Herpes simplex virus 1 glycoprotein C promotes virus penetration from endosomes during entry, independent of interaction with heparan sulfate

Herpes simplex virus 1 (HSV-1) gC is a multi-functional glycoprotein present in the viral envelope and on the surface of infected cells. Virion gC, and to a lesser extent the fusion protein gB, interacts with host heparan sulfate to mediate HSV-1 attachment to the cell surface. Virion gC selectively...

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Main Authors: Seth M. Schneider, Giulia Tebaldi, Katrina A. Gianopulos, Darin J. Weed, Suzanne M. Pritchard, Chloe Leach, Anthony V. Nicola
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-04-01
Series:Frontiers in Microbiology
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Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2025.1549349/full
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author Seth M. Schneider
Seth M. Schneider
Giulia Tebaldi
Katrina A. Gianopulos
Katrina A. Gianopulos
Darin J. Weed
Suzanne M. Pritchard
Chloe Leach
Anthony V. Nicola
Anthony V. Nicola
author_facet Seth M. Schneider
Seth M. Schneider
Giulia Tebaldi
Katrina A. Gianopulos
Katrina A. Gianopulos
Darin J. Weed
Suzanne M. Pritchard
Chloe Leach
Anthony V. Nicola
Anthony V. Nicola
author_sort Seth M. Schneider
collection DOAJ
description Herpes simplex virus 1 (HSV-1) gC is a multi-functional glycoprotein present in the viral envelope and on the surface of infected cells. Virion gC, and to a lesser extent the fusion protein gB, interacts with host heparan sulfate to mediate HSV-1 attachment to the cell surface. Virion gC selectively facilitates HSV-1 entry into cells that support entry by a low pH-dependent endocytic pathway. gC regulates fusion-associated conformational changes in gB. Here we investigated the mechanism by which gC plays a post-attachment role in HSV-1 entry into cells. HSV-1 entered HS-deficient cells by a low pH-dependent route. Similarly, HSV-1 deleted for HS-binding domains entered HS-bearing cells by a low pH pathway. Thus, the presence of HS on cells and the ability of HSV-1 to engage HS do not direct HSV-1 to a pH-dependent entry pathway. HSV-1 lacking gC accumulated in endosomes during viral entry, supporting the notion that gC influences viral penetration from endosomes. Interestingly, the pH-neutral cell–cell fusion mediated by HSV-1 glycoproteins gB, gD, and gH/gL was not altered by gC. Soluble heparin inhibited cell–cell fusion regardless of the presence of gC or heparan sulfate. The kinetics of endocytic uptake of gC-null HSV-1 was rapid and very similar to wild type virus. Thus, the role of gC in regulating low pH entry of HSV-1 occurs downstream of internalization of enveloped particles from the plasma membrane. Together, the results presented here and elsewhere support a post-attachment, post-internalization function for gC in HSV-1 entry that is independent of HS.
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spelling doaj-art-4173834e9af7407a8195ea5c19554e002025-08-20T03:06:13ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2025-04-011610.3389/fmicb.2025.15493491549349Herpes simplex virus 1 glycoprotein C promotes virus penetration from endosomes during entry, independent of interaction with heparan sulfateSeth M. Schneider0Seth M. Schneider1Giulia Tebaldi2Katrina A. Gianopulos3Katrina A. Gianopulos4Darin J. Weed5Suzanne M. Pritchard6Chloe Leach7Anthony V. Nicola8Anthony V. Nicola9Department of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA, United StatesSchool of Molecular Biosciences, College of Veterinary Medicine, Washington State University, Pullman, WA, United StatesDepartment of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA, United StatesDepartment of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA, United StatesSchool of Molecular Biosciences, College of Veterinary Medicine, Washington State University, Pullman, WA, United StatesDepartment of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA, United StatesDepartment of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA, United StatesDepartment of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA, United StatesDepartment of Veterinary Microbiology and Pathology, College of Veterinary Medicine, Washington State University, Pullman, WA, United StatesSchool of Molecular Biosciences, College of Veterinary Medicine, Washington State University, Pullman, WA, United StatesHerpes simplex virus 1 (HSV-1) gC is a multi-functional glycoprotein present in the viral envelope and on the surface of infected cells. Virion gC, and to a lesser extent the fusion protein gB, interacts with host heparan sulfate to mediate HSV-1 attachment to the cell surface. Virion gC selectively facilitates HSV-1 entry into cells that support entry by a low pH-dependent endocytic pathway. gC regulates fusion-associated conformational changes in gB. Here we investigated the mechanism by which gC plays a post-attachment role in HSV-1 entry into cells. HSV-1 entered HS-deficient cells by a low pH-dependent route. Similarly, HSV-1 deleted for HS-binding domains entered HS-bearing cells by a low pH pathway. Thus, the presence of HS on cells and the ability of HSV-1 to engage HS do not direct HSV-1 to a pH-dependent entry pathway. HSV-1 lacking gC accumulated in endosomes during viral entry, supporting the notion that gC influences viral penetration from endosomes. Interestingly, the pH-neutral cell–cell fusion mediated by HSV-1 glycoproteins gB, gD, and gH/gL was not altered by gC. Soluble heparin inhibited cell–cell fusion regardless of the presence of gC or heparan sulfate. The kinetics of endocytic uptake of gC-null HSV-1 was rapid and very similar to wild type virus. Thus, the role of gC in regulating low pH entry of HSV-1 occurs downstream of internalization of enveloped particles from the plasma membrane. Together, the results presented here and elsewhere support a post-attachment, post-internalization function for gC in HSV-1 entry that is independent of HS.https://www.frontiersin.org/articles/10.3389/fmicb.2025.1549349/fullherpes simplex virusfusionglycoprotein Cheparan sulfatevirus entryvirus penetration
spellingShingle Seth M. Schneider
Seth M. Schneider
Giulia Tebaldi
Katrina A. Gianopulos
Katrina A. Gianopulos
Darin J. Weed
Suzanne M. Pritchard
Chloe Leach
Anthony V. Nicola
Anthony V. Nicola
Herpes simplex virus 1 glycoprotein C promotes virus penetration from endosomes during entry, independent of interaction with heparan sulfate
Frontiers in Microbiology
herpes simplex virus
fusion
glycoprotein C
heparan sulfate
virus entry
virus penetration
title Herpes simplex virus 1 glycoprotein C promotes virus penetration from endosomes during entry, independent of interaction with heparan sulfate
title_full Herpes simplex virus 1 glycoprotein C promotes virus penetration from endosomes during entry, independent of interaction with heparan sulfate
title_fullStr Herpes simplex virus 1 glycoprotein C promotes virus penetration from endosomes during entry, independent of interaction with heparan sulfate
title_full_unstemmed Herpes simplex virus 1 glycoprotein C promotes virus penetration from endosomes during entry, independent of interaction with heparan sulfate
title_short Herpes simplex virus 1 glycoprotein C promotes virus penetration from endosomes during entry, independent of interaction with heparan sulfate
title_sort herpes simplex virus 1 glycoprotein c promotes virus penetration from endosomes during entry independent of interaction with heparan sulfate
topic herpes simplex virus
fusion
glycoprotein C
heparan sulfate
virus entry
virus penetration
url https://www.frontiersin.org/articles/10.3389/fmicb.2025.1549349/full
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