Tyrosine phosphatase SHP-2 regulates IL-1 signaling in fibroblasts through focal adhesions

J Cell Physiol. 2006 Apr;207(1):132-43. doi: 10.1002/jcp.20544.

Abstract

Interleukin-1beta (IL-1beta) mediates destruction of matrix collagens in diverse inflammatory diseases including arthritis, periodontitis, and pulmonary fibrosis by activating fibroblasts, cells that interact with matrix proteins through integrin-based adhesions. In vitro, IL-1beta signaling is modulated by focal adhesions, supramolecular protein complexes that are enriched with tyrosine kinases and phosphatases. We assessed the importance of tyrosine phosphatases in regulating cell-matrix interactions and IL-1beta signaling. In human gingival fibroblasts plated on fibronectin, IL-1beta enhanced the maturation of focal adhesions as defined by morphology and enrichment with paxillin and alpha-actinin. IL-1beta also induced activation of ERK and recruitment of phospho-ERK to focal complexes/adhesions. Treatment with the potent tyrosine phosphatase inhibitor pervanadate, in the absence of IL-1beta, recapitulated many of these responses indicating the importance of tyrosine phosphatases. Immunoblotting of collagen bead-associated complexes revealed that the tyrosine phosphatase, SHP-2, was also enriched in focal complexes/adhesions. Depletion of SHP-2 by siRNA or by homologous recombination markedly altered IL-1beta-induced ERK activation and maturation of focal adhesions. IL-1beta-induced tyrosine phosphorylation of SHP-2 on residue Y542 promoted focal adhesion maturation. Association of Gab1 with SHP-2 in focal adhesions correlated temporally with activation of ERK and was abrogated in cells expressing mutant (Y542F) SHP-2. We conclude that IL-1beta mediated maturation of focal adhesions is dependent on tyrosine phosphorylation of SHP-2 at Y542, leading to recruitment of Gab1, a process that may influence the downstream activation of ERK.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actinin / metabolism
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Cell Line
  • Cells, Cultured
  • Collagen / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism*
  • Fibronectins / pharmacology
  • Focal Adhesions / drug effects
  • Focal Adhesions / metabolism*
  • Humans
  • Interleukin-1 / pharmacology*
  • Intracellular Signaling Peptides and Proteins / antagonists & inhibitors
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Mice
  • Mutation
  • Paxillin / metabolism
  • Phosphorylation / drug effects
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases / antagonists & inhibitors
  • Protein Tyrosine Phosphatases / genetics
  • Protein Tyrosine Phosphatases / metabolism*
  • RNA, Small Interfering / genetics
  • Signal Transduction / physiology*
  • Transfection
  • Tyrosine / metabolism
  • Vanadates / pharmacology

Substances

  • Adaptor Proteins, Signal Transducing
  • Enzyme Inhibitors
  • Fibronectins
  • GAB1 protein, human
  • Interleukin-1
  • Intracellular Signaling Peptides and Proteins
  • Paxillin
  • RNA, Small Interfering
  • pervanadate
  • Actinin
  • Vanadates
  • Tyrosine
  • Collagen
  • Extracellular Signal-Regulated MAP Kinases
  • PTPN11 protein, human
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases
  • Ptpn11 protein, mouse