Oxidative stress induces lipid-raft-mediated activation of Src homology 2 domain-containing protein-tyrosine phosphatase 2 in astrocytes

Free Radic Biol Med. 2009 Jun 15;46(12):1694-702. doi: 10.1016/j.freeradbiomed.2009.03.026. Epub 2009 Apr 5.

Abstract

Several protein phosphatases are involved in neuroprotection in response to ischemic brain injury. Here, we report that reactive oxygen species (ROS)-mediated oxidative stress promotes phosphorylation of endogenous SHP-2 through lipid rafts in rat primary astrocytes. SHP-2 was transiently phosphorylated during hypoxia/reoxygenation, an effect abrogated by a ROS scavenger and an NADPH oxidase inhibitor. Additionally, exogenous treatment with hydrogen peroxide (H(2)O(2)) triggered SHP-2 phosphorylation in a time- and dose-dependent manner and led to its translocation into lipid rafts. H(2)O(2)-mediated SHP-2 phosphorylation and translocation were inhibited by filipin III and methyl-beta-cyclodextrin (MCD), lipid-raft-disrupting agents. In the presence of H(2)O(2), SHP-2 formed a complex with STAT-3 and reduced the steady-state STAT-3 phosphorylation level. Interestingly, the effect of H(2)O(2) on SHP-2 phosphorylation was cell-type specific. Remarkably, SHP-2 phosphorylation was induced strongly by H(2)O(2) in astrocytes, but barely detectable in microglia. Our results collectively indicate that SHP-2 is activated by ROS-mediated oxidative stress in astrocytes and functions as a component of the raft-mediated signaling pathway that acts through dephosphorylation and inactivation of other phosphotyrosine proteins, such as STAT-3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Astrocytes / metabolism*
  • Cells, Cultured
  • Dose-Response Relationship, Drug
  • Enzyme Inhibitors / pharmacology
  • Filipin / pharmacology
  • Free Radical Scavengers / pharmacology
  • Hydrogen Peroxide / pharmacology
  • Membrane Microdomains / metabolism*
  • Oxidative Stress / physiology*
  • Phosphorylation
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / antagonists & inhibitors
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11 / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species / metabolism
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction / physiology
  • Time Factors
  • beta-Cyclodextrins / pharmacology

Substances

  • Enzyme Inhibitors
  • Free Radical Scavengers
  • Reactive Oxygen Species
  • STAT3 Transcription Factor
  • Stat3 protein, rat
  • beta-Cyclodextrins
  • methyl-beta-cyclodextrin
  • Filipin
  • Hydrogen Peroxide
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Ptpn11 protein, rat