SARS-CoV-2 Omicron variations reveal mechanisms controlling cell entry dynamics and antibody neutralization.

Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) is adapting to continuous presence in humans. Transitions to endemic infection patterns are associated with changes in the spike (S) proteins that direct virus-cell entry. These changes generate antigenic drift and thereby allow virus main...

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Main Authors: Enya Qing, Julisa Salgado, Alexandria Wilcox, Tom Gallagher
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2024-12-01
Series:PLoS Pathogens
Online Access:https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1012757&type=printable
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author Enya Qing
Julisa Salgado
Alexandria Wilcox
Tom Gallagher
author_facet Enya Qing
Julisa Salgado
Alexandria Wilcox
Tom Gallagher
author_sort Enya Qing
collection DOAJ
description Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) is adapting to continuous presence in humans. Transitions to endemic infection patterns are associated with changes in the spike (S) proteins that direct virus-cell entry. These changes generate antigenic drift and thereby allow virus maintenance in the face of prevalent human antiviral antibodies. These changes also fine tune virus-cell entry dynamics in ways that optimize transmission and infection into human cells. Focusing on the latter aspect, we evaluated the effects of several S protein substitutions on virus-cell membrane fusion, an essential final step in enveloped virus-cell entry. Membrane fusion is executed by integral-membrane "S2" domains, yet we found that substitutions in peripheral "S1" domains altered late-stage fusion dynamics, consistent with S1-S2 heterodimers cooperating throughout cell entry. A specific H655Y change in S1 stabilized a fusion-intermediate S protein conformation and thereby delayed membrane fusion. The H655Y change also sensitized viruses to neutralization by S2-targeting fusion-inhibitory peptides and stem-helix antibodies. The antibodies did not interfere with early fusion-activating steps; rather they targeted the latest stages of S2-directed membrane fusion in a novel neutralization mechanism. These findings demonstrate that single amino acid substitutions in the S proteins both reset viral entry-fusion kinetics and increase sensitivity to antibody neutralization. The results exemplify how selective forces driving SARS-CoV-2 fitness and antibody evasion operate together to shape SARS-CoV-2 evolution.
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spelling doaj-art-fb8b725c177c4bbbb8023aa315d6dfba2025-08-20T02:49:01ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742024-12-012012e101275710.1371/journal.ppat.1012757SARS-CoV-2 Omicron variations reveal mechanisms controlling cell entry dynamics and antibody neutralization.Enya QingJulisa SalgadoAlexandria WilcoxTom GallagherSevere Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) is adapting to continuous presence in humans. Transitions to endemic infection patterns are associated with changes in the spike (S) proteins that direct virus-cell entry. These changes generate antigenic drift and thereby allow virus maintenance in the face of prevalent human antiviral antibodies. These changes also fine tune virus-cell entry dynamics in ways that optimize transmission and infection into human cells. Focusing on the latter aspect, we evaluated the effects of several S protein substitutions on virus-cell membrane fusion, an essential final step in enveloped virus-cell entry. Membrane fusion is executed by integral-membrane "S2" domains, yet we found that substitutions in peripheral "S1" domains altered late-stage fusion dynamics, consistent with S1-S2 heterodimers cooperating throughout cell entry. A specific H655Y change in S1 stabilized a fusion-intermediate S protein conformation and thereby delayed membrane fusion. The H655Y change also sensitized viruses to neutralization by S2-targeting fusion-inhibitory peptides and stem-helix antibodies. The antibodies did not interfere with early fusion-activating steps; rather they targeted the latest stages of S2-directed membrane fusion in a novel neutralization mechanism. These findings demonstrate that single amino acid substitutions in the S proteins both reset viral entry-fusion kinetics and increase sensitivity to antibody neutralization. The results exemplify how selective forces driving SARS-CoV-2 fitness and antibody evasion operate together to shape SARS-CoV-2 evolution.https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1012757&type=printable
spellingShingle Enya Qing
Julisa Salgado
Alexandria Wilcox
Tom Gallagher
SARS-CoV-2 Omicron variations reveal mechanisms controlling cell entry dynamics and antibody neutralization.
PLoS Pathogens
title SARS-CoV-2 Omicron variations reveal mechanisms controlling cell entry dynamics and antibody neutralization.
title_full SARS-CoV-2 Omicron variations reveal mechanisms controlling cell entry dynamics and antibody neutralization.
title_fullStr SARS-CoV-2 Omicron variations reveal mechanisms controlling cell entry dynamics and antibody neutralization.
title_full_unstemmed SARS-CoV-2 Omicron variations reveal mechanisms controlling cell entry dynamics and antibody neutralization.
title_short SARS-CoV-2 Omicron variations reveal mechanisms controlling cell entry dynamics and antibody neutralization.
title_sort sars cov 2 omicron variations reveal mechanisms controlling cell entry dynamics and antibody neutralization
url https://journals.plos.org/plospathogens/article/file?id=10.1371/journal.ppat.1012757&type=printable
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AT alexandriawilcox sarscov2omicronvariationsrevealmechanismscontrollingcellentrydynamicsandantibodyneutralization
AT tomgallagher sarscov2omicronvariationsrevealmechanismscontrollingcellentrydynamicsandantibodyneutralization