Spike substitutions E484D, P812R and Q954H mediate ACE2-independent entry of SARS-CoV-2 across different cell lines.

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which causes coronavirus disease 2019 (COVID-19), has evolved into variants with multiple spike protein coding mutations that affect its transmissibility, infectivity, and immune evasion, in particular from neutralizing antibodies. Severa...

Full description

Saved in:
Bibliographic Details
Main Authors: Greta Vizgirda, Alexander P Underwood, Ulrik Fahnøe, Nina Weis, Santseharay Ramirez, Jens Bukh
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0326419
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849396750704443392
author Greta Vizgirda
Alexander P Underwood
Ulrik Fahnøe
Nina Weis
Santseharay Ramirez
Jens Bukh
author_facet Greta Vizgirda
Alexander P Underwood
Ulrik Fahnøe
Nina Weis
Santseharay Ramirez
Jens Bukh
author_sort Greta Vizgirda
collection DOAJ
description Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which causes coronavirus disease 2019 (COVID-19), has evolved into variants with multiple spike protein coding mutations that affect its transmissibility, infectivity, and immune evasion, in particular from neutralizing antibodies. Several of these amino acid changes have been associated with reduced dependency on the principal angiotensin converting enzyme-2 (ACE2) receptor for cell entry. The present study investigates the role of spike protein changes observed in a cell-culture adapted SARS-CoV-2 isolate (DK-AHH1) in modulating entry, ACE2 dependency, and neutralization across different cells, including human liver and lung cell lines. Using a pseudoparticle system, spike proteins with substitutions E484D, P812R, Q954H, and deletion Δ68-76 were evaluated in Vero E6 and Huh7.5, as well as in A549 cells with and without ACE2 overexpression. Pseudoparticles carrying E484D or P812R individually permitted entry in Huh7.5 cells, and their combination further enhanced this capacity. ACE2 blocking experiments revealed the differential roles of these mutations in mediating entry across cell lines. In Vero E6 cells, P812R was the primary driver for ACE2-independent entry, while E484D facilitated ACE2-independent entry in Huh7.5 cells. In A549 cells, all three substitutions (E484D+P812R + Q954H) were required for ACE2-independent entry. Addition of the Δ68-76 deletion did not increase infectivity in any cell line. Notably, pseudoparticles carrying these mutations, maintained susceptibility to neutralization by convalescent plasma from subjects with COVID-19, regardless of the cell line used. These findings highlight the adaptability of SARS-CoV-2 in utilizing alternative entry mechanisms across various cell types, with E484D and P812R playing critical roles in ACE2-independent entry in cell culture. Overall, this study provides valuable insights into how SARS-CoV-2 can alter its receptor usage to ensure robust infectivity of human cell lines while preserving neutralization sensitivity, contributing to our understanding of viral evolution, and informing potential therapeutic strategies targeting viral entry.
format Article
id doaj-art-ea19d1a2d9f94314b6d52b8a89043bd0
institution Kabale University
issn 1932-6203
language English
publishDate 2025-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-ea19d1a2d9f94314b6d52b8a89043bd02025-08-20T03:39:14ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01208e032641910.1371/journal.pone.0326419Spike substitutions E484D, P812R and Q954H mediate ACE2-independent entry of SARS-CoV-2 across different cell lines.Greta VizgirdaAlexander P UnderwoodUlrik FahnøeNina WeisSantseharay RamirezJens BukhSevere acute respiratory syndrome coronavirus 2 (SARS-CoV-2), which causes coronavirus disease 2019 (COVID-19), has evolved into variants with multiple spike protein coding mutations that affect its transmissibility, infectivity, and immune evasion, in particular from neutralizing antibodies. Several of these amino acid changes have been associated with reduced dependency on the principal angiotensin converting enzyme-2 (ACE2) receptor for cell entry. The present study investigates the role of spike protein changes observed in a cell-culture adapted SARS-CoV-2 isolate (DK-AHH1) in modulating entry, ACE2 dependency, and neutralization across different cells, including human liver and lung cell lines. Using a pseudoparticle system, spike proteins with substitutions E484D, P812R, Q954H, and deletion Δ68-76 were evaluated in Vero E6 and Huh7.5, as well as in A549 cells with and without ACE2 overexpression. Pseudoparticles carrying E484D or P812R individually permitted entry in Huh7.5 cells, and their combination further enhanced this capacity. ACE2 blocking experiments revealed the differential roles of these mutations in mediating entry across cell lines. In Vero E6 cells, P812R was the primary driver for ACE2-independent entry, while E484D facilitated ACE2-independent entry in Huh7.5 cells. In A549 cells, all three substitutions (E484D+P812R + Q954H) were required for ACE2-independent entry. Addition of the Δ68-76 deletion did not increase infectivity in any cell line. Notably, pseudoparticles carrying these mutations, maintained susceptibility to neutralization by convalescent plasma from subjects with COVID-19, regardless of the cell line used. These findings highlight the adaptability of SARS-CoV-2 in utilizing alternative entry mechanisms across various cell types, with E484D and P812R playing critical roles in ACE2-independent entry in cell culture. Overall, this study provides valuable insights into how SARS-CoV-2 can alter its receptor usage to ensure robust infectivity of human cell lines while preserving neutralization sensitivity, contributing to our understanding of viral evolution, and informing potential therapeutic strategies targeting viral entry.https://doi.org/10.1371/journal.pone.0326419
spellingShingle Greta Vizgirda
Alexander P Underwood
Ulrik Fahnøe
Nina Weis
Santseharay Ramirez
Jens Bukh
Spike substitutions E484D, P812R and Q954H mediate ACE2-independent entry of SARS-CoV-2 across different cell lines.
PLoS ONE
title Spike substitutions E484D, P812R and Q954H mediate ACE2-independent entry of SARS-CoV-2 across different cell lines.
title_full Spike substitutions E484D, P812R and Q954H mediate ACE2-independent entry of SARS-CoV-2 across different cell lines.
title_fullStr Spike substitutions E484D, P812R and Q954H mediate ACE2-independent entry of SARS-CoV-2 across different cell lines.
title_full_unstemmed Spike substitutions E484D, P812R and Q954H mediate ACE2-independent entry of SARS-CoV-2 across different cell lines.
title_short Spike substitutions E484D, P812R and Q954H mediate ACE2-independent entry of SARS-CoV-2 across different cell lines.
title_sort spike substitutions e484d p812r and q954h mediate ace2 independent entry of sars cov 2 across different cell lines
url https://doi.org/10.1371/journal.pone.0326419
work_keys_str_mv AT gretavizgirda spikesubstitutionse484dp812randq954hmediateace2independententryofsarscov2acrossdifferentcelllines
AT alexanderpunderwood spikesubstitutionse484dp812randq954hmediateace2independententryofsarscov2acrossdifferentcelllines
AT ulrikfahnøe spikesubstitutionse484dp812randq954hmediateace2independententryofsarscov2acrossdifferentcelllines
AT ninaweis spikesubstitutionse484dp812randq954hmediateace2independententryofsarscov2acrossdifferentcelllines
AT santseharayramirez spikesubstitutionse484dp812randq954hmediateace2independententryofsarscov2acrossdifferentcelllines
AT jensbukh spikesubstitutionse484dp812randq954hmediateace2independententryofsarscov2acrossdifferentcelllines