99
Views
181
CrossRef citations to date
0
Altmetric
Article

Glycogen Synthase Kinase 3 Phosphorylates Hypoxia-Inducible Factor 1α and Mediates Its Destabilization in a VHL-Independent Manner

, , &
Pages 3253-3265 | Received 03 Jan 2007, Accepted 13 Feb 2007, Published online: 27 Mar 2023

REFERENCES

  • Abraham, R. T. 2004. mTOR as a positive regulator of tumor cell responses to hypoxia. Curr. Top. Microbiol. Immunol. 279:299–319.
  • Attwell, S., J. Mills, A. Troussard, C. Wu, and S. Dedhar. 2003. Integration of cell attachment, cytoskeletal localization, and signaling by integrin-linked kinase (ILK), CH-ILKBP, and the tumor suppressor PTEN. Mol. Biol. Cell 14:4813–4825.
  • Bardos, J. I., N. M. Chau, and M. Ashcroft. 2004. Growth factor-mediated induction of HDM2 positively regulates hypoxia-inducible factor 1α expression. Mol. Cell. Biol. 24:2905–2914.
  • Bournat, J. C., A. M. Brown, and A. P. Soler. 2000. Wnt-1 dependent activation of the survival factor NF-kappaB in PC12 cells. J. Neurosci. Res. 61:21–32.
  • Boyle, W. J., T. Smeal, L. H. Defize, P. Angel, J. R. Woodgett, M. Karin, and T. Hunter. 1991. Activation of protein kinase C decreases phosphorylation of c-Jun at sites that negatively regulate its DNA-binding activity. Cell 64:573–584.
  • Bruick, R. K., and S. L. McKnight. 2002. Transcription. Oxygen sensing gets a second wind. Science 295:807–808.
  • Bunn, H. F., and R. O. Poyton. 1996. Oxygen sensing and molecular adaptation to hypoxia. Physiol. Rev. 76:839–885.
  • Burroughs, K. D., J. Oh, J. C. Barrett, and R. P. DiAugustine. 2003. Phosphatidylinositol 3-kinase and mek1/2 are necessary for insulin-like growth factor-I-induced vascular endothelial growth factor synthesis in prostate epithelial cells: a role for hypoxia-inducible factor-1? Mol. Cancer Res. 1:312–322.
  • Carrero, P., K. Okamoto, P. Coumailleau, S. O'Brien, H. Tanaka, and L. Poellinger. 2000. Redox-regulated recruitment of the transcriptional coactivators CREB-binding protein and SRC-1 to hypoxia-inducible factor 1α. Mol. Cell. Biol. 20:402–415.
  • Chen, E. Y., N. M. Mazure, J. A. Cooper, and A. J. Giaccia. 2001. Hypoxia activates a platelet-derived growth factor receptor/phosphatidylinositol 3-kinase/Akt pathway that results in glycogen synthase kinase-3 inactivation. Cancer Res. 61:2429–2433.
  • Cohen, P., H. G. Nimmo, and C. G. Proud. 1978. How does insulin stimulate glycogen synthesis? Biochem. Soc. Symp. 1978:69–95.
  • Du, K., and M. Montminy. 1998. CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273:32377–32379.
  • Durand, M. K., J. S. Bodker, A. Christensen, D. M. Dupont, M. Hansen, J. K. Jensen, S. Kjelgaard, L. Mathiasen, K. E. Pedersen, S. Skeldal, T. Wind, and P. A. Andreasen. 2004. Plasminogen activator inhibitor-I and tumour growth, invasion, and metastasis. Thromb. Haemost. 91:438–449.
  • Ema, M., S. Taya, N. Yokotani, K. Sogawa, Y. Matsuda, and Y. Fujii-Kuriyama. 1997. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1alpha regulates the VEGF expression and is potentially involved in lung and vascular development. Proc. Natl. Acad. Sci. USA 94:4273–4278.
  • Embi, N., D. B. Rylatt, and P. Cohen. 1980. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur. J. Biochem. 107:519–527.
  • Feldser, D., F. Agani, N. V. Iyer, B. Pak, G. Ferreira, and G. L. Semenza. 1999. Reciprocal positive regulation of hypoxia-inducible factor 1 alpha and insulin-like growth factor 2. Cancer Res. 59:3915–3918.
  • Flamme, I., T. Frohlich, M. von-Reutern, A. Kappel, A. Damert, and W. Risau. 1997. HRF, a putative basic helix-loop-helix-PAS-domain transcription factor, is closely related to hypoxia-inducible factor-1 alpha and developmentally expressed in blood vessels. Mech. Dev. 63:51–60.
  • Frame, S., and P. Cohen. 2001. GSK3 takes centre stage more than 20 years after its discovery. Biochem. J. 359:1–16.
  • Fukuda, R., K. Hirota, F. Fan, Y. D. Jung, L. M. Ellis, and G. L. Semenza. 2002. Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J. Biol. Chem. 277:38205–38211.
  • Gorlach, A., I. Diebold, V. B. Schini-Kerth, U. Berchner-Pfannschmidt, U. Roth, R. P. Brandes, T. Kietzmann, and R. Busse. 2001. Thrombin activates the hypoxia-inducible factor-1 signaling pathway in vascular smooth muscle cells: role of the p22(phox)-containing NADPH oxidase. Circ. Res. 89:47–54.
  • Grimes, C. A., and R. S. Jope. 2001. The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling. Prog. Neurobiol. 65:391–426.
  • Gu, Y. Z., S. M. Moran, J. B. Hogenesch, L. Wartman, and C. A. Bradfield. 1998. Molecular characterization and chromosomal localization of a third alpha-class hypoxia inducible factor subunit, HIF3alpha. Gene Expr. 7:205–213.
  • Hardt, S. E., and J. Sadoshima. 2002. Glycogen synthase kinase-3beta: a novel regulator of cardiac hypertrophy and development. Circ. Res. 90:1055–1063.
  • Hirota, K., and G. L. Semenza. 2001. Rac1 activity is required for the activation of hypoxia-inducible factor 1. J. Biol. Chem. 276:21166–21172.
  • Hoeflich, K. P., J. Luo, E. A. Rubie, M. S. Tsao, O. Jin, and J. R. Woodgett. 2000. Requirement for glycogen synthase kinase-3beta in cell survival and NF-kappaB activation. Nature 406:86–90.
  • Hogenesch, J. B., W. K. Chan, V. H. Jackiw, R. C. Brown, Y. Z. Gu, G. M. Pray, G. H. Perdew, and C. A. Bradfield. 1997. Characterization of a subset of the basic-helix-loop-helix-PAS superfamily that interacts with components of the dioxin signaling pathway. J. Biol. Chem. 272:8581–8593.
  • Imahori, K., and T. Uchida. 1997. Physiology and pathology of Tau protein kinases in relation to Alzheimer's disease. J. Biochem. (Tokyo) 121:179–188.
  • Immenschuh, S., V. Hinke, A. Ohlmann, S. Gifhorn-Katz, N. Katz, K. Jungermann, and T. Kietzmann. 1998. Transcriptional activation of the heme oxygenase-1 gene by cGMP via a cAMP response element/activator protein-1 element in primary cultures of rat hepatocytes. Biochem. J. 334:141–146.
  • Ivan, M., K. Kondo, H. Yang, W. Kim, J. Valiando, M. Ohh, A. Salic, J. M. Asara, W. S. Lane, and W. G. Kaelin, Jr. 2001. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 292:464–468.
  • Jaakkola, P., D. R. Mole, Y. M. Tian, M. I. Wilson, J. Gielbert, S. J. Gaskell, A. Kriegsheim, H. F. Hebestreit, M. Mukherji, C. J. Schofield, P. H. Maxwell, C. W. Pugh, and P. J. Ratcliffe. 2001. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292:468–472.
  • Jungermann, K., and T. Kietzmann. 1996. Zonation of parenchymal and nonparenchymal metabolism in liver. Annu. Rev. Nutr. 16:179–203.
  • Kallio, P. J., K. Okamoto, S. O'Brien, P. Carrero, Y. Makino, H. Tanaka, and L. Poellinger. 1998. Signal transduction in hypoxic cells: inducible nuclear translocation and recruitment of the CBP/p300 coactivator by the hypoxia-inducible factor-1alpha. EMBO J. 17:6573–6586.
  • Kietzmann, T., Y. Cornesse, K. Brechtel, S. Modaressi, and K. Jungermann. 2001. Perivenous expression of the mRNA of the three hypoxia-inducible factor alpha-subunits, HIF1alpha, HIF2alpha and HIF3alpha, in rat liver. Biochem. J. 354:531–537.
  • Kietzmann, T., K. Jungermann, and A. Gorlach. 2003. Regulation of the hypoxia-dependent plasminogen activator inhibitor 1 expression by MAP kinases in HepG2 cells. Thromb. Haemost. 89:666–674.
  • Kietzmann, T., U. Roth, and K. Jungermann. 1999. Induction of the plasminogen activator inhibitor-1 gene expression by mild hypoxia via a hypoxia response element binding the hypoxia inducible factor-1 in rat hepatocytes. Blood 94:4177–4185.
  • Kietzmann, T., A. Samoylenko, U. Roth, and K. Jungermann. 2003. Hypoxia-inducible factor-1 and hypoxia response elements mediate the induction of plasminogen activator inhibitor-1 gene expression by insulin in primary rat hepatocytes. Blood 101:907–914.
  • Kops, G. J., N. D. de Ruiter, A. M. Vries-Smits, D. R. Powell, J. L. Bos, and B. M. Burgering. 1999. Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398:630–634.
  • Kruger, M., M. Schwaninger, R. Blume, E. Oetjen, and W. Knepel. 1997. Inhibition of CREB- and cAMP response element-mediated gene transcription by the immunosuppressive drugs cyclosporin A and FK506 in T cells. Naunyn Schmiedebergs Arch. Pharmacol. 356:433–440.
  • Lando, D., D. J. Peet, D. A. Whelan, J. Gorman, and M. L. Whitelaw. 2002. Aspargine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science 295:858–861.
  • Laughner, E., P. Taghavi, K. Chiles, P. C. Mahon, and G. L. Semenza. 2001. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1α (HIF-1α) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol. Cell. Biol. 21:3995–4004.
  • Liu, Q., U. Berchner-Pfannschmidt, U. Moller, M. Brecht, C. Wotzlaw, H. Acker, K. Jungermann, and T. Kietzmann. 2004. A Fenton reaction at the endoplasmic reticulum is involved in the redox control of hypoxia-inducible gene expression. Proc. Natl. Acad. Sci. USA 101:4302–4307.
  • Mahon, P. C., K. Hirota, and G. L. Semenza. 2001. FIH-1: a novel protein that interacts with HIF-1α and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 15:2675–2686.
  • Maxwell, P. H., and P. J. Ratcliffe. 2002. Oxygen sensors and angiogenesis. Semin. Cell Dev. Biol. 13:29–37.
  • Mazure, N. M., E. Y. Chen, K. R. Laderoute, and A. J. Giaccia. 1997. Induction of vascular endothelial growth factor by hypoxia is modulated by a phosphatidylinositol 3-kinase/Akt signaling pathway in Ha-ras-transformed cells through a hypoxia inducible factor-1 transcriptional element. Blood 90:3322–3331.
  • Miller, J. R., A. M. Hocking, J. D. Brown, and R. T. Moon. 1999. Mechanism and function of signal transduction by the Wnt/beta-catenin and Wnt/Ca2+ pathways. Oncogene 18:7860–7872.
  • Mottet, D., V. Dumont, Y. Deccache, C. Demazy, N. Ninane, M. Raes, and C. Michiels. 2003. Regulation of hypoxia-inducible factor-1alpha protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta pathway in HepG2 cells. J. Biol. Chem. 278:31277–31285.
  • Nikolakaki, E., P. J. Coffer, R. Hemelsoet, J. R. Woodgett, and L. H. Defize. 1993. Glycogen synthase kinase 3 phosphorylates Jun family members in vitro and negatively regulates their transactivating potential in intact cells. Oncogene 8:833–840.
  • Rubinfeld, B., I. Albert, E. Porfiri, C. Fiol, S. Munemitsu, and P. Polakis. 1996. Binding of GSK3beta to the APC-beta-catenin complex and regulation of complex assembly. Science 272:1023–1026.
  • Sadowski, I., and M. Ptashne. 1989. A vector for expressing GAL4(1-147) fusions in mammalian cells. Nucleic Acids Res. 17:7539.
  • Samoylenko, A., U. Roth, K. Jungermann, and T. Kietzmann. 2001. The upstream stimulatory factor-2a inhibits plasminogen activator inhibitor-1 gene expression by binding to a promoter element adjacent to the hypoxia-inducible factor-1 binding site. Blood 97:2657–2666.
  • Sandau, K. B., H. G. Faus, and B. Brune. 2000. Induction of hypoxia-inducible-factor 1 by nitric oxide is mediated via the PI 3K pathway. Biochem. Biophys. Res. Commun. 278:263–267.
  • Sears, R., F. Nuckolls, E. Haura, Y. Taya, K. Tamai, and J. R. Nevins. 2000. Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Genes Dev. 14:2501–2514.
  • Semenza, G. 2002. Signal transduction to hypoxia-inducible factor 1. Biochem. Pharmacol. 64:993–998.
  • Semenza, G. L. 2000. HIF-1: mediator of physiological and pathophysiological responses to hypoxia. J. Appl. Physiol. 88:1474–1480.
  • Semenza, G. L. 2001. Hypoxia-inducible factor 1: control of oxygen homeostasis in health and disease. Pediatr. Res. 49:614–617.
  • Semenza, G. L. 2001. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol. Med. 7:345–350.
  • Shaw, M., and P. Cohen. 1999. Role of protein kinase B and the MAP kinase cascade in mediating the EGF-dependent inhibition of glycogen synthase kinase 3 in Swiss 3T3 cells. FEBS Lett. 461:120–124.
  • Skinner, H. D., J. Z. Zheng, J. Fang, F. Agani, and B. H. Jiang. 2004. Vascular endothelial growth factor transcriptional activation is mediated by hypoxia-inducible factor 1α, HDM2, and p70S6K1 in response to phosphatidylinositol 3-kinase/AKT signaling. J. Biol. Chem. 279:45643–45651.
  • Sodhi, A., S. Montaner, H. Miyazaki, and J. S. Gutkind. 2001. MAPK and Akt act cooperatively but independently on hypoxia inducible factor-1α in rasV12 upregulation of VEGF. Biochem. Biophys. Res. Commun. 287:292–300.
  • Sonenberg, N., and A. C. Gingras. 1998. The mRNA 5′ cap-binding protein eIF4E and control of cell growth. Curr. Opin. Cell Biol. 10:268–275.
  • Stambolic, V., and J. R. Woodgett. 1994. Mitogen inactivation of glycogen synthase kinase-3 beta in intact cells via serine 9 phosphorylation. Biochem. J. 303:701–704.
  • Stiehl, D. P., W. Jelkmann, R. H. Wenger, and T. Hellwig-Burgel. 2002. Normoxic induction of the hypoxia-inducible factor 1α by insulin and interleukin-1β involves the phosphatidylinositol 3-kinase pathway. FEBS Lett. 512:157–162.
  • Takata, M., W. Ogawa, T. Kitamura, Y. Hino, S. Kuroda, K. Kotani, A. Klip, A. C. Gingras, N. Sonenberg, and M. Kasuga. 1999. Requirement for Akt (protein kinase B) in insulin-induced activation of glycogen synthase and phosphorylation of 4E-BP1 (PHAS-1). J. Biol. Chem. 274:20611–20618.
  • Tanimoto, K., Y. Makino, T. Pereira, and L. Poellinger. 2000. Mechanism of regulation of the hypoxia-inducible factor-1 alpha by the von Hippel-Lindau tumor suppressor protein. EMBO J. 19:4298–4309.
  • Treins, C., S. Giorgetti-Peraldi, J. Murdaca, G. L. Semenza, and E. Van Obberghen. 2002. Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J. Biol. Chem. 277:27975–27981.
  • Wenger, R. H. 2002. Cellular adaptation to hypoxia: O2-sensing protein hydroxylases, hypoxia-inducible transcription factors, and O2-regulated gene expression. FASEB J. 16:1151–1162.
  • Wenger, R. H., and M. Gassmann. 1997. Oxygen(es) and the hypoxia-inducible factor-1. Biol. Chem. 378:609–616.
  • Wenger, R. H., D. P. Stiehl, and G. Camenisch. 2005. Integration of oxygen signaling at the consensus HRE. Sci. STKE 2005:re12.
  • Woods, Y. L., P. Cohen, W. Becker, R. Jakes, M. Goedert, X. Wang, and C. G. Proud. 2001. The kinase DYRK phosphorylates protein-synthesis initiation factor eIF2Bε at Ser539 and the microtubule-associated protein Tau at Thr212: potential role for DYRK as a glycogen synthase kinase 3-priming kinase. Biochem. J. 355:609–615.
  • Zelzer, E., Y. Levy, C. Kahana, B. Z. Shilo, M. Rubinstein, and B. Cohen. 1998. Insulin induces transcription of target genes through the hypoxia-inducible factor HIF-1alpha/ARNT. EMBO J. 17:5085–5094.
  • Zhong, H., K. Chiles, D. Feldser, E. Laughner, C. Hanrahan, M. M. Georgescu, J. W. Simons, and G. L. Semenza. 2000. Modulation of hypoxia-inducible factor 1 alpha expression by the epidermal growth factor/phosphatidylinositol 3-kinase/PTEN/AKT/FRAP pathway in human prostate cancer cells: implications for tumor angiogenesis and therapeutics. Cancer Res. 60:1541–1545.
  • Zundel, W., C. Schindler, K. D. Haas, A. Koong, F. Kaper, E. Chen, A. R. Gottschalk, H. E. Ryan, R. S. Johnson, A. B. Jefferson, D. Stokoe, and A. J. Giaccia. 2000. Loss of PTEN facilitates HIF-1-mediated gene expression. Genes Dev. 14:391–396.

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.