The differential regulation of human ACT1 isoforms by Hsp90 in IL-17 signaling

J Immunol. 2014 Aug 15;193(4):1590-9. doi: 10.4049/jimmunol.1400715. Epub 2014 Jul 14.

Abstract

IL-17 is a proinflammatory cytokine implicated in the pathogenesis of autoimmune diseases including psoriasis. ACT1 is an essential adaptor molecule in the IL-17 signaling pathway. A missense single nucleotide polymorphism (rs33980500; SNP-D10N) that resulted in the substitution of an asparagine for an aspartic acid at position 10 of ACT1 (ACT1-D10N) is associated with psoriasis susceptibility. Due to alternative splicing in humans, SNP-D10N encodes two mutated ACT1 proteins, ACT1-D10N and ACT1-D19N. Although both ACT1 isoforms are Hsp90 client proteins, the nine additional amino acids in ACT1-D19N provide an additional Hsp90 binding site that is absent in ACT1-D10N. Therefore, whereas ACT1-D10N is a dead protein that is unable to transduce IL-17 signals for gene expression, ACT1-D19N is fully responsive to IL-17. Intriguingly, the two ACT1 isoforms are differentially expressed in ACT1(D10N/D10N) fibroblasts and T cells. Fibroblasts express both isoforms equally, enabling ACT1-D19N to compensate for the loss of ACT1-D10N function. ACT1(D10N/D10N) T cells, however, express predominantly ACT1-D10N. Lacking this compensatory mechanism, ACT1(D10N/D10N) T cells behave like ACT1-deficient T cells, exhibiting a dysregulated and hyperactive Th17 phenotype with overproduction of IL-22 and IL-17. The hyperactive Th17 response combined with fully responsive fibroblasts likely synergized to contribute to psoriasis susceptibility in SNP-D10N patients.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Alternative Splicing / genetics
  • Base Sequence
  • Binding Sites
  • Genetic Predisposition to Disease
  • HEK293 Cells
  • HSP90 Heat-Shock Proteins / immunology*
  • HeLa Cells
  • Humans
  • Interleukin-17 / biosynthesis
  • Interleukin-17 / immunology*
  • Interleukin-22
  • Interleukins / biosynthesis
  • Molecular Sequence Data
  • Mutation, Missense
  • Polymorphism, Single Nucleotide
  • Protein Isoforms / biosynthesis
  • Protein Isoforms / genetics
  • Psoriasis / immunology*
  • Psoriasis / pathology
  • RNA Interference
  • Signal Transduction / immunology*
  • Skin / immunology
  • Skin / pathology
  • Th17 Cells / immunology
  • Tumor Necrosis Factor Receptor-Associated Peptides and Proteins / biosynthesis
  • Tumor Necrosis Factor Receptor-Associated Peptides and Proteins / genetics*

Substances

  • Adaptor Proteins, Signal Transducing
  • HSP90 Heat-Shock Proteins
  • Interleukin-17
  • Interleukins
  • Protein Isoforms
  • TRAF3IP2 protein, human
  • Tumor Necrosis Factor Receptor-Associated Peptides and Proteins