Phospholipase Cgamma2 is critical for Dectin-1-mediated Ca2+ flux and cytokine production in dendritic cells

J Biol Chem. 2009 Mar 13;284(11):7038-46. doi: 10.1074/jbc.M806650200. Epub 2009 Jan 9.

Abstract

Dectin-1 is a C-type lectin that recognizes beta-glucan in the cell walls of fungi and plays an important role in anti-fungal immunity. It signals via tyrosine kinase Syk and adaptor protein Card9 to activate NF-kappaB leading to proinflammatory cytokine production in dendritic cells (DCs). Other than this, not much else is known of the mechanism of Dectin-1 signaling. We demonstrate here that stimulation of DCs with zymosan triggers an intracellular Ca2+ flux that can be attenuated by a blocking anti-Dectin-1 antibody or by pre-treatment of cells with the phospholipase C (PLC) gamma-inhibitor U73122, suggesting that Dectin-1 signals via a PLCgamma pathway to induce Ca2+ flux in DCs. Interestingly, treatment of DCs with particulate curdlan, which specifically engages Dectin-1, results in the phosphorylation of both PLCgamma1 and PLCgamma2. However, we show that PLCgamma2 is the critical enzyme for Dectin-1 signaling in DCs. PLCgamma2-deficient DCs have drastic impairment of Ca2+ signaling and are defective in their secretion of interleukin 2 (IL-2), IL-6, IL-10, IL-12, IL-23, and tumor necrosis factor alpha. PLCgamma2-deficient DCs also exhibit impaired activation of ERK and JNK MAPKs and AP-1 and NFAT transcription factors in response to Dectin-1 stimulation. In addition, PLCgamma2-deficient DCs are also impaired in their activation of NF-kappaB upon Dectin-1 engagement due to defective assembly of the Card9-Bcl10-Malt1 complex and impaired IKKalpha/beta activation and IkappaBalpha degradation. Thus, our data indicate that pattern recognition receptors such as Dectin-1 could elicit Ca2+ signaling and that PLCgamma2 is a critical player in the Dectin-1 signal transduction pathway.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / immunology
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • B-Cell CLL-Lymphoma 10 Protein
  • CARD Signaling Adaptor Proteins
  • Calcium / immunology
  • Calcium / metabolism*
  • Calcium Signaling / drug effects
  • Calcium Signaling / physiology*
  • Caspases / genetics
  • Caspases / immunology
  • Caspases / metabolism
  • Cell Wall / immunology
  • Cell Wall / metabolism
  • Cytokines / immunology
  • Cytokines / metabolism*
  • Dendritic Cells / cytology
  • Dendritic Cells / enzymology*
  • Dendritic Cells / immunology
  • Enzyme Activation / drug effects
  • Enzyme Activation / immunology
  • Estrenes / pharmacology
  • Extracellular Signal-Regulated MAP Kinases / genetics
  • Extracellular Signal-Regulated MAP Kinases / immunology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Fungi / immunology
  • Fungi / metabolism
  • I-kappa B Kinase / genetics
  • I-kappa B Kinase / immunology
  • I-kappa B Kinase / metabolism
  • Lectins, C-Type
  • Membrane Proteins / genetics
  • Membrane Proteins / immunology
  • Membrane Proteins / metabolism*
  • Mice
  • Mice, Knockout
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein
  • NF-kappa B / genetics
  • NF-kappa B / immunology
  • NF-kappa B / metabolism
  • NFATC Transcription Factors / genetics
  • NFATC Transcription Factors / immunology
  • NFATC Transcription Factors / metabolism
  • Neoplasm Proteins / genetics
  • Neoplasm Proteins / immunology
  • Neoplasm Proteins / metabolism
  • Nerve Tissue Proteins / genetics
  • Nerve Tissue Proteins / immunology
  • Nerve Tissue Proteins / metabolism*
  • Phosphodiesterase Inhibitors / pharmacology
  • Phospholipase C gamma / genetics
  • Phospholipase C gamma / immunology
  • Phospholipase C gamma / metabolism*
  • Pyrrolidinones / pharmacology
  • Zymosan / pharmacology
  • beta-Glucans / pharmacology

Substances

  • Adaptor Proteins, Signal Transducing
  • B-Cell CLL-Lymphoma 10 Protein
  • Bcl10 protein, mouse
  • CARD Signaling Adaptor Proteins
  • Card9 protein, mouse
  • Cytokines
  • Estrenes
  • Lectins, C-Type
  • Membrane Proteins
  • NF-kappa B
  • NFATC Transcription Factors
  • Neoplasm Proteins
  • Nerve Tissue Proteins
  • Phosphodiesterase Inhibitors
  • Pyrrolidinones
  • beta-Glucans
  • dectin 1
  • 1-(6-((3-methoxyestra-1,3,5(10)-trien-17-yl)amino)hexyl)-1H-pyrrole-2,5-dione
  • curdlan
  • Zymosan
  • I-kappa B Kinase
  • Extracellular Signal-Regulated MAP Kinases
  • Phospholipase C gamma
  • Plcg1 protein, mouse
  • Caspases
  • Malt1 protein, mouse
  • Mucosa-Associated Lymphoid Tissue Lymphoma Translocation 1 Protein
  • Calcium