Human intracellular ISG15 prevents interferon-α/β over-amplification and auto-inflammation

Nature. 2015 Jan 1;517(7532):89-93. doi: 10.1038/nature13801. Epub 2014 Oct 12.

Abstract

Intracellular ISG15 is an interferon (IFN)-α/β-inducible ubiquitin-like modifier which can covalently bind other proteins in a process called ISGylation; it is an effector of IFN-α/β-dependent antiviral immunity in mice. We previously published a study describing humans with inherited ISG15 deficiency but without unusually severe viral diseases. We showed that these patients were prone to mycobacterial disease and that human ISG15 was non-redundant as an extracellular IFN-γ-inducing molecule. We show here that ISG15-deficient patients also display unanticipated cellular, immunological and clinical signs of enhanced IFN-α/β immunity, reminiscent of the Mendelian autoinflammatory interferonopathies Aicardi-Goutières syndrome and spondyloenchondrodysplasia. We further show that an absence of intracellular ISG15 in the patients' cells prevents the accumulation of USP18, a potent negative regulator of IFN-α/β signalling, resulting in the enhancement and amplification of IFN-α/β responses. Human ISG15, therefore, is not only redundant for antiviral immunity, but is a key negative regulator of IFN-α/β immunity. In humans, intracellular ISG15 is IFN-α/β-inducible not to serve as a substrate for ISGylation-dependent antiviral immunity, but to ensure USP18-dependent regulation of IFN-α/β and prevention of IFN-α/β-dependent autoinflammation.

Publication types

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

MeSH terms

  • Adolescent
  • Alleles
  • Child
  • Cytokines / deficiency
  • Cytokines / genetics
  • Cytokines / metabolism*
  • Endopeptidases / chemistry
  • Endopeptidases / metabolism
  • Female
  • Gene Expression Regulation
  • Humans
  • Inflammation / genetics
  • Inflammation / immunology
  • Inflammation / prevention & control*
  • Interferon Type I / immunology*
  • Interferon Type I / metabolism
  • Intracellular Space / metabolism*
  • Male
  • Pedigree
  • S-Phase Kinase-Associated Proteins / metabolism
  • Signal Transduction
  • Ubiquitin Thiolesterase
  • Ubiquitination
  • Ubiquitins / deficiency
  • Ubiquitins / genetics
  • Ubiquitins / metabolism*
  • Viruses / immunology

Substances

  • Cytokines
  • Interferon Type I
  • S-Phase Kinase-Associated Proteins
  • Ubiquitins
  • ISG15 protein, human
  • Endopeptidases
  • USP18 protein, human
  • Ubiquitin Thiolesterase

Associated data

  • BioProject/PRJNA167660
  • GEO/GSE60359