Inhibition of GSK3β by indirubins restores HIF-1α accumulation under prolonged periods of hypoxia/anoxia

FEBS Letters

Volumn 579, Issue 2, 2005, Pages 529-533

  Schnitzer, Steffen E ^a   Schmid, Tobias ^a   Zhou, Jie ^a   Eisenbrand, Gerhard ^a   Brüne, Bernhard ^a  

^a University of Koblenz Landau   (Germany)

Author keywords

Akt; HIF 1 ; Hypoxia; Indirubin; PI3K; Translation

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; GLYCOGEN SYNTHASE KINASE 3BETA; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDIRUBIN; MESSENGER RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; 2-(4-MORPHOLINYL)-8-PHENYL-4H-1-BENZOPYRAN-4-ONE; CHROMONE DERIVATIVE; CYCLOHEXIMIDE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; HIF1A PROTEIN, HUMAN; INDOLE DERIVATIVE; MORPHOLINE DERIVATIVE; PROTEASOME; PROTEIN KINASE INHIBITOR; TRANSCRIPTION FACTOR;

ANOXIA; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HYPOXIA; INCUBATION TIME; MODULATION; PRIORITY JOURNAL; REPRODUCIBILITY; RNA TRANSLATION; CELL HYPOXIA; DRUG ANTAGONISM; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN SYNTHESIS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; CELL HYPOXIA; CHROMONES; CYCLOHEXIMIDE; GENE EXPRESSION REGULATION; GLYCOGEN SYNTHASE KINASE 3; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INDOLES; MORPHOLINES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BIOSYNTHESIS; PROTEIN KINASE INHIBITORS; RNA, MESSENGER; TRANSCRIPTION FACTORS;

EID: 11844263980     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2004.12.023     Document Type: Article

References (28)

1. G. Semenza Signal transduction to hypoxia-inducible factor 1 Biochem. Pharmacol. 64 2002 993 998
2. L.E. Huang, and H.F. Bunn Hypoxia-inducible factor and its biomedical relevance J. Biol. Chem. 278 2003 19575 19578
3. G.L. Wang, B.H. Jiang, E.A. Rue, and G.L. Semenza Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension Proc. Natl. Acad. Sci. USA 92 1995 5510 5514
4. M. Ivan, K. Kondo, H. Yang, W. Kim, J. Valiando, M. Ohh, A. Salic, J.M. Asara, W.S. Lane, and W.G. Kaelin Jr. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing Science 292 2001 464 468
5. P. Jaakkola, 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 Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation Science 292 2001 468 472
6. E. Berra, E. Benizri, A. Ginouves, V. Volmat, D. Roux, and J. Pouyssegur HIF prolyl-hydroxylase 2 is the key oxygen sensor setting low steady-state levels of HIF-1alpha in normoxia EMBO J. 22 2003 4082 4090
7. R.K. Bruick, and S.L. McKnight A conserved family of prolyl-4- hydroxylases that modify HIF Science 294 2001 1337 1340
8. A.C. Epstein, J.M. Gleadle, L.A. McNeill, K.S. Hewitson, J. O'Rourke, D.R. Mole, M. Mukherji, E. Metzen, M.I. Wilson, A. Dhanda, Y.M. Tian, N. Masson, D.L. Hamilton, P. Jaakkola, R. Barstead, J. Hodgkin, P.H. Maxwell, C.W. Pugh, C.J. Schofield, and P.J. Ratcliffe C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation Cell 107 2001 43 54
9. J. Zhou, T. Schmid, and B. Brune Tumor necrosis factor-alpha causes accumulation of a ubiquitinated form of hypoxia inducible factor-1alpha through a nuclear factor-kappaB-dependent pathway Mol. Biol. Cell. 14 2003 2216 2225
10. B. Brune, and J. Zhou The role of nitric oxide (NO) in stability regulation of hypoxia inducible factor-1alpha (HIF-1alpha) Curr. Med. Chem. 10 2003 845 855
11. R. Fukuda, K. Hirota, F. Fan, Y.D. Jung, L.M. Ellis, and G.L. Semenza 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 2002 38205 38211
12. L.C. Cantley The phosphoinositide 3-kinase pathway Science 296 2002 1655 1657
13. C.A. Grimes, and R.S. Jope The multifaceted roles of glycogen synthase kinase 3beta in cellular signaling Prog. Neurobiol. 65 2001 391 426
14. X. Wang, M. Janmaat, A. Beugnet, F.E. Paulin, and C.G. Proud Evidence that the dephosphorylation of Ser(535) in the epsilon-subunit of eukaryotic initiation factor (eIF) 2B is insufficient for the activation of eIF2B by insulin Biochem. J. 367 2002 475 481
15. P. Cohen, and S. Frame The renaissance of GSK3 Nat. Rev. Mol. Cell Biol. 2 2001 769 776
16. D. Mottet, V. Dumont, Y. Deccache, C. Demazy, N. Ninane, M. Raes, and C. Michiels 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 2003 31277 31285
17. T.T. Tang, and L.A. Lasky The forkhead transcription factor FOXO4 induces the down-regulation of hypoxia-inducible factor 1 alpha by a von Hippel-Lindau protein-independent mechanism J. Biol. Chem. 278 2003 30125 30135
18. S. Leclerc, M. Garnier, R. Hoessel, D. Marko, J.A. Bibb, G.L. Snyder, P. Greengard, J. Biernat, Y.Z. Wu, E.M. Mandelkow, G. Eisenbrand, and L. Meijer Indirubins inhibit glycogen synthase kinase-3 beta and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer's disease. A property common to most cyclin-dependent kinase inhibitors? J. Biol. Chem. 276 2001 251 260
19. L. Meijer, A.L. Skaltsounis, P. Magiatis, P. Polychronopoulos, M. Knockaert, M. Leost, X.P. Ryan, C.A. Vonica, A. Brivanlou, R. Dajani, C. Crovace, C. Tarricone, A. Musacchio, S.M. Roe, L. Pearl, and P. Greengard GSK-3-selective inhibitors derived from Tyrian purple indirubins Chem. Biol. 10 2003 1255 1266
20. P. Polychronopoulos, P. Magiatis, A.L. Skaltsounis, V. Myrianthopoulos, E. Mikros, A. Tarricone, A. Musacchio, S.M. Roe, L. Pearl, M. Leost, P. Greengard, and L. Meijer Structural basis for the synthesis of indirubins as potent and selective inhibitors of glycogen synthase kinase-3 and cyclin-dependent kinases J. Med. Chem. 47 2004 935 946
21. J. Zhou, T. Schmid, R. Frank, and B. Brune PI3K/Akt is required for heat shock proteins to protect hypoxia-inducible factor 1alpha from pVHL-independent degradation J. Biol. Chem. 279 2004 13506 13513
22. D. Mottet, V. Dumont, Y. Deccache, C. Demazy, N. Ninane, M. Raes, and C. Michiels Regulation of HIF-1alpha protein level during hypoxic conditions by the PI3K/AKT/GSK3beta pathway in HepG2 cells J. Biol. Chem. 2003
23. B.H. Jiang, G. Jiang, J.Z. Zheng, Z. Lu, T. Hunter, and P.K. Vogt Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1 Cell Growth Differ. 12 2001 363 369
24. K.J. Lang, A. Kappel, and G.J. Goodall Hypoxia-inducible factor-1alpha mRNA contains an internal ribosome entry site that allows efficient translation during normoxia and hypoxia Mol. Biol. Cell 13 2002 1792 1801
25. A.M. Arsham, J.J. Howell, and M.C. Simon A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets J. Biol. Chem. 278 2003 29655 29660
26. M. Kleijn, G.C. Scheper, H.O. Voorma, and A.A. Thomas Regulation of translation initiation factors by signal transduction Eur. J. Biochem. 253 1998 531 544
27. R.E. Rhoads Signal transduction pathways that regulate eukaryotic protein synthesis J. Biol. Chem. 274 1999 30337 30340
28. T.E. Childs, E.E. Spangenburg, D.R. Vyas, and F.W. Booth Temporal alterations in protein signaling cascades during recovery from muscle atrophy Am. J. Physiol. Cell Physiol. 285 2003 C391 398