Gain-of-function/Noonan syndrome SHP-2/Ptpn11 mutants enhance calcium oscillations and impair NFAT signaling

Proc Natl Acad Sci U S A. 2006 Feb 14;103(7):2160-5. doi: 10.1073/pnas.0510876103. Epub 2006 Feb 3.

Abstract

Gain-of-function mutations in SHP-2/PTPN11 cause Noonan syndrome, a human developmental disorder. Noonan syndrome is characterized by proportionate short stature, facial dysmorphia, increased risk of leukemia, and congenital heart defects in approximately 50% of cases. Congenital heart abnormalities are common in Noonan syndrome, but the signaling pathway(s) linking gain-of-function SHP-2 mutants to heart disease is unclear. Diverse cell types coordinate cardiac morphogenesis, which is regulated by calcium (Ca2+) and the nuclear factor of activated T-cells (NFAT). It has been shown that the frequency of Ca2+ oscillations regulates NFAT activity. Here, we show that in fibroblasts, Ca2+ oscillations in response to FGF-2 require the phosphatase activity of SHP-2. Conversely, gain-of-function mutants of SHP-2 enhanced FGF-2-mediated Ca2+ oscillations in fibroblasts and spontaneous Ca2+ oscillations in cardiomyocytes. The enhanced frequency of cardiomyocyte Ca2+ oscillations induced by a gain-of-function SHP-2 mutant correlated with reduced nuclear translocation and transcriptional activity of NFAT. These data imply that gain-of-function SHP-2 mutants disrupt the Ca2+ oscillatory control of NFAT, suggesting a potential mechanism for congenital heart defects in Noonan syndrome.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Animals
  • Calcium Signaling* / genetics
  • Cell Nucleus / chemistry
  • Cell Nucleus / metabolism
  • Cells, Cultured
  • Fibroblast Growth Factor 2 / pharmacology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Heart Valve Diseases / genetics
  • Heart Valve Diseases / metabolism*
  • Intracellular Signaling Peptides and Proteins / analysis
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism*
  • Mice
  • Mutation
  • Myocytes, Cardiac / metabolism
  • NFATC Transcription Factors / genetics
  • NFATC Transcription Factors / metabolism*
  • Noonan Syndrome / genetics
  • Noonan Syndrome / metabolism*
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases / analysis
  • Protein Tyrosine Phosphatases / genetics
  • Protein Tyrosine Phosphatases / metabolism*
  • Rats
  • Signal Transduction
  • Suppression, Genetic
  • Transcription, Genetic

Substances

  • Intracellular Signaling Peptides and Proteins
  • NFATC Transcription Factors
  • Fibroblast Growth Factor 2
  • PTPN11 protein, human
  • Protein Tyrosine Phosphatase, Non-Receptor Type 11
  • Protein Tyrosine Phosphatases
  • Ptpn11 protein, mouse
  • Ptpn11 protein, rat