Regulation of the tyrosine kinase Pyk2 by calcium is through production of reactive oxygen species in cytotoxic T lymphocytes

J Biol Chem. 2010 Oct 8;285(41):31174-84. doi: 10.1074/jbc.M110.118265. Epub 2010 Aug 5.

Abstract

Pyk2 was identified as a Ca(2+)-dependent kinase, however, the regulation of Pyk2 by Ca(2+) in T cells remains controversial. We found that Ca(2+) mobilization preferentially induced Pyk2 phosphorylation in cytotoxic T lymphocytes (CTL). Furthermore, Pyk2 phosphorylation in CTL was not absolutely Ca(2+) dependent but relied on the strength of T cell receptor stimulation. Ionomycin-stimulated Pyk2 phosphorylation did not require calmodulin activity, because phosphorylation was not inhibited by the calmodulin inhibitor W7, and we detected no Ca(2+)-regulated association between Pyk2 and calmodulin. Ca(2+)-stimulated Pyk2 phosphorylation was dependent on Src-family kinase activity, even at the Pyk2 autophosphorylation site. We sought to identify a Ca(2+)-regulated pathway that could trigger Pyk2 phosphorylation in T cells and found that ionomycin stimulated the production of reactive oxygen species and an H(2)O(2) scavenger inhibited ionomycin-induced Pyk2 phosphorylation. Additionally, H(2)O(2) induced strong Erk activation and ionomycin-stimulated Pyk2 phosphorylation was Erk dependent. These data support the conclusion that Ca(2+) mobilization induces the production of reactive oxygen species, which in turn activate the Erk pathway, leading to Src-family kinase-dependent Pyk2 phosphorylation. Our data demonstrate that Pyk2 is not a Ca(2+)-dependent kinase in T cells but instead, increased intracellular Ca(2+) induces Pyk2 phosphorylation through production of reactive oxygen species. These findings are consistent with the possibility that Pyk2 acts as an early sensor of numerous extracellular signals that trigger a Ca(2+) flux and/or reactive oxygen species to amplify tyrosine phosphorylation signaling events.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • CD8-Positive T-Lymphocytes / cytology
  • CD8-Positive T-Lymphocytes / enzymology*
  • Calcium / metabolism*
  • Calcium Signaling / drug effects*
  • Calcium Signaling / physiology
  • Enzyme Activation / drug effects
  • Enzyme Activation / physiology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Focal Adhesion Kinase 2 / metabolism*
  • Humans
  • Hydrogen Peroxide / metabolism
  • Hydrogen Peroxide / pharmacology*
  • Ionomycin / pharmacology
  • Ionophores / pharmacology
  • Jurkat Cells
  • Mice
  • Oxidants / metabolism
  • Oxidants / pharmacology*
  • Phosphorylation / drug effects
  • Phosphorylation / physiology
  • Rats
  • src-Family Kinases / metabolism

Substances

  • Ionophores
  • Oxidants
  • Ionomycin
  • Hydrogen Peroxide
  • Focal Adhesion Kinase 2
  • PTK2B protein, human
  • Ptk2b protein, mouse
  • Ptk2b protein, rat
  • src-Family Kinases
  • Extracellular Signal-Regulated MAP Kinases
  • Calcium