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PreprintCited by 10SARS-CoV-2 and COVID-19 ResearchAnimal Virus Infections StudiesZoonotic diseases and public health

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Distinct pathway for evolution of enhanced receptor binding and cell entry in SARS-like bat coronaviruses

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Tse, Alexandra L., Acreman, Cory M., Ricardo-Lax, Inna, Berrigan, Jacob, Lasso, Gorka, Balogun, Toheeb, Kearns, Fiona L., Casalino, Lorenzo, McClain, Georgia L., Chandran, Amartya Mudry, Lemeunier, Charlotte, Amaro, Rommie E., Rice, Charles M., Jangra, Rohit K., McLellan, Jason S., Chandran, Kartik, Miller, Emily Happy·2024·PLoS Pathogens
DOI 10.1101/2024.06.24.600393PMC PMC11602109

Preprint — published as 10.1371/journal.ppat.1012704

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Abstract

Understanding the zoonotic risks posed by bat coronaviruses (CoVs) is critical for pandemic preparedness. Herein, we generated recombinant vesicular stomatitis viruses (rVSVs) bearing spikes from divergent bat CoVs to investigate their cell entry mechanisms. Unexpectedly, the successful recovery of rVSVs bearing the spike from SHC014, a SARS-like bat CoV, was associated with the acquisition of a novel substitution in the S2 fusion peptide-proximal region (FPPR). This substitution enhanced viral entry in both VSV and coronavirus contexts by increasing the availability of the spike receptor-binding domain to recognize its cellular receptor, ACE2. A second substitution in the spike N–terminal domain, uncovered through forward-genetic selection, interacted epistatically with the FPPR substitution to synergistically enhance spike:ACE2 interaction and viral entry. Our findings identify genetic pathways for adaptation by bat CoVs during spillover and host-to-host transmission, fitness trade-offs inherent to these pathways, and potential Achilles’ heels that could be targeted with countermeasures.

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Metadata

Authors
Tse, A. L., Acreman, C. M., Ricardo-Lax, I., Berrigan, J., Lasso, G., Balogun, T., Kearns, F. L., Casalino, L., McClain, G. L., Chandran, A. M., Lemeunier, C., Amaro, R. E., Rice, C. M., Jangra, R. K., McLellan, J. S., Chandran, K., & Miller, E. H.
Affiliations
  • Albert Einstein College of Medicine (US)
  • The University of Texas at Austin (US)
  • Rockefeller University (US)
  • University of California San Diego (US)
Corresponding author
Chandran, Kartik
ORCID
Venue
PLoS Pathogens
Publisher
openRxiv
Published
2024-06-27
Volume
20
Issue
11
Pages
e1012704-e1012704
ISSN
1553-7366 (ISSN-L)
DOI
10.1101/2024.06.24.600393
PMC
PMC11602109
OpenAlex
W4404432015
Cited by
10
References
1
Citations by year
2026: 4 · 2025: 4 · 2024: 2
FWCI
3.44
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • PLoS Pathogens (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by)
  • PubMed Central (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • Bill and Melinda Gates Foundation (INV-031624)
  • Welch Foundation (F-0003-19620604)
  • G. Harold and Leila Y. Mathers Charitable Foundation
  • Meyer Foundation
  • Shurl and Kay Curci Foundation
  • Thermo Fisher Scientific
  • Fast Grants
  • Department of Biotechnology, Ministry of Science and Technology, India
  • A.G. Leventis Foundation
  • National Institutes of Health (1k08ai180364-01a1, K12TR004411)
  • National Institute of General Medical Sciences (P20GM134974, T32GM149364)
  • National Institute of Allergy and Infectious Diseases (P01AI165075, K08 AI180364, R01AI132633, T32AI070117, R21AI156482)
  • National Center for Advancing Translational Sciences
Topics
  • Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
  • Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Zoonotic diseases and public health
Keywords
bat coronaviruses, SARS-like coronaviruses, vesicular stomatitis virus, viral entry, spike protein, receptor binding domain, ACE2, zoonotic transmission, host adaptation, fitness trade-offs, pandemic preparedness

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