ACE2-independent sarbecovirus cell entry can be supported by TMPRSS2-related enzymes and can reduce sensitivity to antibody-mediated neutralization

PLoS Pathog. 2024 Nov 13;20(11):e1012653. doi: 10.1371/journal.ppat.1012653. eCollection 2024 Nov.

Abstract

The COVID-19 pandemic, caused by SARS-CoV-2, demonstrated that zoonotic transmission of animal sarbecoviruses threatens human health but the determinants of transmission are incompletely understood. Here, we show that most spike (S) proteins of horseshoe bat and Malayan pangolin sarbecoviruses employ ACE2 for entry, with human and raccoon dog ACE2 exhibiting broad receptor activity. The insertion of a multibasic cleavage site into the S proteins increased entry into human lung cells driven by most S proteins tested, suggesting that acquisition of a multibasic cleavage site might increase infectivity of diverse animal sarbecoviruses for the human respiratory tract. In contrast, two bat sarbecovirus S proteins drove cell entry in an ACE2-independent, trypsin-dependent fashion and several ACE2-dependent S proteins could switch to the ACE2-independent entry pathway when exposed to trypsin. Several TMPRSS2-related cellular proteases but not the insertion of a multibasic cleavage site into the S protein allowed for ACE2-independent entry in the absence of trypsin and may support viral spread in the respiratory tract. Finally, the pan-sarbecovirus antibody S2H97 enhanced cell entry driven by two S proteins and this effect was reversed by trypsin while trypsin protected entry driven by a third S protein from neutralization by S2H97. Similarly, plasma from quadruple vaccinated individuals neutralized entry driven by all S proteins studied, and availability of the ACE2-independent, trypsin-dependent pathway reduced neutralization sensitivity. In sum, our study reports a pathway for entry into human cells that is ACE2-independent, can be supported by TMPRSS2-related proteases and may be associated with antibody evasion.

MeSH terms

  • Angiotensin-Converting Enzyme 2* / immunology
  • Angiotensin-Converting Enzyme 2* / metabolism
  • Animals
  • Antibodies, Neutralizing* / immunology
  • Antibodies, Viral / immunology
  • COVID-19* / immunology
  • COVID-19* / virology
  • Chiroptera / immunology
  • Chiroptera / virology
  • Humans
  • SARS-CoV-2* / immunology
  • SARS-CoV-2* / physiology
  • Serine Endopeptidases* / immunology
  • Serine Endopeptidases* / metabolism
  • Spike Glycoprotein, Coronavirus* / immunology
  • Spike Glycoprotein, Coronavirus* / metabolism
  • Virus Internalization*

Substances

  • Angiotensin-Converting Enzyme 2
  • Serine Endopeptidases
  • Spike Glycoprotein, Coronavirus
  • TMPRSS2 protein, human
  • Antibodies, Neutralizing
  • ACE2 protein, human
  • spike protein, SARS-CoV-2
  • Antibodies, Viral

Grants and funding

This work was supported by the European Union project UNDINE (101057100 to SP), the EU Hera project DURABLE (101102733 to CD), the COVID-19-Research Network Lower Saxony (COFONI) through funding from the Ministry of Science and Culture of Lower Saxony in Germany (14-76103-184, projects 7FF22, 6FF22, and 10FF22 to SP; project 4LZF23 to GMNB), the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG; PO 716/11-1 to SP), the German Center for Infection Research (grant no 80018019238 to GMNB), the European Regional Development Funds Defeat Corona (ZW7-8515131 to GMNB) and Getting AIR (ZW7-85151373 to GMNB), the China Scholarship Council (202006270031 to LZ), the German Federal Ministry of Education and Research (Bundesministerium für Bildung und Forschung; 01KI2043 and NaFoUniMedCovid19-COVIM: 01KX2021 to H-MJ; project DZIF [8040701710 and 8064701703] to CD), the Bavarian State Ministry for Science and the Arts and DFG (through the research training groups RTG1660 and TRR130 to H-MJ), the Bayerische Forschungsstiftung (Project CORAd to H-MJ), and the Kastner Foundation (to H-MJ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.