Priming of eosinophils by GM-CSF is mediated by protein kinase CbetaII-phosphorylated L-plastin

J Immunol. 2011 Jun 1;186(11):6485-96. doi: 10.4049/jimmunol.1001868. Epub 2011 Apr 27.

Abstract

The priming of eosinophils by cytokines leading to augmented response to chemoattractants and degranulating stimuli is a characteristic feature of eosinophils in the course of allergic inflammation and asthma. Actin reorganization and integrin activation are implicated in eosinophil priming by GM-CSF, but their molecular mechanism of action is unknown. In this regard, we investigated the role of L-plastin, an eosinophil phosphoprotein that we identified from eosinophil proteome analysis. Phosphoproteomic analysis demonstrated the upregulation of phosphorylated L-plastin after eosinophil stimulation with GM-CSF. Additionally, coimmunoprecipitation studies demonstrated a complex formation of phosphorylated L-plastin with protein kinase CβII (PKCβII), GM-CSF receptor α-chain, and two actin-associated proteins, paxilin and cofilin. Inhibition of PKCβII with 4,5-bis(4-fluoroanilino)phtalimide or PKCβII-specific small interfering RNA blocked GM-CSF-induced phosphorylation of L-plastin. Furthermore, flow cytometric analysis also showed an upregulation of α(M)β(2) integrin, which was sensitive to PKCβII inhibition. In chemotaxis assay, GM-CSF treatment allowed eosinophils to respond to lower concentrations of eotaxin, which was abrogated by the above-mentioned PKCβII inhibitors. Similarly, inhibition of PKCβII blocked GM-CSF induced priming for degranulation as assessed by release of eosinophil cationic protein and eosinophil peroxidase in response to eotaxin. Importantly, eosinophil stimulation with a synthetic L-plastin peptide (residues 2-19) phosphorylated on Ser(5) upregulated α(M)β(2) integrin expression and increased eosinophil migration in response to eotaxin independent of GM-CSF stimulation. Our results establish a causative role for PKCβII and L-plastin in linking GM-CSF-induced eosinophil priming for chemotaxis and degranulation to signaling events associated with integrin activation via induction of PKCβII-mediated L-plastin phosphorylation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Actin Depolymerizing Factors / metabolism
  • Amino Acid Sequence
  • Blotting, Western
  • Cells, Cultured
  • Chemotaxis / drug effects
  • Electrophoresis, Gel, Two-Dimensional
  • Eosinophils / drug effects*
  • Eosinophils / metabolism
  • Granulocyte-Macrophage Colony-Stimulating Factor / pharmacology*
  • Humans
  • Integrins / metabolism
  • Membrane Glycoproteins / chemistry
  • Membrane Glycoproteins / metabolism*
  • Microfilament Proteins / chemistry
  • Microfilament Proteins / metabolism*
  • Molecular Sequence Data
  • Multiprotein Complexes / metabolism
  • Paxillin / metabolism
  • Peptides / pharmacology
  • Phosphoproteins / analysis
  • Phosphoproteins / metabolism
  • Phosphorylation / drug effects
  • Phthalimides / pharmacology
  • Protein Binding / drug effects
  • Protein Kinase C / antagonists & inhibitors
  • Protein Kinase C / genetics
  • Protein Kinase C / metabolism*
  • Protein Kinase C beta
  • Proteome / analysis
  • Proteome / metabolism
  • Proteomics / methods
  • RNA Interference
  • Receptors, Granulocyte-Macrophage Colony-Stimulating Factor / antagonists & inhibitors
  • Receptors, Granulocyte-Macrophage Colony-Stimulating Factor / metabolism
  • Recombinant Proteins
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization

Substances

  • 4,5-bis(4-fluoroanilino)phthalimide
  • Actin Depolymerizing Factors
  • Integrins
  • Membrane Glycoproteins
  • Microfilament Proteins
  • Multiprotein Complexes
  • Paxillin
  • Peptides
  • Phosphoproteins
  • Phthalimides
  • Proteome
  • Receptors, Granulocyte-Macrophage Colony-Stimulating Factor
  • Recombinant Proteins
  • plastin
  • Granulocyte-Macrophage Colony-Stimulating Factor
  • Protein Kinase C
  • Protein Kinase C beta