Angiotensin II induces hypoxia-inducible factor-1 alpha in PC 12 cells through a posttranscriptional mechanism: role of AT2 receptors

Am J Nephrol. 2004 Jul-Aug;24(4):415-21. doi: 10.1159/000080086. Epub 2004 Aug 11.

Abstract

Background: Angiotensin II (ANG II) inhibits proliferation and induces differentiation in PC 12 cells via AT(2) receptor activation. Using differential display analysis, we previously isolated SM-20/PHD3 as a key factor, which is downregulated by ANG II treatment. Subsequently, it turned out that SM-20/PHD3 is a rat homologue of PHD3, a key prolyl hydroxylase involved in the initial steps fostering the degradation of hypoxia-inducible factor (HIF). The present study was undertaken to investigate whether the ANG-II-mediated suppression of SM-20/PHD3/PHD3 may be associated with an increase in HIF-1 alpha.

Methods: HIF-1 alpha protein expression was assessed by Western blots. mRNA levels for HIF-1 alpha were measured by real-time PCR and for SM-20/PHD3 by Northern blots. Binding of HIF-1 alpha to consensus oligonucleotides in vitro was determined with gel shift analysis. SM-20/PHD3 was transiently overexpressed in PC 12 cells using an inducible expression system.

Results: ANG II stimulated HIF-1alpha protein expression. This effect was already detected after 30 min and peaked at 6 h, but was not detectable anymore after 24- 48 h of stimulation. PD 123177, but not losartan, antagonized this effect, indicating transduction through AT(2) receptors. Real-time PCR failed to show a significant increase in HIF-1 alpha transcripts after ANG II challenge at any time point. Gel shift analysis revealed that ANG-II-induced nuclear HIF-1 alpha protein binds to consensus sites. A reduction in SM-20/PHD3 mRNA expression paralleled the increase in HIF-1 alpha. Overexpression of SM-20/PHD3 transiently resulted in a decrease in HIF-1 alpha protein concentrations under basal conditions as well as after stimulation with ANG II.

Conclusion: ANG II stimulates HIF-1 alpha expression by a posttranscriptional mechanism via AT(2) receptors. This increase is likely caused by a downregulation of SM-20/PHD3. The ANG-II-mediated increase in HIF-1 alpha expression could be potentially involved in physiological as well as pathophysiological processes such as differentiation, growth inhibition, and remodeling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiotensin II / antagonists & inhibitors
  • Angiotensin II / pharmacology*
  • Angiotensin II Type 1 Receptor Blockers / pharmacology
  • Angiotensin II Type 2 Receptor Blockers
  • Animals
  • Gene Expression / drug effects
  • Gene Expression / physiology
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Imidazoles / pharmacology
  • Losartan / pharmacology
  • PC12 Cells
  • Pyridines / pharmacology
  • RNA Processing, Post-Transcriptional / drug effects*
  • RNA, Messenger / metabolism
  • Rats
  • Receptor, Angiotensin, Type 2 / metabolism*
  • Transcription Factors / genetics*
  • Up-Regulation / drug effects
  • Vasoconstrictor Agents / antagonists & inhibitors
  • Vasoconstrictor Agents / pharmacology*

Substances

  • Angiotensin II Type 1 Receptor Blockers
  • Angiotensin II Type 2 Receptor Blockers
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Imidazoles
  • Pyridines
  • RNA, Messenger
  • Receptor, Angiotensin, Type 2
  • Transcription Factors
  • Vasoconstrictor Agents
  • Angiotensin II
  • PD 123177
  • Losartan