Enterovirus 71 protease 2Apro targets MAVS to inhibit anti-viral type I interferon responses

PLoS Pathog. 2013 Mar;9(3):e1003231. doi: 10.1371/journal.ppat.1003231. Epub 2013 Mar 21.

Abstract

Enterovirus 71 (EV71) is the major causative pathogen of hand, foot, and mouth disease (HFMD). Its pathogenicity is not fully understood, but innate immune evasion is likely a key factor. Strategies to circumvent the initiation and effector phases of anti-viral innate immunity are well known; less well known is whether EV71 evades the signal transduction phase regulated by a sophisticated interplay of cellular and viral proteins. Here, we show that EV71 inhibits anti-viral type I interferon (IFN) responses by targeting the mitochondrial anti-viral signaling (MAVS) protein--a unique adaptor molecule activated upon retinoic acid induced gene-I (RIG-I) and melanoma differentiation associated gene (MDA-5) viral recognition receptor signaling--upstream of type I interferon production. MAVS was cleaved and released from mitochondria during EV71 infection. An in vitro cleavage assay demonstrated that the viral 2A protease (2A(pro)), but not the mutant 2A(pro) (2A(pro)-110) containing an inactivated catalytic site, cleaved MAVS. The Protease-Glo assay revealed that MAVS was cleaved at 3 residues between the proline-rich and transmembrane domains, and the resulting fragmentation effectively inactivated downstream signaling. In addition to MAVS cleavage, we found that EV71 infection also induced morphologic and functional changes to the mitochondria. The EV71 structural protein VP1 was detected on purified mitochondria, suggesting not only a novel role for mitochondria in the EV71 replication cycle but also an explanation of how EV71-derived 2A(pro) could approach MAVS. Taken together, our findings reveal a novel strategy employed by EV71 to escape host anti-viral innate immunity that complements the known EV71-mediated immune-evasion mechanisms.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / immunology
  • Adaptor Proteins, Signal Transducing / metabolism*
  • Antiviral Agents / pharmacology*
  • Cysteine Endopeptidases / metabolism*
  • Enterovirus A, Human / drug effects
  • Enterovirus A, Human / enzymology*
  • Female
  • HeLa Cells
  • Humans
  • Interferon Type I / pharmacology*
  • Mitochondria / metabolism
  • Mitochondrial Membranes / metabolism
  • Protease Inhibitors / pharmacology
  • RNA Virus Infections
  • Rhabdomyosarcoma
  • Signal Transduction

Substances

  • Adaptor Proteins, Signal Transducing
  • Antiviral Agents
  • Interferon Type I
  • Protease Inhibitors
  • Cysteine Endopeptidases

Grants and funding

This work was supported by grants from the National Basic Research Program of China (973 Project, 2011CB504903), Eleven-fifth Mega-Scientific project on “prevention and treatment of AIDS, viral hepatitis and other infectious diseases” (2009ZX10004-303), the National Natural Science Foundation of China (NSFC 31270200, http://www.nsfc.gov.cn), and the China Outstanding Young Scientist Foundation (81225014 http://www.nsfc.gov.cn). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.