CKIP-1 is an intrinsic negative regulator of T-cell activation through an interaction with CARMA1

PLoS One. 2014 Jan 17;9(1):e85762. doi: 10.1371/journal.pone.0085762. eCollection 2014.

Abstract

The transcription factor NF-κB plays a key regulatory role in lymphocyte activation and generation of immune response. Stimulation of T cell receptor (TCR) induces phosphorylation of CARMA1 by PKCθ, resulting in formation of CARMA1-Bcl10-MALT1 (CBM) complex at lipid rafts and subsequently leading to NF-κB activation. While many molecular events leading to NF-κB activation have been reported, it is less understood how this activation is negatively regulated. We performed a cell-based screening for negative regulators of TCR-mediated NF-κB activation, using mutagenesis and complementation cloning strategies. Here we show that casein kinase-2 interacting protein-1 (CKIP-1) suppresses PKCθ-CBM-NF-κB signaling. We found that CKIP-1 interacts with CARMA1 and competes with PKCθ for association. We further confirmed that a PH domain of CKIP-1 is required for association with CARMA1 and its inhibitory effect. CKIP-1 represses NF-κB activity in unstimulated cells, and inhibits NF-κB activation induced by stimulation with PMA or constitutively active PKCθ, but not by stimulation with TNFα. Interestingly, CKIP-1 does not inhibit NF-κB activation induced by CD3/CD28 costimulation, which caused dissociation of CKIP-1 from lipid rafts. These data suggest that CKIP-1 contributes maintenance of a resting state on NF-κB activity or prevents T cells from being activated by inadequate signaling. In conclusion, we demonstrate that CKIP-1 interacts with CARMA1 and has an inhibitory effect on PKCθ-CBM-NF-κB signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CARD Signaling Adaptor Proteins / metabolism*
  • Carrier Proteins / chemistry
  • Carrier Proteins / metabolism*
  • Enzyme Activation / drug effects
  • Guanylate Cyclase / metabolism*
  • Humans
  • Intracellular Signaling Peptides and Proteins
  • Isoenzymes / metabolism
  • Jurkat Cells
  • Lymphocyte Activation / drug effects
  • Lymphocyte Activation / immunology*
  • Membrane Microdomains / drug effects
  • Membrane Microdomains / metabolism
  • NF-kappa B / metabolism
  • Protein Binding / drug effects
  • Protein Kinase C / metabolism
  • Protein Kinase C-theta
  • Protein Structure, Tertiary
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / enzymology
  • T-Lymphocytes / immunology
  • Tetradecanoylphorbol Acetate / pharmacology

Substances

  • CARD Signaling Adaptor Proteins
  • Carrier Proteins
  • Intracellular Signaling Peptides and Proteins
  • Isoenzymes
  • NF-kappa B
  • PLEKHO1 protein, human
  • PRKCQ protein, human
  • Protein Kinase C
  • Protein Kinase C-theta
  • CARD11 protein, human
  • Guanylate Cyclase
  • Tetradecanoylphorbol Acetate

Grants and funding

This work was supported by JSPS KAKENHI Grant Number 23591383. The URL is http://www.jsps.go.jp/j-grantsinaid/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.