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

J Cell Sci. 2003 Apr 1;116(Pt 7):1319-26. doi: 10.1242/jcs.00318.

Abstract

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Compartmentation / physiology
  • Cell Hypoxia / physiology*
  • Cell Nucleus / enzymology*
  • Cytoplasm / enzymology*
  • Genes, Reporter / genetics
  • Green Fluorescent Proteins
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Luminescent Proteins
  • Mixed Function Oxygenases
  • Osteosarcoma / metabolism
  • Oxygen / metabolism*
  • Procollagen-Proline Dioxygenase / genetics
  • Procollagen-Proline Dioxygenase / metabolism*
  • Protein Isoforms / metabolism
  • RNA, Messenger / metabolism
  • Recombinant Fusion Proteins
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transcriptional Activation / genetics
  • Tumor Cells, Cultured

Substances

  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Luminescent Proteins
  • Protein Isoforms
  • RNA, Messenger
  • Recombinant Fusion Proteins
  • Repressor Proteins
  • Transcription Factors
  • Green Fluorescent Proteins
  • Mixed Function Oxygenases
  • HIF1AN protein, human
  • Procollagen-Proline Dioxygenase
  • Oxygen