Regulation of M2-type pyruvate kinase mediated by the high-affinity IgE receptors is required for mast cell degranulation

Br J Pharmacol. 2008 Jul;154(5):1035-46. doi: 10.1038/bjp.2008.148. Epub 2008 Apr 21.

Abstract

Background and purpose: M2-type pyruvate kinase (M2PK) was found to interact directly with the 'ITAM' region of the gamma chain of the high-affinity IgE receptor (FcvarepsilonRI). Our hypothesis was that mast cell degranulation might require the FcvarepsilonRI-mediated inhibition of M2PK activity.

Experimental approach: In rat basophilic leukaemia (RBL-2H3) cells, the effects of directly inhibiting M2PK or preventing the FcvarepsilonRI-mediated inhibition of M2PK (disinhibition) on degranulation was measured by hexosaminidase release. Effects of blocking the FcvarepsilonRI-mediated inhibition of M2PK was also assessed in vivo in a mouse model of allergen-induced airway hyper-responsiveness.

Key results: Activation of FcvarepsilonRI in RBL-2H3 cells caused the rapid phosphorylation of tyrosine residues in M2PK, associated with a decrease in M2PK enzymatic activity. There was an inverse correlation between M2PK activity and mast cell degranulation. FcvarepsilonRI-mediated inhibition of M2PK involved Src kinase, phosphatidylinositol 3-kinase, PKC and calcium. Direct inhibition of M2PK potentiated FcvarepsilonRI-mediated degranulation and prevention of the FcvarepsilonRI-mediated inhibition of M2PK attenuated mast cell degranulation. Transfection of RBL-2H3 cells with M1PK which prevents FcvarepsilonRI-induced inhibition of M2PK, markedly reduced their degranulation and exogenous M1PK (i.p.) inhibited ovalbumin-induced airway hyper-responsiveness in vivo.

Conclusions and implications: We have identified a new control point and a novel biochemical pathway in the process of mast cell degranulation. Our study suggests that the FcvarepsilonRI-mediated inhibition of M2PK is a crucial step in responses to allergens. Moreover, the manipulation of glycolytic processes and intermediates could provide novel strategies for the treatment of allergic diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bronchial Hyperreactivity / enzymology
  • Bronchial Hyperreactivity / immunology
  • Bronchial Hyperreactivity / prevention & control
  • Calcium / metabolism
  • Cell Degranulation* / drug effects
  • Cell Line, Tumor
  • Disease Models, Animal
  • Down-Regulation
  • Enzyme Inhibitors / pharmacology
  • Female
  • Glycolysis*
  • Hexosaminidases / metabolism
  • Male
  • Mast Cells / drug effects
  • Mast Cells / enzymology*
  • Mast Cells / immunology
  • Mice
  • Mice, Inbred C57BL
  • Ovalbumin
  • Phosphatidylinositol 3-Kinases / metabolism
  • Phosphorylation
  • Protein Kinase C / metabolism
  • Pyruvate Kinase / genetics
  • Pyruvate Kinase / metabolism*
  • Rats
  • Receptors, IgE / genetics
  • Receptors, IgE / metabolism*
  • Signal Transduction
  • Transfection
  • src-Family Kinases / metabolism

Substances

  • Enzyme Inhibitors
  • Receptors, IgE
  • Ovalbumin
  • Phosphatidylinositol 3-Kinases
  • Pyruvate Kinase
  • src-Family Kinases
  • Protein Kinase C
  • Hexosaminidases
  • Calcium