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Originally published In Press as doi:10.1074/jbc.M110377200 on January 4, 2002

J. Biol. Chem., Vol. 277, Issue 11, 9262-9267, March 15, 2002
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Heat Induction of the Unphosphorylated Form of Hypoxia-inducible Factor-1alpha Is Dependent on Heat Shock Protein-90 Activity*

Dörthe M. KatschinskiDagger §||, Lu LeDagger , Daniel HeinrichDagger , Klaus F. WagnerDagger **, Thomas HoferDagger Dagger , Susann G. SchindlerDagger , and Roland H. WengerDagger §§§¶¶

From the Dagger  Institute of Physiology and ** Department of Anaesthesiology, Medical University of Lübeck, Ratzeburger Allee 160, D-23538 Lübeck, Germany and the Dagger Dagger  Institute of Physiology, University of Zürich, Winterthurerstrasse. 190, Zürich CH-8057, Switzerland

Hypoxia-inducible factor (HIF)-1alpha is the oxygen-sensitive subunit of HIF-1, a transcriptional master regulator of oxygen homeostasis. Oxygen-dependent prolyl hydroxylation targets HIF-1alpha for ubiquitinylation and proteasomal degradation. Unexpectedly, we found that exposing mice to elevated temperatures resulted in a strong HIF-1alpha induction in kidney, liver, and spleen. To elucidate the molecular mechanisms responsible for this effect, HepG2 hepatoma cells were exposed to different temperatures (34-42 °C) under normoxic (20% O2) or hypoxic (3% O2) conditions. Heat was sufficient to stabilize mainly a phosphatase-resistant, low molecular weight form of HIF-1alpha (termed HIF-1alpha a). Heat-induced HIF-1alpha a accumulated in the nucleus but neither bound to DNA nor trans-activated reporter or target gene expression, demonstrating the need for post-translational modifications for these functions. The protein banding pattern of heat-induced HIF-1alpha in immunoblot analyses was clearly distinct from the HIF-1alpha pattern after prolyl hydroxylase inhibition (by hypoxia or iron chelation/replacement) or following proteasome inhibition, suggesting that heat stabilizes HIF-1alpha by a novel mechanism. Inhibition of the ATP-dependent chaperone activity of HSP90 by novobiocin or geldanamycin prevented heat-induced as well as hypoxia-induced HIF-1alpha accumulation, indicating a common role of the HSP90 chaperone activity in HIF-1alpha stabilization by these two environmental parameters.

* 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.

§ Supported by grants from the Forschungsschwerpunkt Onkologie of the Medical University of Lübeck.

Supported by Deutsche Forschungsgemeinschaft Grant GRK288.

|| To whom correspondence should be addressed. Tel.: 49-451-500-4152; Fax: 49-451-500-4151; E-mail: katschinski@physio.mu-luebeck.de.

§§ Supported by Deutsche Forschungsgemeinschaft Grant We2672/1-1.

¶¶ Present address: Carl-Ludwig-Institute of Physiology, University of Leipzig, Liebigstrasse 27, D-04103 Leipzig, Germany.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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