Role of ERK and calcium in the hypoxia-induced activation of HIF-1

J Cell Physiol. 2003 Jan;194(1):30-44. doi: 10.1002/jcp.10176.

Abstract

Oxygen-dependent regulation of HIF-1 activity occurs at multiple levels in vivo. The mechanisms regulating HIF-1alpha protein expression have been most extensively analyzed but the ones modulating HIF-1 transcriptional activity remain unclear. Changes in the phosphorylation and/or redox status of HIF-1alpha certainly play a role. Here, we show that ionomycin could activate HIF-1 transcriptional activity in a way that was additive to the effect of hypoxia without affecting HIF-1alpha protein level. In addition, a calmodulin dominant negative mutant and W7, a calmodulin antagonist, as well as BAPTA, an intracellular calcium chelator, inhibited the hypoxia-induced HIF-1 activation. These results indicate that elevated calcium in hypoxia could participate in HIF-1 activation. Furthermore, ERK but not JNK phosphorylation was evidenced in both conditions, ionomycin and hypoxia. PD98059, an inhibitor of the ERK pathway as well as a ERK1 dominant negative mutant also blocked HIF-1 activation by hypoxia and by ionomycin. A MEKK1 (a kinase upstream of JNK) dominant negative mutant had no effect. In addition, BAPTA, calmidazolium, a calmodulin antagonist and PD98059 inhibited VEGF secretion by hypoxic HepG2. All together, these results suggest that calcium and calmodulin would act upstream of ERK in the hypoxia signal transduction pathway.

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium Signaling / physiology*
  • Calmodulin / antagonists & inhibitors
  • Calmodulin / metabolism
  • Cell Hypoxia / physiology*
  • Cells, Cultured
  • Chelating Agents / pharmacology
  • DNA-Binding Proteins / drug effects
  • DNA-Binding Proteins / metabolism*
  • Dose-Response Relationship, Drug
  • Drug Interactions / physiology
  • Endothelial Growth Factors / metabolism
  • Enzyme Inhibitors / pharmacology
  • Eukaryotic Cells / metabolism*
  • Humans
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Ionomycin / pharmacology
  • Ionophores / pharmacology
  • Lymphokines / metabolism
  • Mitogen-Activated Protein Kinases / metabolism*
  • Nuclear Proteins / metabolism*
  • Transcription Factors*
  • Transcription, Genetic / physiology
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors

Substances

  • Calmodulin
  • Chelating Agents
  • DNA-Binding Proteins
  • Endothelial Growth Factors
  • Enzyme Inhibitors
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Intercellular Signaling Peptides and Proteins
  • Ionophores
  • Lymphokines
  • Nuclear Proteins
  • Transcription Factors
  • Vascular Endothelial Growth Factor A
  • Vascular Endothelial Growth Factors
  • Ionomycin
  • Mitogen-Activated Protein Kinases
  • Calcium