A protective role for HIF-1 in response to redox manipulation and glucose deprivation: implications for tumorigenesis

Oncogene. 2002 Jan 10;21(2):282-90. doi: 10.1038/sj.onc.1205047.

Abstract

We have investigated the role of HIF-1 in the cellular response to redox modulation via the inhibition of oxidative phosphorylation. We demonstrate that manipulation of redox in air, achieved by inhibiting cytochrome oxidase with cyanide, induces HIF-1 mediated transcription in wild-type CHO and HT1080 human tumour cells but not in CHO cells deficient in the oxygen responsive, HIF-1alpha sub-unit of HIF-1. Hypoglycaemia attenuates cyanide-mediated transcription in non-transformed HIF-1 wild-type CHO cells but not the human tumour derived cell line. Cells lacking either HIF-1alpha, or the second composite sub-unit of HIF-1, HIF-1beta, were markedly more sensitive to the combined stress of perturbed redox and hypoglycaemia than wild-type cells. As such conditions together with hypoxia are prevalent in tumours, these data suggest that HIF-1 may have a protective role in adaptation to the tumour micro-environment. In support of this we demonstrate that HIF-1alpha deficient cells are less tumorigenic than wild-type cells. They showed a reduced growth rate when grown as xenografts in nude mice. This was not related to vascular parameters that were identical to those found in HIF-1 wild-type tumours. The HIF-1 deficient tumours lacked focal expression of Glut-1 in hypoxic tumour regions. Compromised glucose uptake and metabolic adaptation to the tumour micro-environment may form the basis of the reduced tumorigenicity associated with these cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CHO Cells
  • Cell Survival
  • Cell Transformation, Neoplastic*
  • Cricetinae
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism*
  • Female
  • Fibrosarcoma / blood supply
  • Fibrosarcoma / genetics*
  • Fibrosarcoma / pathology
  • Glucose / metabolism*
  • Glucose Transporter Type 1
  • Humans
  • Hypoglycemia / physiopathology
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Mice
  • Mice, Nude
  • Monosaccharide Transport Proteins / analysis
  • Monosaccharide Transport Proteins / genetics
  • Mutagenesis
  • Neovascularization, Pathologic / genetics
  • Nuclear Proteins / deficiency
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Oxidation-Reduction
  • Transcription Factors / metabolism
  • Transplantation, Heterologous
  • Tumor Cells, Cultured

Substances

  • DNA-Binding Proteins
  • Glucose Transporter Type 1
  • HIF1A protein, human
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Monosaccharide Transport Proteins
  • Nuclear Proteins
  • SLC2A1 protein, human
  • Slc2a1 protein, mouse
  • Transcription Factors
  • Glucose