Structural Plasticity of the Semliki Forest Virus Glycome upon Interspecies Transmission

Hdl Handle:
http://hdl.handle.net/10149/621122
Title:
Structural Plasticity of the Semliki Forest Virus Glycome upon Interspecies Transmission
Authors:
Crispin, M. (Max); Harvey, D. J. (David J.); Bitto, D. (David); Bonomelli, C. (Camille); Edgeworth, M. (Matthew); Scrivens, J. H. (James H.) ( 0000-0001-7444-6871 ) ; Huiskonen, J. T. (Juha T.); Bowden, T. A. (Thomas A.)
Affiliation:
Teesside University. Technology Futures Institute
Citation:
Crispin, M., Harvey, D. J., Bitto, D., Bonomelli, C., Edgeworth, M., Scrivens, J. H., Huiskonen, J. T., Bowden, T. A. (2014) 'Structural Plasticity of the Semliki Forest Virus Glycome upon Interspecies Transmission' Journal of Proteome Research; 13(3): 1702-1712 : DOI: 10.1021/pr401162k
Publisher:
American Chemical Society
Journal:
Journal of Proteome Research
Issue Date:
28-Jan-2014
URI:
http://hdl.handle.net/10149/621122
DOI:
10.1021/pr401162k
Additional Links:
http://pubs.acs.org/doi/abs/10.1021/pr401162k
Abstract:
Cross-species viral transmission subjects parent and progeny alphaviruses to differential post-translational processing of viral envelope glycoproteins. Alphavirus biogenesis has been extensively studied, and the Semliki Forest virus E1 and E2 glycoproteins have been shown to exhibit differing degrees of processing of N-linked glycans. However the composition of these glycans, including that arising from different host cells, has not been determined. Here we determined the chemical composition of the glycans from the prototypic alphavirus, Semliki Forest virus, propagated in both arthropod and rodent cell lines, by using ion-mobility mass spectrometry and collision-induced dissociation analysis. We observe that both the membrane-proximal E1 fusion glycoprotein and the protruding E2 attachment glycoprotein display heterogeneous glycosylation that contains N-linked glycans exhibiting both limited and extensive processing. However, E1 contained predominantly highly processed glycans dependent on the host cell, with rodent and mosquito-derived E1 exhibiting complex-type and paucimannose-type glycosylation, respectively. In contrast, the protruding E2 attachment glycoprotein primarily contained conserved under-processed oligomannose-type structures when produced in both rodent and mosquito cell lines. It is likely that glycan processing of E2 is structurally restricted by steric-hindrance imposed by local viral protein structure. This contrasts E1, which presents glycans characteristic of the host cell and is accessible to enzymes. We integrated our findings with previous cryo-electron microscopy and crystallographic analyses to produce a detailed model of the glycosylated mature virion surface. Taken together, these data reveal the degree to which virally encoded protein structure and cellular processing enzymes shape the virion glycome during interspecies transmission of Semliki Forest virus.
Type:
Article
Language:
en
ISSN:
1535-3893; 1535-3907
Rights:
This is an open access article published under a Creative Commons Attribution (CC-BY) License, which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited. For full details see http://pubs.acs.org/doi/abs/10.1021/pr401162k [Accessed: 18/05/2017]

Full metadata record

DC FieldValue Language
dc.contributor.authorCrispin, M. (Max)en
dc.contributor.authorHarvey, D. J. (David J.)en
dc.contributor.authorBitto, D. (David)en
dc.contributor.authorBonomelli, C. (Camille)en
dc.contributor.authorEdgeworth, M. (Matthew)en
dc.contributor.authorScrivens, J. H. (James H.)en
dc.contributor.authorHuiskonen, J. T. (Juha T.)en
dc.contributor.authorBowden, T. A. (Thomas A.)en
dc.date.accessioned2017-05-18T17:48:23Z-
dc.date.available2017-05-18T17:48:23Z-
dc.date.issued2014-01-28-
dc.identifier.citationJournal of Proteome Research; 13(3): 1702-1712en
dc.identifier.issn1535-3893-
dc.identifier.issn1535-3907-
dc.identifier.doi10.1021/pr401162k-
dc.identifier.urihttp://hdl.handle.net/10149/621122-
dc.description.abstractCross-species viral transmission subjects parent and progeny alphaviruses to differential post-translational processing of viral envelope glycoproteins. Alphavirus biogenesis has been extensively studied, and the Semliki Forest virus E1 and E2 glycoproteins have been shown to exhibit differing degrees of processing of N-linked glycans. However the composition of these glycans, including that arising from different host cells, has not been determined. Here we determined the chemical composition of the glycans from the prototypic alphavirus, Semliki Forest virus, propagated in both arthropod and rodent cell lines, by using ion-mobility mass spectrometry and collision-induced dissociation analysis. We observe that both the membrane-proximal E1 fusion glycoprotein and the protruding E2 attachment glycoprotein display heterogeneous glycosylation that contains N-linked glycans exhibiting both limited and extensive processing. However, E1 contained predominantly highly processed glycans dependent on the host cell, with rodent and mosquito-derived E1 exhibiting complex-type and paucimannose-type glycosylation, respectively. In contrast, the protruding E2 attachment glycoprotein primarily contained conserved under-processed oligomannose-type structures when produced in both rodent and mosquito cell lines. It is likely that glycan processing of E2 is structurally restricted by steric-hindrance imposed by local viral protein structure. This contrasts E1, which presents glycans characteristic of the host cell and is accessible to enzymes. We integrated our findings with previous cryo-electron microscopy and crystallographic analyses to produce a detailed model of the glycosylated mature virion surface. Taken together, these data reveal the degree to which virally encoded protein structure and cellular processing enzymes shape the virion glycome during interspecies transmission of Semliki Forest virus.en
dc.language.isoenen
dc.publisherAmerican Chemical Societyen
dc.relation.urlhttp://pubs.acs.org/doi/abs/10.1021/pr401162ken
dc.rightsThis is an open access article published under a Creative Commons Attribution (CC-BY) License, which permits unrestricted use, distribution and reproduction in any medium, provided the author and source are cited. For full details see http://pubs.acs.org/doi/abs/10.1021/pr401162k [Accessed: 18/05/2017]en
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/*
dc.titleStructural Plasticity of the Semliki Forest Virus Glycome upon Interspecies Transmissionen
dc.typeArticleen
dc.contributor.departmentTeesside University. Technology Futures Instituteen
dc.identifier.journalJournal of Proteome Researchen
or.citation.harvardCrispin, M., Harvey, D. J., Bitto, D., Bonomelli, C., Edgeworth, M., Scrivens, J. H., Huiskonen, J. T., Bowden, T. A. (2014) 'Structural Plasticity of the Semliki Forest Virus Glycome upon Interspecies Transmission' Journal of Proteome Research; 13(3): 1702-1712 : DOI: 10.1021/pr401162k-
dc.eprint.versionPublisher's Version/PDFen
dc.embargoNoneen
dc.date.accepted2014-
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