Small-molecule inhibitors of ubiquitin-specific protease 7 enhance type-I interferon antiviral efficacy by destabilizing SOCS1

Immunology. 2020 Mar;159(3):309-321. doi: 10.1111/imm.13147. Epub 2019 Dec 5.

Abstract

Type-I interferons (IFN-I) are used as common antiviral drugs for a range of viral diseases in clinic. However, the antiviral efficacy of IFN-I is largely restricted by negative regulators of IFN-I signaling in cells. Therefore, identification of intracellular inhibitors of IFN-I signaling is important for developing novel targets to improve IFN-I antiviral therapy. In this study, we report that the deubiquitinase ubiquitin-specific protease 7 (USP7) negatively regulates IFN-I-mediated antiviral activity. USP7 physically interacts with suppressor of cytokine signaling 1 (SOCS1) and enhances SOCS1 protein stability by deubiquitination effects, which in turn restricts IFN-I-induced activation of Janus kinase-signal transducer and activator of transcription 1 signaling. Interestingly, viral infection up-regulates USP7 and therefore facilitates viral immune evasion. Importantly, the USP7 small-molecule inhibitors P5091 and P22077 inhibit SOCS1 expression and enhance IFN-I antiviral efficacy. Our findings identify a novel regulator of IFN-I antiviral activity and reveal that USP7 inhibitors could be potential enhancement agents for improving IFN-I antiviral therapy.

Keywords: antiviral activity; interferon; small-molecule inhibitor; suppressor of cytokine signaling 1; ubiquitin-specific protease 7.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • A549 Cells
  • Antiviral Agents / pharmacology*
  • Enzyme Inhibitors / pharmacology*
  • HEK293 Cells
  • HeLa Cells
  • Host-Pathogen Interactions
  • Humans
  • Influenza A Virus, H1N1 Subtype / drug effects*
  • Influenza A Virus, H1N1 Subtype / immunology
  • Influenza A Virus, H1N1 Subtype / pathogenicity
  • Interferon-alpha / pharmacology*
  • Janus Kinases / metabolism
  • Protein Binding
  • Protein Stability
  • Proteolysis
  • Signal Transduction
  • Suppressor of Cytokine Signaling 1 Protein / genetics
  • Suppressor of Cytokine Signaling 1 Protein / metabolism*
  • Thiophenes / pharmacology*
  • Time Factors
  • Ubiquitin-Specific Peptidase 7 / antagonists & inhibitors*
  • Ubiquitin-Specific Peptidase 7 / metabolism
  • Ubiquitination
  • Vesiculovirus / drug effects*
  • Vesiculovirus / immunology
  • Vesiculovirus / pathogenicity

Substances

  • 1-(5-((2,4-difluorophenyl)thio)-4-nitrothiophen-2-yl)ethanone
  • Antiviral Agents
  • Enzyme Inhibitors
  • Interferon-alpha
  • P5091
  • SOCS1 protein, human
  • Suppressor of Cytokine Signaling 1 Protein
  • Thiophenes
  • Janus Kinases
  • USP7 protein, human
  • Ubiquitin-Specific Peptidase 7