CARMA1 regulation of regulatory T cell development involves modulation of interleukin-2 receptor signaling

J Biol Chem. 2010 May 21;285(21):15696-703. doi: 10.1074/jbc.M109.095190. Epub 2010 Mar 16.

Abstract

T cell receptor-stimulated NF-kappaB activation requires CARMA1 and is negatively regulated by the deubiquitinase CYLD. Recent studies suggest that CARMA1 regulates regulatory T cell (Treg) development, although the role of NF-kappaB in this event is incompletely understood. We show that CYLD deficiency causes constitutive NF-kappaB activation in thymocytes, which is associated with enhanced frequency of Treg cells. The NF-kappaB activation in CYLD-deficient thymocytes is independent of CARMA1, because the NF-kappaB activation was also detected in CYLD/CARMA1 double knock-out thymocytes. Interestingly, although loss of CYLD causes NF-kappaB activation in the CARMA1-deficient thymocytes, the CYLD deficiency fails to rescue the defect of CARMA1 knock-out mice in Treg development. Furthermore, inhibition of canonical NF-kappaB by an IkappaBalpha transgene only partially inhibits Treg development. We demonstrate that CARMA1 regulates IL-2 receptor signaling and controls the IL-2-stimulated maturation of Treg precursors to mature Tregs. These results suggest that the role of CARMA1 in Treg regulation involves both NF-kappaB activation and IL-2 receptor signaling.

Publication types

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

MeSH terms

  • Animals
  • CARD Signaling Adaptor Proteins / genetics
  • CARD Signaling Adaptor Proteins / metabolism*
  • Cysteine Endopeptidases / genetics
  • Cysteine Endopeptidases / metabolism*
  • Deubiquitinating Enzyme CYLD
  • I-kappa B Proteins / genetics
  • I-kappa B Proteins / metabolism
  • Interleukin-2 / genetics
  • Interleukin-2 / metabolism*
  • Mice
  • Mice, Knockout
  • NF-KappaB Inhibitor alpha
  • NF-kappa B / genetics
  • NF-kappa B / metabolism
  • Receptors, Interleukin-2 / genetics
  • Receptors, Interleukin-2 / metabolism*
  • Signal Transduction / physiology*
  • T-Lymphocytes, Regulatory / metabolism*

Substances

  • CARD Signaling Adaptor Proteins
  • Card11 protein, mouse
  • I-kappa B Proteins
  • Interleukin-2
  • NF-kappa B
  • Nfkbia protein, mouse
  • Receptors, Interleukin-2
  • NF-KappaB Inhibitor alpha
  • CYLD protein, mouse
  • Deubiquitinating Enzyme CYLD
  • Cysteine Endopeptidases