The matrix metalloproteinase ADAM10 supports hepatitis C virus entry and cell-to-cell spread via its sheddase activity

PLoS Pathog. 2023 Nov 15;19(11):e1011759. doi: 10.1371/journal.ppat.1011759. eCollection 2023 Nov.

Abstract

Hepatitis C virus (HCV) exploits the four entry factors CD81, scavenger receptor class B type I (SR-BI, also known as SCARB1), occludin, and claudin-1 as well as the co-factor epidermal growth factor receptor (EGFR) to infect human hepatocytes. Here, we report that the disintegrin and matrix metalloproteinase 10 (ADAM10) associates with CD81, SR-BI, and EGFR and acts as HCV host factor. Pharmacological inhibition, siRNA-mediated silencing and genetic ablation of ADAM10 reduced HCV infection. ADAM10 was dispensable for HCV replication but supported HCV entry and cell-to-cell spread. Substrates of the ADAM10 sheddase including epidermal growth factor (EGF) and E-cadherin, which activate EGFR family members, rescued HCV infection of ADAM10 knockout cells. ADAM10 did not influence infection with other enveloped RNA viruses such as alphaviruses and a common cold coronavirus. Collectively, our study reveals a critical role for the sheddase ADAM10 as a HCV host factor, contributing to EGFR family member transactivation and as a consequence to HCV uptake.

MeSH terms

  • ADAM10 Protein / genetics
  • ADAM10 Protein / metabolism
  • Amyloid Precursor Protein Secretases / genetics
  • Amyloid Precursor Protein Secretases / metabolism
  • Carrier Proteins
  • ErbB Receptors / metabolism
  • Hepacivirus* / physiology
  • Hepatitis C*
  • Humans
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Scavenger Receptors, Class B / genetics
  • Scavenger Receptors, Class B / metabolism
  • Tetraspanin 28 / genetics
  • Tetraspanin 28 / metabolism
  • Virus Internalization

Substances

  • Scavenger Receptors, Class B
  • Carrier Proteins
  • ErbB Receptors
  • Tetraspanin 28
  • ADAM10 protein, human
  • ADAM10 Protein
  • Membrane Proteins
  • Amyloid Precursor Protein Secretases

Grants and funding

This work was supported by grants to G.G. from the Deutsche Forschungsgemeinschaft (DFG, SFB900-C7, Project 158989968 and Project 452467953; Research Training Group 2485 VIPER; RESIST, EXC-2155, Project 390874280; Project 452467953 GE 2145/6-1), the Bundesministerium für Bildung und Forschung, the Niedersächsische Ministerium für Wissenschaft und Kultur (Professorinnen Programm III) and the Knut och Alice Wallenbergs Stiftelse. B.C.M. was funded by the Hannover Biomedical Research School. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.