A human immune dysregulation syndrome characterized by severe hyperinflammation with a homozygous nonsense Roquin-1 mutation

Nat Commun. 2019 Oct 21;10(1):4779. doi: 10.1038/s41467-019-12704-6.

Abstract

Hyperinflammatory syndromes are life-threatening disorders caused by overzealous immune cell activation and cytokine release, often resulting from defects in negative feedback mechanisms. In the quintessential hyperinflammatory syndrome familial hemophagocytic lymphohistiocytosis (HLH), inborn errors of cytotoxicity result in effector cell accumulation, immune dysregulation and, if untreated, tissue damage and death. Here, we describe a human case with a homozygous nonsense R688* RC3H1 mutation suffering from hyperinflammation, presenting as relapsing HLH. RC3H1 encodes Roquin-1, a posttranscriptional repressor of immune-regulatory proteins such as ICOS, OX40 and TNF. Comparing the R688* variant with the murine M199R variant reveals a phenotypic resemblance, both in immune cell activation, hypercytokinemia and disease development. Mechanistically, R688* Roquin-1 fails to localize to P-bodies and interact with the CCR4-NOT deadenylation complex, impeding mRNA decay and dysregulating cytokine production. The results from this unique case suggest that impaired Roquin-1 function provokes hyperinflammation by a failure to quench immune activation.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adolescent
  • Animals
  • Codon, Nonsense
  • Consanguinity
  • Cyclosporine / therapeutic use
  • Eosinophilia / genetics
  • Eosinophilia / immunology
  • Homozygote
  • Humans
  • Immunophenotyping
  • Immunosuppressive Agents / therapeutic use
  • Inducible T-Cell Co-Stimulator Protein / genetics
  • Inducible T-Cell Co-Stimulator Protein / immunology
  • Inducible T-Cell Co-Stimulator Protein / metabolism
  • Lymphohistiocytosis, Hemophagocytic / drug therapy
  • Lymphohistiocytosis, Hemophagocytic / genetics*
  • Lymphohistiocytosis, Hemophagocytic / immunology
  • Male
  • Mice
  • Monocytes / immunology
  • RNA-Binding Proteins / genetics*
  • Receptors, OX40 / genetics
  • Receptors, OX40 / immunology
  • Receptors, OX40 / metabolism
  • Recurrence
  • T-Lymphocytes / immunology
  • T-Lymphocytes, Regulatory / immunology
  • Ubiquitin-Protein Ligases / genetics*
  • Ubiquitin-Protein Ligases / immunology

Substances

  • Codon, Nonsense
  • Icos protein, mouse
  • Immunosuppressive Agents
  • Inducible T-Cell Co-Stimulator Protein
  • RC3H1 protein, human
  • RNA-Binding Proteins
  • Receptors, OX40
  • Tnfrsf4 protein, mouse
  • Cyclosporine
  • Rc3h1 protein, mouse
  • Ubiquitin-Protein Ligases