Interleukin-6-Induced STAT3 and AP-1 Amplify Hepatocyte Nuclear Factor 1-Mediated Transactivation of Hepatic Genes, an Adaptive Response to Liver Injury

REFERENCES

• Babajko, S., and A. Groyer. 1993. Interplay of liver-enriched trans-acting factors, DBP and HNF1 in the transactivation of human IGFBP-1 promoter. Biochem. Biophys. Res. Commun. 196:480–486.
   PubMedGoogle Scholar
• Babajko, S., F. Tronche, and A. Groyer. 1993. Liver-specific expression of human insulin-like growth factor binding protein-1: functional role of transcription factor HNF-1 in vivo. Proc. Natl. Acad. Sci. USA 90:272–276.
   PubMedGoogle Scholar
• Baumhueter, S., G. Courtois, and G. R. Crabtree. 1988. A variant nuclear protein in dedifferentiated hepatoma cells binds to the same functional sequences in the β fibrinogen gene promoter as HNF-1. EMBO J. 7:2485–2493.
   PubMedGoogle Scholar
• Cereghini, S.. 1996. Liver-enriched transcription factors and hepatocyte differentiation. FASEB J. 10:267–282.
   PubMed Web of Science ®Google Scholar
• Costa, R. H., D. R. Grayson, K. G. Xanthopoulos, and J. E. Darnell Jr.. 1988. A liver specific DNA binding protein recognizes multiple nucleotide sites in regulatory regions of transthyretin, α1-antitrypsin, albumin, and simian virus 40 genes. Proc. Natl. Acad. Sci. USA 85:3840–3844.
   PubMedGoogle Scholar
• Courtois, G., S. Baumhueter, and G. R. Crabtree. 1988. Purified hepatocyte nuclear factor 1 interacts with a family of hepatocyte specific promoters. Proc. Natl. Acad. Sci. USA 85:7937–7941.
   PubMedGoogle Scholar
• Courtois, G., J. G. Morgan, L. A. Campbell, G. Fourel, and G. R. Crabtree. 1987. Interaction of a liver specific nuclear factor with the fibrinogen and α-1 antitrypsin promoters. Science 238:688–692.
   PubMed Web of Science ®Google Scholar
• Cressman, D. E., L. E. Greenbaum, R. A. DeAngelis, G. Ciliberto, E. E. Furth, V. Poli, and R. Taub. 1996. Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science 22:1379–1383.
   Google Scholar
• Crissey, M. S., J. I. Leu, R. A. DeAngelis, L. E. Greenbaum, L. M. Scearce, K. Kovalovich, and R. Taub. 1999. Liver specific and proliferation-induced deoxyribonuclease I hypersensitive sites in the mouse insulin-like growth factor binding protein-1 gene. Hepatology 30:1187–1197.
   PubMedGoogle Scholar
• Curran, T.. 1988. The fos oncogene. The oncogene handbook.. E. P. Reddy, A. M. Skalka, and T. Curran. 307–325. Elsevier, Amsterdam, The Netherlands
   Google Scholar
• Dalmon, J., M. Laurent, and G. Courtois. 1993. The human beta fibrinogen promoter contains a hepatocyte nuclear factor 1-dependent interleukin-6-responsive element. Mol. Cell. Biol. 13:1183–1193.
   PubMed Web of Science ®Google Scholar
• De Simone, V., G. Ciliberto, E. Hardon, G. Paonessa, F. Palla, L. Lundberg, and R. Cortese. 1987. Cis- and trans-acting elements responsible for the cell-specific expression of the human α1-antitrypsin gene. EMBO J. 6:2759–2766.
   PubMedGoogle Scholar
• Du, K., J. I. Leu, Y. Peng, and R. Taub. 1998. Transcriptional up-regulation of the delayed early gene HRS/SRp40 during liver regeneration. J. Biol. Chem. 273:35208–35215.
   PubMedGoogle Scholar
• Haber, B. A., S. Chin, E. Chuang, W. Buikhuisen, A. Naji, and R. Taub. 1995. High levels of glucose-6-phosphatase gene and protein expression in proliferating liver and diabetes. J. Clin. Investrs. 95:832–841.
   PubMed Web of Science ®Google Scholar
• Hardon, E., M. Frain, G. Paonessa, and R. Corteso. 1988. Two distinct factors interact with the promoter regions of several liver specific genes. EMBO J. 7:1711–1719.
   PubMed Web of Science ®Google Scholar
• Higgins, G. M., and R. M. Anderson. 1931. Restoration of the liver of the white rat following partial surgical removal. Arch. Pathol. 12:656–665.
   Google Scholar
• Hu, C.-H., J. E. Harris, E. W. Davie, and D. W. Chung. 1995. Characterization of the 5′-flanking region of the gene for the α chain of human fibrinogen. J. Biol. Chem. 270:28342–28349.
   PubMedGoogle Scholar
• Huber, P., J. Dalmon, G. Courtois, M. Laurent, Z. Assouline, and G. Marguerie. 1987. Characterization of the 5′-flanking region for the human fibrinogen beta gene. Nucleic Acids Res. 15:1615–1625.
   PubMedGoogle Scholar
• Huber, P., M. Laurent, and J. Dalmon. 1990. Human beta-fibrinogen gene expression. Upstream sequences involved in its tissue specific expression and its dexamethasone and interleukin 6 stimulation. J. Biol. Chem. 265:5695–5701.
   PubMedGoogle Scholar
• Janknecht, R., and T. Hunter. 1996. A growing coactivator network. Nature 383:22–23.
   PubMed Web of Science ®Google Scholar
• Janknecht, R., and T. Hunter. 1996. Transcriptional control: versatile molecular glue. Curr. Biol. 6:951–954.
   PubMed Web of Science ®Google Scholar
• Janknecht, R., and T. Hunter. 1999. Nuclear fusion of signaling pathways. Science 284:443–444.
   PubMedGoogle Scholar
• Kaptein, A., V. Paillard, and M. Saunders. 1996. Dominant negative STAT3 mutant inhibits interleukin-6 induced Jak-STAT signal transduction. J. Biol. Chem. 271:5961–5964.
   PubMedGoogle Scholar
• Kovalovich, K., R. A. DeAngelis, W. Li, E. Furth, G. Ciliberto, and R. Taub. 2000. Increased toxin-induced liver injury and fibrosis in interleukin-6 deficient mice. Hepatology 31:149–159.
   PubMed Web of Science ®Google Scholar
• Ktistaki, E., and I. Talianidis, I.. 1997. Modulation of hepatic gene expression by hepatic nuclear factor 1. Science 277:109–112.
   PubMedGoogle Scholar
• Lee, J., L. Greenbaum, B. A. Haber, D. Nagle, V. Lee, V. Miles, K. L. Mohn, M. Bucan, and R. Taub. 1994. Structure and localization of the IGFBP-1 gene and its expression during liver regeneration. Hepatology 19:656–665.
   PubMedGoogle Scholar
• Lee, P.D.K., L. C. Giudice, C. A. Conover, and D. R. Powell. 1997. Insulin-like growth factor binding protein-1: recent findings and new directions. Proc. Soc. Exp. Bio. Med. 216:319–357.
   PubMed Web of Science ®Google Scholar
• Lee, Y. R. Hintz, P. James, P. Lee, J. Shively, and D. R. Powell. 1988. Insulin-like growth factor (IGF) binding protein complementary deoxyribonucleic acid from human HEP G2 hepatoma cells: fredicted sequence suggests an IGF binding domain different from those of the IGF-I and IGF-II receptors. Mol. Endocrinol. 2:404–411.
   PubMed Web of Science ®Google Scholar
• Li, S. P., and N. D. Goldman. 1996. Regulation of human C-reactive protein gene expression by two synergistic IL-6 responsive elements. Biochemistry 35:9060–9068.
   PubMed Web of Science ®Google Scholar
• Lin, B., D. W. Morris, and J. Y. Chou. 1998. Hepatocyte nuclear factor 1alpha is an accessory factor required for activation of glucose-6-phosphatase gene transcription by glucocorticoids. DNA Cell Biol. 17:967–974.
   PubMed Web of Science ®Google Scholar
• Lin, B., D. W. Morris, and J. Y. Chou. 1998. The role of HNF1α, HNF3γ, and cyclic AMP in glucose-6-phosphatase gene activation. Biochemistry 36:14096–14106.
   Google Scholar
• Liu, Z., and G. M. Fuller. 1995. Detection of a novel transcription factor for the A alpha-fibrinogen gene in response to interleukin-6. J. Biol. Chem. 270:7580–7586.
   PubMed Web of Science ®Google Scholar
• Maione, D., E. Di Carlo, W. Li, P. Musiani, A. Modesti, M. Peters, S. Rose-John, C. Della Rocca, M. Tripodi, D. Lazzaro, R. Taub, R. Savino, and G. Ciliberto. 1998. Coexpression of IL-6 and soluble IL-6 receptor causes nodular regenerative hyperplasia and adenomas of the liver. EMBO J. 17:5588–5597.
   PubMed Web of Science ®Google Scholar
• Maire, P., J. Wuarin, and U. Schibler. 1989. The role of cis-acting promoter elements in tissue-specific albumin gene expression. Science 244:343–346.
   PubMed Web of Science ®Google Scholar
• Michalopoulos, G. K., and M. C. DeFrances. 1997. Liver regeneration. Science 276:60–66.
   PubMed Web of Science ®Google Scholar
• Mizuguchi, J., C.-H. Hu, Z. Cao, K. R. Loeb, D. W. Chung, and E. W. Davie. 1995. Characterization of the 5′ flanking region of the gene for the γ chain of human fibrinogen. J. Biol. Chem. 270:28350–28356.
   PubMedGoogle Scholar
• Mohn, K. L., T. M. Laz, A. E. Melby, and R. Taub. 1990. Immediate early gene expression differs between regenerating liver, insulin-stimulated H-35 cells, and mitogen-stimulated 3T3 cells: liver specific induction patterns of gene 33, PEPCK, and the jun, fos, and egr families. J. Biol. Chem. 265:21914–21921.
   PubMed Web of Science ®Google Scholar
• Mohn, K. L., A. E. Melby, D. S. Tewari, T. M. Laz, and R. Taub. 1991. The gene encoding rat insulin like growth factor binding protein 1 is rapidly and highly induced in regenerating liver. Mol. Cell. Biol. 11:1393–1401.
   PubMed Web of Science ®Google Scholar
• Morgan, J. I., and T. Curran. 1991. Stimulus-transcription coupling in the nervous system: involvement of the inducible protooncogenes fos and jun. Annu. Rev. Neurosci. 14:421–451.
   PubMed Web of Science ®Google Scholar
• Moshage, H.. 1997. Cytokines and the hepatic acute phase response. J. Pathol. 181:257–266.
   PubMed Web of Science ®Google Scholar
• Nagarajan, R. P., J. Zhang, W. Li, and Y. Chen. 1999. Regulation of Smad7 promoter by direct association with Smad3 and Smad4. J. Biol. Chem. 274:33412–33418.
   PubMed Web of Science ®Google Scholar
• Nordlie, R. C., J. D. Foster, and A. J. Lange. 1999. Regulation of glucose production by the liver. Annu. Rev. Nutr. 19:379–406.
   PubMed Web of Science ®Google Scholar
• Peng, Y., A. Genin, N. B. Spinner, R. H. Diamond, and R. Taub. 1998. The gene encoding human nuclear protein tyrosine phosphatase, PRL-1. J. Biol. Chem. 273:17286–17295.
   PubMedGoogle Scholar
• Peng, Y., K. Du, S. Ramirez, R. H. Diamond, and R. Taub. 1999. Mitogenic up-regulation of the PRL-1 protein-tyrosine phosphatase gene by Egr-1. Egr-1 activation is an early event in liver regeneration. J. Biol. Chem. 274:4513–4520.
   PubMedGoogle Scholar
• Poli, V., R. Balena, E. Fattori, A. Markatos, M. Yamamoto, H. Tanaka, G. Ciliberto, G. A. Rodan, and F. Costantini. 1994. Interleukin-6 deficient mice are protected from bone loss caused by estrogen depletion. EMBO J. 13:1189–1196.
   PubMed Web of Science ®Google Scholar
• Powell, D. R., and A. Suwanichkul. 1993. HNF1 activates transcription of the human gene for insulin-like growth factor binding protein-1. DNA Cell Biol. 12:283–289.
   PubMedGoogle Scholar
• Rollini, P., and R. E. K. Fournier. 1999. The HNF-4/HNF-1α transactivation cascade regulates gene activity and chromatin structure of the human serine protease inhibitor gene cluster at 14q32.1. Proc. Natl. Acad. Sci. USA 96:10308–10313.
   PubMedGoogle Scholar
• Ryffel, G. U., W. Kugler, U. Wagner, and M. Kaling. 1989. Liver-specific gene transcription in vitro: the promoter element HP1 and a TATA box are necessary and sufficient to generate a liver-specific promoter. Nucleic Acids Res. 17:939–953.
   PubMedGoogle Scholar
• Samstein, B., M. L. Hoimes, J. Fan, R. A. Frost, M. C. Gelato, and C. H. Lang. 1996. IL-6 stimulation of insulin-like growth factor binding protein (IGFBP)-1 production. Biochem. Biophys. Res. Commun. 228:611–615.
   PubMed Web of Science ®Google Scholar
• Scearce, L. M., D. E. Cressman, and R. Taub. 1996. Early transcriptional changes in regenerating liver reflect triggering mechanisms. Death Differ. 3:47–55.
   PubMedGoogle Scholar
• Soutoglou, E., G. Papafotiou, N. Katrakili, and I. Talianidis. 2000. Transcriptional activation by hepatocyte nuclear factor-1 requires synergism between multiple coactivator proteins. J. Biol. Chem. 275:12515–12520.
   PubMed Web of Science ®Google Scholar
• Streeper, R. S., C. A. Svitek, J. K. Goldman, and R. M. O'Brian. 2000. Differential role of hepatocyte nuclear factor-1 in the regulation of glucose-6-phosphatase catalytic subunit gene transcription by cAMP in liver- and kidney-derived cell lines. J. Biol. Chem. 275:12108–12118.
   PubMedGoogle Scholar
• Suwanichkul, A., M. L. Cubbage, and D. R. Powell. 1990. The promoter region of the human gene for insulin-like growth factor binding protein-1. J. Biol. Chem. 265:21185–21193.
   PubMedGoogle Scholar
• Taub, R.. 1996. Liver regeneration 4: transcriptional control of liver regeneration. FASEB J. 10:413–427.
   PubMed Web of Science ®Google Scholar
• Taub, R.. 1996. Liver regeneration in health and disease. Clin. Lab. Med. 16:341–360.
   PubMedGoogle Scholar
• Taub, R.. 1999. Interleukin-6 and liver growth regulation. Proceedings of the International Falk Workshop: Normal and Malignant Liver Cell Growth.. X. Fleig. 68–74. Kluwer Academic Publishers, Dordrecht, The Netherlands
   Google Scholar
• Taub, R., L. E. Greenbaum, and Y. Peng. 1999. Transcriptional regulatory signals define cytokine-dependent and independent pathways in liver regeneration. Semin. Liver Dis. 19:17–127.
   PubMedGoogle Scholar
• Toniatti, C., A. Demartis, P. Monaci, A. Nicosia, and G. Ciliberto. 1990. Synergistic trans-activation of the human C-reactive protein promoter by transcription factor HNF1 binding at two distinct sites. EMBO J. 9:4467–4475.
   PubMedGoogle Scholar
• Tronche, F., A. Rollier, I. Bach, M. C. Weiss, and M. Yaniv. 1989. The rat albumin promoter: cooperation with upstream elements is required when binding of APF/HNF1 to the proximal element is impaired by mutations or bacterial methylation. Mol. Cell. Biol. 9:4759–4766.
   PubMedGoogle Scholar
• Tronche, F., and M. Yaniv. 1992. HNF1, a homeoprotein member of the hepatic transcription regulation network. Bioessays 14:579–587.
   PubMed Web of Science ®Google Scholar
• Tronche, F., F. Ringeisen, M. Blumenfeld, M. Yaniv, and M. Pontoglio. 1997. Analysis of the distribution of binding sites for a tissue-specific transcription factor in the vertebrate genome. J. Mol. Biol. 266:231–245.
   PubMedGoogle Scholar
• Ulloa, L., J. Doody, and J. Massague. 1999. Inhibition of transforming growth factor-β/SMAD signaling by the interferon-γ/STAT pathway. Nature 397:710–713.
   PubMed Web of Science ®Google Scholar
• Zhang, D., M. Sun, D. Samols, and I. Kushner. 1996. STAT3 participates in transcriptional activation of the C-reactive protein gene by interleukin-6. J. Biol. Chem. 271:9503–9509.
   PubMed Web of Science ®Google Scholar
• Zhang, X., M. H. Wrzeszczynska, C. M. Horvath, and J. E. Darnell Jr.. 1999. Interaction regions in Stat3 and c-Jun that participate in cooperative transcriptional activation. Mol. Cell. Biol. 19:7138–7146.
   PubMedGoogle Scholar
• Zhang, Z., N. L. Fuentes, and G. M. Fuller. 1995. Characterization of the IL-6 responsive elements in the γ fibrinogen gene promoter. J. Biol. Chem. 270:24287–24291.
   PubMedGoogle Scholar