Human ISG15 conjugation targets both IFN-induced and constitutively expressed proteins functioning in diverse cellular pathways

Proc Natl Acad Sci U S A. 2005 Jul 19;102(29):10200-5. doi: 10.1073/pnas.0504754102. Epub 2005 Jul 11.

Abstract

IFN-alpha/beta plays an essential role in innate immunity against viral and bacterial infection. Among the proteins induced by IFN-alpha/beta are the ubiquitin-like ISG15 protein and its E1- (Ube1L) and E2- (UbcH8) conjugating enzymes, leading to the conjugation of ISG15 to cellular proteins. It is likely that ISG15 conjugation plays an important role in antiviral response because a human virus, influenza B virus, inhibits ISG15 conjugation. However, the biological function of ISG15 modification remains unknown, largely because only a few human ISG15 target proteins have been identified. Here we purify ISG15-modified proteins from IFN-beta-treated human (HeLa) cells by using double-affinity selection and use mass spectroscopy to identify a large number (158) of ISG15 target proteins. Eight of these proteins were subjected to further analysis and verified to be ISG15 modified in IFN-beta-treated cells, increasing the likelihood that most, if not all, targets identified by mass spectroscopy are bona fide ISG15 targets. Several of the targets are IFN-alpha/beta-induced antiviral proteins, including PKR, MxA, HuP56, and RIG-I, providing a rationale for the inhibition of ISG15 conjugation by influenza B virus. Most targets are constitutively expressed proteins that function in diverse cellular pathways, including RNA splicing, chromatin remodeling/polymerase II transcription, cytoskeleton organization and regulation, stress responses, and translation. These results indicate that ISG15 conjugation impacts nuclear as well as cytoplasmic functions. By targeting a wide array of constitutively expressed proteins, ISG15 conjugation greatly extends the repertoire of cellular functions that are affected by IFN-alpha/beta.

Publication types

  • Comparative Study
  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Antiviral Agents / metabolism*
  • Cytokines / metabolism*
  • DEAD Box Protein 58
  • DEAD-box RNA Helicases
  • GTP-Binding Proteins / metabolism
  • HeLa Cells
  • Humans
  • Immunity, Innate / physiology*
  • Influenza B virus / metabolism
  • Interferon Type I / metabolism*
  • Mass Spectrometry
  • Myxovirus Resistance Proteins
  • RNA Helicases / metabolism
  • Receptors, Immunologic
  • Ubiquitin-Activating Enzymes / metabolism
  • Ubiquitin-Conjugating Enzymes / metabolism
  • Ubiquitins / metabolism
  • eIF-2 Kinase / metabolism

Substances

  • Antiviral Agents
  • Cytokines
  • Interferon Type I
  • MX1 protein, human
  • Myxovirus Resistance Proteins
  • Receptors, Immunologic
  • UBA1 protein, human
  • Ubiquitins
  • ISG15 protein, human
  • UBE2L6 protein, human
  • Ubiquitin-Conjugating Enzymes
  • eIF-2 Kinase
  • RIGI protein, human
  • GTP-Binding Proteins
  • DEAD Box Protein 58
  • DEAD-box RNA Helicases
  • RNA Helicases
  • Ubiquitin-Activating Enzymes