Roquin-2 shares functions with its paralog Roquin-1 in the repression of mRNAs controlling T follicular helper cells and systemic inflammation

Immunity. 2013 Apr 18;38(4):669-80. doi: 10.1016/j.immuni.2013.01.011. Epub 2013 Apr 11.

Abstract

Accumulation of T follicular helper (Tfh) cells and proinflammatory cytokines drive autoantibody-mediated diseases. The RNA-binding protein Roquin-1 (Rc3h1) represses the inducible costimulator ICOS and interferon-γ (IFN-γ) in T cells to prevent Tfh cell accumulation. Unlike Rc3h1(san) mice with a mutation in the ROQ domain of Roquin-1, mice lacking the protein, paradoxically do not display increased Tfh cells. Here we have analyzed mice with mutations that eliminate the RING domain from Roquin-1 or its paralog, Roquin-2 (Rc3h2). RING or ROQ mutations both disrupted Icos mRNA regulation by Roquin-1, but, unlike the ROQ mutant that still occupied mRNA-regulating stress granules, RING-deficient Roquin-1 failed to localize to stress granules and allowed Roquin-2 to compensate in the repression of ICOS and Tfh cells. These paralogs also targeted tumor necrosis factor (TNF) in nonlymphoid cells, ameliorating autoantibody-induced arthritis. The Roquin family emerges as a posttranscriptional brake in the adaptive and innate phases of antibody responses.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptive Immunity / genetics
  • Animals
  • Antibody Formation / genetics
  • Cell Line
  • Immunity, Innate / genetics
  • Inducible T-Cell Co-Stimulator Protein / metabolism*
  • Mice
  • Mice, Mutant Strains
  • Mutation / genetics
  • RING Finger Domains / genetics
  • RNA, Messenger / metabolism*
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • T-Lymphocytes, Helper-Inducer / immunology*
  • Tumor Necrosis Factor-alpha / immunology*
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism*

Substances

  • Icos protein, mouse
  • Inducible T-Cell Co-Stimulator Protein
  • RNA, Messenger
  • Repressor Proteins
  • Tumor Necrosis Factor-alpha
  • roquin-2 protein, mouse
  • Rc3h1 protein, mouse
  • Ubiquitin-Protein Ligases