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First published online 12 February 2003
doi: 10.1242/jcs.00318

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Journal of Cell Science 116, 1319-1326 (2003)
doi: 10.1242/jcs.00318

Research Article

Intracellular localisation of human HIF-1{alpha} hydroxylases: implications for oxygen sensing

Eric Metzen1,*, Utta Berchner-Pfannschmidt2, Petra Stengel1, Jan H. Marxsen1, Ineke Stolze2, Matthias Klinger3, Wei Qi Huang1, Christoph Wotzlaw4, Thomas Hellwig-Bürgel1, Wolfgang Jelkmann1, Helmut Acker4 and Joachim Fandrey2

1 Institute of Physiology, University of Lübeck, Ratzeburger Allee 160, D-23538 Lübeck, Germany
2 Institute of Physiology, University of Essen, Hufelandstr. 55, D-45122 Essen, Germany
3 Institute of Anatomy, University of Lübeck, Ratzeburger Allee 160, D-23538 Lübeck, Germany
4 Max-Planck-Institute of Molecular Physiology, Dortmund, Otto-Hahn-Straße 11, D-44227 Dortmund, Germany

* Author for correspondence (e-mail: metzen{at}physio.uni-luebeck.de)

Accepted 12 December 2002

Hypoxia-inducible factor1 (HIF-1) is an essential transcription factor for cellular adaptation to decreased oxygen availability. In normoxia the oxygen-sensitive {alpha}-subunit of HIF-1 is hydroxylated on Pro564 and Pro402 and thus targeted for proteasomal degradation. Three human oxygen-dependent HIF-1{alpha} prolyl hydroxylases (PHD1, PHD2, and PHD3) function as oxygen sensors in vivo. Furthermore, the asparagine hydroxylase FIH-1 (factor inhibiting HIF) has been found to hydroxylate Asp803 of the HIF-1 C-terminal transactivation domain, which results in the decreased ability of HIF-1 to bind to the transcriptional coactivator p300/CBP. We have fused these enzymes to the N-terminus of fluorescent proteins and transiently transfected the fusion proteins into human osteosarcoma cells (U2OS). Three-dimensional 2-photon confocal fluorescence microscopy showed that PHD1 was exclusively present in the nucleus, PHD2 and FIH-1 were mainly located in the cytoplasm and PHD3 was homogeneously distributed in cytoplasm and nucleus. Hypoxia did not influence the localisation of any enzyme under investigation. In contrast to FIH-1, each PHD inhibited nuclear HIF-1{alpha} accumulation in hypoxia. All hydroxylases suppressed activation of a cotransfected hypoxia-responsive luciferase reporter gene. Endogenous PHD2mRNA and PHD3mRNA were hypoxia-inducible, whereas expression of PHD1mRNA and FIH-1mRNA was oxygen independent. We propose that PHDs and FIH-1 form an oxygen sensor cascade of distinct subcellular localisation.

Key words: Hypoxia, Oxygen sensing, Hypoxia inducible factor, Hydroxylase




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