Larsen. 1993. Physiological and genetic analyses of inbred mouse strains with a type I iodothyronine 5′ deiodinase deficiency. J. Clin. Investig. 92:1517–1528.
  • Bianco, A. C., and B. W. Kim. 2006. Deiodinases: implications of the local control of thyroid hormone action. J. Clin. Investig. 116:2571–2579.
  • Bianco, A. C., D. Salvatore, B. Gereben, M. J. Berry, and P. R. Larsen. 2002. Biochemistry, cellular and molecular biology, and physiological roles of the iodothyronine selenodeiodinases. Endocr. Rev. 23:38–89.
  • Bieker, J. J. 2001. Krüppel-like factors: three fingers in many pies. J. Biol. Chem. 276:34355–34358.
  • Cantor, A. B., and S. H. Orkin. 2002. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene 21:3368–3376.
  • Cayrou, C., R. J. Denver, and J. Puymirat. 2002. Suppression of the basic transcription element-binding protein in brain neuronal cultures inhibits thyroid hormone-induced neurite branching. Endocrinology 143:2242–2249.
  • Christoffolete, M. A., R. Arrojo e Drigo, F. Gazoni, S. M. Tente, V. Goncalves, B. S. Amorim, P. R. Larsen, A. C. Bianco, and A. M. Zavacki. 2007. Mice with impaired extrathyroidal thyroxine to 3,5,3′-triiodothyronine conversion maintain normal serum 3,5,3′-triiodothyronine concentrations. Endocrinology 148:954–960.
  • Dame, C., M. C. Sola, J. Fandrey, L. M. Rimsza, P. Freitag, G. Knopfle, R. D. Christensen, and J. Bungert. 2002. Developmental changes in the expression of transcription factors GATA-1, -2 and -3 during the onset of human medullary haematopoiesis. Br J. Haematol. 119:510–515.
  • Denver, R. J., L. Ouellet, D. Furling, A. Kobayashi, Y. Fujii-Kuriyama, and J. Puymirat. 1999. Basic transcription element-binding protein (BTEB) is a thyroid hormone-regulated gene in the developing central nervous system. Evidence for a role in neurite outgrowth. J. Biol. Chem. 274:23128–23134.
  • Glass, C. K. R., and G. Michael. 2000. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 14:121–141.
  • 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.
  • 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.
  • Iguchi, H., Y. Urashima, Y. Inagaki, Y. Ikeda, M. Okamura, T. Tanaka, A. Uchida, T. T. Yamamoto, T. Kodama, and J. Sakai. 2007. SOX6 suppresses cyclin D1 promoter activity by interacting with β-catenin and histone deacetylase 1, and its down-regulation induces pancreatic β-cell proliferation. J. Biol. Chem. 282:19052–19061.
  • 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.
  • Inoue, Y., G. P. Hayhurst, J. Inoue, M. Mori, and F. J. Gonzalez. 2002. Defective ureagenesis in mice carrying a liver-specific disruption of hepatocyte nuclear factor 4α (HNF4α). HNF4α regulates ornithine transcarbamylase in vivo. J. Biol. Chem. 277:25257–25265.
  • Inoue, Y., L. L. Peters, S. H. Yim, J. Inoue, and F. J. Gonzalez. 2006. Role of hepatocyte nuclear factor 4α in control of blood coagulation factor gene expression. J. Mol. Med. 84:334–344.
  • Inoue, Y., A. M. Yu, J. Inoue, and F. J. Gonzalez. 2004. Hepatocyte nuclear factor 4α is a central regulator of bile acid conjugation. J. Biol. Chem. 279:2480–2489.
  • Inoue, Y., A. M. Yu, S. H. Yim, X. Ma, K. W. Krausz, J. Inoue, C. C. Xiang, M. J. Brownstein, G. Eggertsen, I. Bjorkhem, and F. J. Gonzalez. 2006. Regulation of bile acid biosynthesis by hepatocyte nuclear factor 4α. J. Lipid Res. 47:215–227.
  • 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.
  • Kobayashi, A., K. Sogawa, H. Imataka, and Y. Fujii-Kuriyama. 1995. Analysis of functional domains of a GC box-binding protein, BTEB. J. Biochem. (Tokyo) 117:91–95.
  • Köhrle, J., F. Jakob, B. Contempre, and J. E. Dumont. 2005. Selenium, the thyroid, and the endocrine system. Endocr. Rev. 26:944–984.
  • 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.
  • Larsen, P. R., J. E. Silva, and M. M. Kaplan. 1981. Relationships between circulating and intracellular thyroid hormones: physiological and clinical implications. Endocr. Rev. 2:87–102.
  • Lavallée, G., G. Andelfinger, M. Nadeau, C. Lefebvre, G. Nemer, M. E. Horb, and M. Nemer. 2006. The Krüppel-like transcription factor KLF13 is a novel regulator of heart development. EMBO J. 25:5201–5213.
  • 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.
  • Leonard, J. L., and I. N. Rosenberg. 1980. Characterization of essential enzyme sulfhydryl groups of thyroxine 5′-deiodinase from rat kidney. Endocrinology 106:444–451.
  • Liang, G., J. Yang, J. D. Horton, R. E. Hammer, J. L. Goldstein, and M. S. Brown. 2002. Diminished hepatic response to fasting/refeeding and liver X receptor agonists in mice with selective deficiency of sterol regulatory element-binding protein-1c. J. Biol. Chem. 277:9520–9528.
  • Lu, J. R., T. A. McKinsey, H. Xu, D. Z. Wang, J. A. Richardson, and E. N. Olson. 1999. FOG-2, a heart- and brain-enriched cofactor for GATA transcription factors. Mol. Cell. Biol. 19:4495–4502.
  • Maia, A., M. Berry, R. Sabbag, J. Harney, and P. Larsen. 1995. Structural and functional differences in the dio1 gene in mice with inherited type 1 deiodinase deficiency. Mol. Endocrinol. 9:969–980.
  • Maia, A. L., J. Kieffer, J. Harney, and P. Larsen. 1995. Effect of 3,5,3′-triiodothyronine (T3) administration on dio1 gene expression and T3 metabolism in normal and type 1 deiodinase-deficient mice. Endocrinology 136:4842–4849.
  • Maia, A. L., J. W. Harney, and P. R. Larsen. 1995. Pituitary cells respond to thyroid hormone by discrete, gene-specific pathways. Endocrinology 136:1488–1494.
  • Matsushita, A., S. Sasaki, Y. Kashiwabara, K. Nagayama, K. Ohba, H. Iwaki, H. Misawa, K. Ishizuka, and H. Nakamura. 2007. Essential role of GATA2 in the negative regulation of thyrotropin β gene by thyroid hormone and its receptors. Mol. Endocrinol. 21:865–884.
  • Moeller, L. C., A. M. Dumitrescu, R. L. Walker, P. S. Meltzer, and S. Refetoff. 2005. Thyroid hormone responsive genes in cultured human fibroblasts. J. Clin. Endocrinol. Metab. 90:936–943.
  • Molkentin, J. D. 2000. The zinc finger-containing transcription factors GATA-4, -5, and -6. Ubiquitously expressed regulators of tissue-specific gene expression. J. Biol. Chem. 275:38949–38952.
  • Molkentin, J. D., J. R. Lu, C. L. Antos, B. Markham, J. Richardson, J. Robbins, S. R. Grant, and E. N. Olson. 1998. A calcineurin-dependent transcriptional pathway for cardiac hypertrophy. Cell 93:215–228.
  • 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.
  • Mouthon, M. A., O. Bernard, M. T. Mitjavila, P. H. Romeo, W. Vainchenker, and D. Mathieu-Mahul. 1993. Expression of tal-1 and GATA-binding proteins during human hematopoiesis. Blood 81:647–655.
  • Nuez, B., D. Michalovich, A. Bygrave, R. Ploemacher, and F. Grosveld. 1995. Defective haematopoiesis in fetal liver resulting from inactivation of the EKLF gene. Nature 375:316–318.
  • Oishi, Y., I. Manabe, K. Tobe, K. Tsushima, T. Shindo, K. Fujiu, G. Nishimura, K. Maemura, T. Yamauchi, N. Kubota, R. Suzuki, T. Kitamura, S. Akira, T. Kadowaki, and R. Nagai. 2005. Krüppel-like transcription factor KLF5 is a key regulator of adipocyte differentiation. Cell Metab. 1:27–39.
  • Owens, R. B., H. S. Smith, and A. J. Hackett. 1974. Epithelial cell cultures from normal glandular tissue of mice. J. Natl. Cancer Inst. 53:261–269.
  • Perkins, A. C., A. H. Sharpe, and S. H. Orkin. 1995. Lethal β-thalassaemia in mice lacking the erythroid CACCC-transcription factor EKLF. Nature 375:318–322.
  • Rhee, J., H. Ge, W. Yang, M. Fan, C. Handschin, M. Cooper, J. Lin, C. Li, and B. M. Spiegelman. 2006. Partnership of PGC-1α and HNF4α in the regulation of lipoprotein metabolism. J. Biol. Chem. 281:14683–14690.
  • Rhee, J., Y. Inoue, J. C. Yoon, P. Puigserver, M. Fan, F. J. Gonzalez, and B. M. Spiegelman. 2003. Regulation of hepatic fasting response by PPARγ coactivator-1α (PGC-1): requirement for hepatocyte nuclear factor 4α in gluconeogenesis. Proc. Natl. Acad. Sci. USA 100:4012–4017.
  • 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.
  • Schneider, M. J., S. N. Fiering, S. E. Pallud, A. F. Parlow, D. L. St. Germain, and V. A. Galton. 2001. Targeted disruption of the type 2 selenodeiodinase gene (DIO2) results in a phenotype of pituitary resistance to T4. Mol. Endocrinol. 15:2137–2148.
  • Schneider, M. J., S. N. Fiering, B. Thai, S.-Y. Wu, E. St. Germain, A. F. Parlow, D. L. St. Germain, and V. A. Galton. 2006. Targeted disruption of the type 1 selenodeiodinase gene (Dio1) results in marked changes in thyroid hormone economy in mice. Endocrinology 147:580–589.
  • Schoenmakers, C. H., I. G. Pigmans, A. Poland, and T. J. Visser. 1993. Impairment of the selenoenzyme type I iodothyronine deiodinase in C3H/He mice. Endocrinology 132:357–361.
  • Sladek, F. M., and S. D. Seidel. 2001. Hepatocyte nuclear factor 4α, p. 309-361. In T. P. Burris and E. R. B. McCabe (ed.), Nuclear receptors and genetic disease. Academic Press, San Diego, CA.
  • 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.
  • 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.
  • Song, A., A. Patel, K. Thamatrakoln, C. Liu, D. Feng, C. Clayberger, and A. M. Krensky. 2002. Functional domains and DNA-binding sequences of RFLAT-1/KLF13, a Krüppel-like transcription factor of activated T lymphocytes. J. Biol. Chem. 277:30055–30065.
  • Sumi, K., T. Tanaka, A. Uchida, K. Magoori, Y. Urashima, R. Ohashi, H. Ohguchi, M. Okamura, H. Kudo, K. Daigo, T. Maejima, N. Kojima, I. Sakakibara, S. Jiang, G. Hasegawa, I. Kim, T. F. Osborne, M. Naito, F. J. Gonzalez, T. Hamakubo, T. Kodama, and J. Sakai. 2007. Cooperative interaction between hepatocyte nuclear factor 4α and GATA transcription factors regulates ATP-binding cassette sterol transporters ABCG5 and ABCG8. Mol. Cell. Biol. 27:4248–4260.
  • Suske, G., E. Bruford, and S. Philipsen. 2005. Mammalian SP/KLF transcription factors: bring in the family. Genomics 85:551–556.
  • 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.
  • Svensson, E. C., R. L. Tufts, C. E. Polk, and J. M. Leiden. 1999. Molecular cloning of FOG-2: a modulator of transcription factor GATA-4 in cardiomyocytes. Proc. Natl. Acad. Sci. USA 96:956–961.
  • 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-4α in the pathogenesis of human cancer. J. Pathol. 208:662–672.
  • 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 δ induces fatty acid β-oxidation in skeletal muscle and attenuates metabolic syndrome. Proc. Natl. Acad. Sci. USA 100:15924–15929.
  • Tevosian, S. G., A. E. Deconinck, A. B. Cantor, H. I. Rieff, Y. Fujiwara, G. Corfas, and S. H. Orkin. 1999. FOG-2: a novel GATA-family cofactor related to multitype zinc-finger proteins Friend of GATA-1 and U-shaped. Proc. Natl. Acad. Sci. USA 96:950–955.
  • Tong, Q., J. Tsai, G. Tan, G. Dalgin, and G. S. Hotamisligil. 2005. Interaction between GATA and the C/EBP family of transcription factors is critical in GATA-mediated suppression of adipocyte differentiation. Mol. Cell. Biol. 25:706–715.
  • Toyoda, N., A. M. Zavacki, A. L. Maia, J. W. Harney, and P. R. Larsen. 1995. A novel retinoid X receptor-independent thyroid hormone response element is present in the human type 1 deiodinase gene. Mol. Cell. Biol. 15:5100–5112.
  • Wada, H., K. Hasegawa, T. Morimoto, T. Kakita, T. Yanazume, and S. Sasayama. 2000. A p300 protein as a coactivator of GATA-6 in the transcription of the smooth muscle-myosin heavy chain gene. J. Biol. Chem. 275:25330–25335.
  • 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 Krüppel-like factor KLF15 contributes fasting-induced transcriptional activation of mitochondrial acetyl-CoA synthetase gene AceCS2. J. Biol. Chem. 279:16954–16962.
  • Yet, S. F., M. M. McA'Nulty, S. C. Folta, H. W. Yen, M. Yoshizumi, C. M. Hsieh, M. D. Layne, M. T. Chin, H. Wang, M. A. Perrella, M. K. Jain, and M. E. Lee. 1998. Human EZF, a Krüppel-like zinc finger protein, is expressed in vascular endothelial cells and contains transcriptional activation and repression domains. J. Biol. Chem. 273:1026–1031.
  • Zhang, M., and J. Y. Chiang. 2001. Transcriptional regulation of the human sterol 12α-hydroxylase gene (CYP8B1): roles of hepatocyte nuclear factor 4α in mediating bile acid repression. J. Biol. Chem. 276:41690–41699.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.