NS5A Promotes Constitutive Degradation of IP3R3 to Counteract Apoptosis Induced by Hepatitis C Virus

Cell Rep. 2018 Oct 23;25(4):833-840.e3. doi: 10.1016/j.celrep.2018.09.088.

Abstract

FBXL2 targets IP3R3 for ubiquitin-mediated degradation to limit Ca2+ flux to mitochondria and, consequently, apoptosis. Efficient replication of hepatitis C virus (HCV) requires geranylgeranylation of FBXL2. Here, we show that the viral protein NS5A forms a trimeric complex with IP3R3 and FBXL2, unmasking IP3R3's degron in the absence of inositol 1,4,5-trisphosphate (IP3) stimulation. FBXL2 knockdown or expression of a stable IP3R3 mutant causes persistent Ca2+ flux and sensitizes cells to apoptosis, resulting in the inhibition of viral replication. Importantly, the effect of FBXL2 silencing is rescued by depleting IP3R3, but not p85β, another established FBXL2 substrate, indicating that the anti-HCV effect of FBXL2 knockdown is largely due to IP3R3 stabilization. Finally, disruption of the FBXL2-NS5A-IP3R3 complex using somatic cell genetics or pharmacologic inhibition results in IP3R3 stabilization and suppression of HCV replication. This study reveals an IP3-independent molecular mechanism through which HCV promotes IP3R3 degradation, thereby inhibiting virus-induced apoptosis and establishing chronic infection.

Keywords: FBXL2; HCV-NS5A; IP3R3; apoptosis; calcium overload; hepatitis C virus; proteasomal degradation; ubiquitin; ubiquitin ligase.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis* / drug effects
  • Carbamates
  • Cell Line
  • F-Box Proteins / metabolism
  • Hepacivirus / drug effects
  • Hepacivirus / physiology*
  • Hepatitis C / metabolism
  • Hepatitis C / pathology
  • Hepatitis C / virology
  • Humans
  • Imidazoles / pharmacology
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism*
  • Leucine / analogs & derivatives
  • Leucine / pharmacology
  • Protein Multimerization / drug effects
  • Proteolysis* / drug effects
  • Pyrrolidines
  • Valine / analogs & derivatives
  • Viral Nonstructural Proteins / metabolism*
  • Virus Replication / drug effects

Substances

  • Carbamates
  • F-Box Proteins
  • FBXL2 protein, human
  • GGTI 286
  • Imidazoles
  • Inositol 1,4,5-Trisphosphate Receptors
  • Pyrrolidines
  • Viral Nonstructural Proteins
  • NS-5 protein, hepatitis C virus
  • Leucine
  • Valine
  • daclatasvir