Enteroviral Infection Inhibits Autophagic Flux via Disruption of the SNARE Complex to Enhance Viral Replication

Cell Rep. 2018 Mar 20;22(12):3292-3303. doi: 10.1016/j.celrep.2018.02.090.

Abstract

Picornaviruses have evolved to hijack host cellular machinery, including the autophagic pathway. However, the mechanisms remain largely unclear. We use coxsackievirus B3 (CVB3) as a model organism to explore the possible role of picornavirus subversion of the autophagic pathway in viral infection. Our in vivo and in vitro experiments demonstrate that CVB3 infection causes a significant, albeit incomplete, inhibition of autophagic flux by limiting the fusion of autophagosomes with lysosomes and/or late endosomes. Furthermore, we show that CVB3 specifically targets SNARE protein SNAP29 and adaptor protein PLEKHM1, two critical proteins known to regulate autophagosome fusion, for cleavage through the catalytic activity of viral proteinase 3C, ultimately impairing the formation of SNARE complexes. Finally, we demonstrate that loss of SNAP29/PLEKHM1 inhibits autophagic flux, resulting in increased viral replication. Collectively, our study reveals a mechanism that supports an emerging model whereby CVB3 hijacks the autophagic machinery to facilitate its own propagation.

Keywords: PLEKHM1; SNAP29; SNARE proteins; autophagic flux; coxsackievirus; endocytic pathway; picornavirus; syntaxin 17; viral proteinase 3C; viral replication.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autophagy / drug effects
  • Enterovirus / genetics
  • Enterovirus / physiology*
  • Enterovirus Infections / metabolism*
  • Enterovirus Infections / pathology
  • Enterovirus Infections / virology*
  • HeLa Cells
  • Humans
  • Macrolides / pharmacology
  • Qb-SNARE Proteins / metabolism
  • Qc-SNARE Proteins / metabolism
  • SNARE Proteins / metabolism*
  • Virus Replication*

Substances

  • Macrolides
  • Qb-SNARE Proteins
  • Qc-SNARE Proteins
  • SNAP29 protein, human
  • SNARE Proteins
  • bafilomycin A1