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J. Biol. Chem., Vol. 277, Issue 33, 29936-29944, August 16, 2002
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From the Cell and Cancer Biology Branch, Center for Cancer
Research, NCI, National Institutes of Health, Rockville, Maryland
20850
HIF-1
Hsp90 Regulates a von Hippel Lindau-independent
Hypoxia-inducible Factor-1
-degradative Pathway*
is a normally labile
proangiogenic transcription factor that is stabilized and
activated in hypoxia. Although the von Hippel Lindau (VHL) gene
product, the ubiquitin ligase responsible for regulating HIF-1
protein levels, efficiently targets HIF-1 for rapid
proteasome-dependent degradation under normoxia, HIF-1 is
resistant to the destabilizing effects of VHL under hypoxia. HIF-1
also associates with the molecular chaperone Hsp90. To examine the role
of Hsp90 in HIF-1 function, we used renal carcinoma cell (RCC) lines
that lack functional VHL and express stable HIF-1 protein under
normoxia. Geldanamycin (GA), an Hsp90 antagonist, promoted efficient
ubiquitination and proteasome-mediated degradation of HIF-1 in RCC
in both normoxia and hypoxia. Furthermore, HIF-1 point mutations
that block VHL association did not protect HIF-1 from GA-induced
destabilization. Hsp90 antagonists also inhibited HIF-1
transcriptional activity and dramatically reduced both hypoxia-induced
accumulation of VEGF mRNA and hypoxia-dependent angiogenic activity. These findings demonstrate that disruption of
Hsp90 function 1) promotes HIF-1 degradation via a novel, oxygen-independent E3 ubiquitin ligase and 2) diminishes HIF-1 transcriptional activity. Existence of an Hsp90-dependent
pathway for elimination of HIF-1 predicts that Hsp90 antagonists may be hypoxic cell sensitizers and possess antiangiogenic activity in vivo, thus extending the utility of these drugs as
therapeutic anticancer agents.
*
The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
To whom correspondence should be addressed: Cell and Cancer
Biology Branch, Center for Cancer Research, NCI, National Institutes of
Health, 9610 Medical Center Dr., Ste. 300, Rockville, MD 20850. Tel.:
301-402-3128 (ext. 318); Fax: 301-402-4422; E-mail:
len@helix.nih.gov.
Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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 P. de Candia, D. B. Solit, D. Giri, E. Brogi, P. M. Siegel, A. B. Olshen, W. J. Muller, N. Rosen, and R. Benezra Angiogenesis impairment in Id-deficient mice cooperates with an Hsp90 inhibitor to completely suppress HER2/neu-dependent breast tumors PNAS, October 14, 2003; 100(21): 12337 - 12342. [Abstract] [Full Text] [PDF]
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 M. P. Goetz, D. O. Toft, M. M. Ames, and C. Erlichman The Hsp90 chaperone complex as a novel target for cancer therapy Ann. Onc., August 1, 2003; 14(8): 1169 - 1176. [Abstract] [Full Text] [PDF]
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S. T. Palayoor, P. J. Tofilon, and C. N. Coleman Ibuprofen-mediated Reduction of Hypoxia-inducible Factors HIF-1{alpha} and HIF-2{alpha} in Prostate Cancer Cells Clin. Cancer Res., August 1, 2003; 9(8): 3150 - 3157. [Abstract] [Full Text] [PDF]
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E. Metzen, J. Zhou, W. Jelkmann, J. Fandrey, and B. Brune Nitric Oxide Impairs Normoxic Degradation of HIF-1{alpha} by Inhibition of Prolyl Hydroxylases Mol. Biol. Cell, August 1, 2003; 14(8): 3470 - 3481. [Abstract] [Full Text] [PDF]
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S.-k. Park, A. M. Dadak, V. H. Haase, L. Fontana, A. J. Giaccia, and R. S. Johnson Hypoxia-Induced Gene Expression Occurs Solely through the Action of Hypoxia-Inducible Factor 1{alpha} (HIF-1{alpha}): Role of Cytoplasmic Trapping of HIF-2{alpha} Mol. Cell. Biol., July 15, 2003; 23(14): 4959 - 4971. [Abstract] [Full Text] [PDF]
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L. E. Huang and H. F. Bunn Hypoxia-inducible Factor and Its Biomedical Relevance J. Biol. Chem., May 23, 2003; 278(22): 19575 - 19578. [Full Text] [PDF]
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E. Metzen, U. Berchner-Pfannschmidt, P. Stengel, J. H. Marxsen, I. Stolze, M. Klinger, W. Q. Huang, C. Wotzlaw, T. Hellwig-Burgel, W. Jelkmann, et al. Intracellular localisation of human HIF-1{alpha} hydroxylases: implications for oxygen sensing J. Cell Sci., April 1, 2003; 116(7): 1319 - 1326. [Abstract] [Full Text] [PDF]
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S. J. Welsh, R. R. Williams, A. Birmingham, D. J. Newman, D. L. Kirkpatrick, and G. Powis The Thioredoxin Redox Inhibitors 1-Methylpropyl 2-Imidazolyl Disulfide and Pleurotin Inhibit Hypoxia-induced Factor 1{alpha} and Vascular Endothelial Growth Factor Formation Mol. Cancer Ther., March 1, 2003; 2(3): 235 - 243. [Abstract] [Full Text] [PDF]
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Y.-J. Jung, J. S. Isaacs, S. Lee, J. Trepel, and L. Neckers Microtubule Disruption Utilizes an NFkappa B-dependent Pathway to Stabilize HIF-1alpha Protein J. Biol. Chem., February 21, 2003; 278(9): 7445 - 7452. [Abstract] [Full Text] [PDF]
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L. E. Huang, E. A. Pete, M. Schau, J. Milligan, and J. Gu Leu-574 of HIF-1alpha Is Essential for the von Hippel-Lindau (VHL)-mediated Degradation Pathway J. Biol. Chem., October 25, 2002; 277(44): 41750 - 41755. [Abstract] [Full Text] [PDF]
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D. A. Chan, P. D. Sutphin, N. C. Denko, and A. J. Giaccia Role of Prolyl Hydroxylation in Oncogenically Stabilized Hypoxia-inducible Factor-1alpha J. Biol. Chem., October 11, 2002; 277(42): 40112 - 40117. [Abstract] [Full Text] [PDF]
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W. Xu, M. Marcu, X. Yuan, E. Mimnaugh, C. Patterson, and L. Neckers Chaperone-dependent E3 ubiquitin ligase CHIP mediates a degradative pathway for c-ErbB2/Neu PNAS, October 1, 2002; 99(20): 12847 - 12852. [Abstract] [Full Text] [PDF]
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M. D. Basson Gut Mucosal Healing : Is the Science Relevant? Am. J. Pathol., October 1, 2002; 161(4): 1101 - 1105. [Full Text] [PDF]
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 J.M. ARBEIT Quiescent Hypervascularity Mediated by Gain of HIF-1{alpha} Function Cold Spring Harb Symp Quant Biol, January 1, 2002; 67(0): 133 - 142. [Abstract] [PDF]
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