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Structure and Assembly

Palmitoylation of Sindbis Virus TF Protein Regulates Its Plasma Membrane Localization and Subsequent Incorporation into Virions

Jolene Ramsey, Emily C. Renzi, Randy J. Arnold, Jonathan C. Trinidad, Suchetana Mukhopadhyay
Douglas S. Lyles, Editor
Jolene Ramsey
aDepartment of Biology, Indiana University, Bloomington, Indiana, USA
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Emily C. Renzi
bDepartment of Chemistry, Indiana University, Bloomington, Indiana, USA
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Randy J. Arnold
bDepartment of Chemistry, Indiana University, Bloomington, Indiana, USA
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Jonathan C. Trinidad
bDepartment of Chemistry, Indiana University, Bloomington, Indiana, USA
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Suchetana Mukhopadhyay
aDepartment of Biology, Indiana University, Bloomington, Indiana, USA
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Douglas S. Lyles
Wake Forest University
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DOI: 10.1128/JVI.02000-16
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ABSTRACT

Palmitoylation is a reversible, posttranslational modification that helps target proteins to cellular membranes. The alphavirus small membrane proteins 6K and TF have been reported to be palmitoylated and to positively regulate budding. 6K and TF are isoforms that are identical in their N termini but unique in their C termini due to a −1 ribosomal frameshift during translation. In this study, we used cysteine (Cys) mutants to test differential palmitoylation of the Sindbis virus 6K and TF proteins. We modularly mutated the five Cys residues in the identical N termini of 6K and TF, the four additional Cys residues in TF's unique C terminus, or all nine Cys residues in TF. Using these mutants, we determined that TF palmitoylation occurs primarily in the N terminus. In contrast, 6K is not palmitoylated, even on these shared residues. In the C-terminal Cys mutant, TF protein levels increase both in the cell and in the released virion compared to the wild type. In viruses with the N-terminal Cys residues mutated, TF is much less efficiently localized to the plasma membrane, and it is not incorporated into the virion. The three Cys mutants have minor defects in cell culture growth but a high incidence of abnormal particle morphologies compared to the wild-type virus as determined by transmission electron microscopy. We propose a model where the C terminus of TF modulates the palmitoylation of TF at the N terminus, and palmitoylated TF is preferentially trafficked to the plasma membrane for virus budding.

IMPORTANCE Alphaviruses are a reemerging viral cause of arthritogenic disease. Recently, the small 6K and TF proteins of alphaviruses were shown to contribute to virulence in vivo. Nevertheless, a clear understanding of the molecular mechanisms by which either protein acts to promote virus infection is missing. The TF protein is a component of budded virions, and optimal levels of TF correlate positively with wild-type-like particle morphology. In this study, we show that the palmitoylation of TF regulates its localization to the plasma membrane, which is the site of alphavirus budding. Mutants in which TF is not palmitoylated display drastically reduced plasma membrane localization, which effectively prevents TF from participating in budding or being incorporated into virus particles. Investigation of the regulation of TF will aid current efforts in the alphavirus field searching for approaches to mitigate alphaviral disease in humans.

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Palmitoylation of Sindbis Virus TF Protein Regulates Its Plasma Membrane Localization and Subsequent Incorporation into Virions
Jolene Ramsey, Emily C. Renzi, Randy J. Arnold, Jonathan C. Trinidad, Suchetana Mukhopadhyay
Journal of Virology Jan 2017, 91 (3) e02000-16; DOI: 10.1128/JVI.02000-16

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Palmitoylation of Sindbis Virus TF Protein Regulates Its Plasma Membrane Localization and Subsequent Incorporation into Virions
Jolene Ramsey, Emily C. Renzi, Randy J. Arnold, Jonathan C. Trinidad, Suchetana Mukhopadhyay
Journal of Virology Jan 2017, 91 (3) e02000-16; DOI: 10.1128/JVI.02000-16
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KEYWORDS

membrane proteins
Sindbis virus
Viral Proteins
virion
virus release
protein localization
virus budding
palmitoylation
6K
TF
alphavirus

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