Tombusviruses upregulate phospholipid biosynthesis via interaction between p33 replication protein and yeast lipid sensor proteins during virus replication in yeast

Daniel Barajas; Kai Xu; Monika Sharma; Cheng Yu Wu; Peter D. Nagy

doi:10.1016/j.virol.2014.10.005

Tombusviruses upregulate phospholipid biosynthesis via interaction between p33 replication protein and yeast lipid sensor proteins during virus replication in yeast

Daniel Barajas, Kai Xu, Monika Sharma, Cheng Yu Wu, Peter D. Nagy

Plant Pathology

Research output: Contribution to journal › Article › peer-review

28 Scopus citations

Abstract

Positive-stranded RNA viruses induce new membranous structures and promote membrane proliferation in infected cells to facilitate viral replication. In this paper, the authors show that a plant-infecting tombusvirus upregulates transcription of phospholipid biosynthesis genes, such as INO1, OPI3 and CHO1, and increases phospholipid levels in yeast model host. This is accomplished by the viral p33 replication protein, which interacts with Opi1p FFAT domain protein and Scs2p VAP protein. Opi1p and Scs2p are phospholipid sensor proteins and they repress the expression of phospholipid genes. Accordingly, deletion of OPI1 transcription repressor in yeast has a stimulatory effect on TBSV RNA accumulation and enhanced tombusvirus replicase activity in an in vitro assay. Altogether, the presented data convincingly demonstrate that de novo lipid biosynthesis is required for optimal TBSV replication. Overall, this work reveals that a (+)RNA virus reprograms the phospholipid biosynthesis pathway in a unique way to facilitate its replication in yeast cells.

Original language	English
Pages (from-to)	72-80
Number of pages	9
Journal	Virology
Volume	471-473
DOIs	https://doi.org/10.1016/j.virol.2014.10.005
State	Published - Dec 1 2014

Bibliographical note

Funding Information:
We thank Dr. Menghsuen Chiu for his initial contribution to this project, and Dr. Judit Pogany for critical reading of the manuscript and for very helpful suggestions. This work was supported by the National Science Foundation ( MCB-1122039 ), and the Kentucky Science Foundation to PDN. The lipid analyses described in this work were performed at the Kansas Lipidomics Research Center Analytical Laboratory. Kansas Lipidomics Research Center was supported by National Science Foundation ( EPS 0236913 , MCB 0455318 , DBI 0521587 ), Kansas Technology Enterprise Corporation, K-IDeA Networks of Biomedical Research Excellence (INBRE) of National Institute of Health ( P20RR16475 ), and Kansas State University .

Publisher Copyright:
© 2014 Elsevier Inc.

Keywords

FFAT domain
Membrane proliferation
Phosphatidic acid
Phospholipids
Replicase
Replication in vitro
Tomato bushy stunt virus
Transcription repressor
VAP domain
Yeast host

ASJC Scopus subject areas

Virology

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10.1016/j.virol.2014.10.005

Cite this

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title = "Tombusviruses upregulate phospholipid biosynthesis via interaction between p33 replication protein and yeast lipid sensor proteins during virus replication in yeast",

abstract = "Positive-stranded RNA viruses induce new membranous structures and promote membrane proliferation in infected cells to facilitate viral replication. In this paper, the authors show that a plant-infecting tombusvirus upregulates transcription of phospholipid biosynthesis genes, such as INO1, OPI3 and CHO1, and increases phospholipid levels in yeast model host. This is accomplished by the viral p33 replication protein, which interacts with Opi1p FFAT domain protein and Scs2p VAP protein. Opi1p and Scs2p are phospholipid sensor proteins and they repress the expression of phospholipid genes. Accordingly, deletion of OPI1 transcription repressor in yeast has a stimulatory effect on TBSV RNA accumulation and enhanced tombusvirus replicase activity in an in vitro assay. Altogether, the presented data convincingly demonstrate that de novo lipid biosynthesis is required for optimal TBSV replication. Overall, this work reveals that a (+)RNA virus reprograms the phospholipid biosynthesis pathway in a unique way to facilitate its replication in yeast cells.",

keywords = "FFAT domain, Membrane proliferation, Phosphatidic acid, Phospholipids, Replicase, Replication in vitro, Tomato bushy stunt virus, Transcription repressor, VAP domain, Yeast host",

author = "Daniel Barajas and Kai Xu and Monika Sharma and Wu, {Cheng Yu} and Nagy, {Peter D.}",

note = "Funding Information: We thank Dr. Menghsuen Chiu for his initial contribution to this project, and Dr. Judit Pogany for critical reading of the manuscript and for very helpful suggestions. This work was supported by the National Science Foundation ( MCB-1122039 ), and the Kentucky Science Foundation to PDN. The lipid analyses described in this work were performed at the Kansas Lipidomics Research Center Analytical Laboratory. Kansas Lipidomics Research Center was supported by National Science Foundation ( EPS 0236913 , MCB 0455318 , DBI 0521587 ), Kansas Technology Enterprise Corporation, K-IDeA Networks of Biomedical Research Excellence (INBRE) of National Institute of Health ( P20RR16475 ), and Kansas State University . Publisher Copyright: {\textcopyright} 2014 Elsevier Inc.",

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AU - Barajas, Daniel

AU - Xu, Kai

AU - Sharma, Monika

AU - Wu, Cheng Yu

AU - Nagy, Peter D.

N1 - Funding Information: We thank Dr. Menghsuen Chiu for his initial contribution to this project, and Dr. Judit Pogany for critical reading of the manuscript and for very helpful suggestions. This work was supported by the National Science Foundation ( MCB-1122039 ), and the Kentucky Science Foundation to PDN. The lipid analyses described in this work were performed at the Kansas Lipidomics Research Center Analytical Laboratory. Kansas Lipidomics Research Center was supported by National Science Foundation ( EPS 0236913 , MCB 0455318 , DBI 0521587 ), Kansas Technology Enterprise Corporation, K-IDeA Networks of Biomedical Research Excellence (INBRE) of National Institute of Health ( P20RR16475 ), and Kansas State University . Publisher Copyright: © 2014 Elsevier Inc.

PY - 2014/12/1

Y1 - 2014/12/1

N2 - Positive-stranded RNA viruses induce new membranous structures and promote membrane proliferation in infected cells to facilitate viral replication. In this paper, the authors show that a plant-infecting tombusvirus upregulates transcription of phospholipid biosynthesis genes, such as INO1, OPI3 and CHO1, and increases phospholipid levels in yeast model host. This is accomplished by the viral p33 replication protein, which interacts with Opi1p FFAT domain protein and Scs2p VAP protein. Opi1p and Scs2p are phospholipid sensor proteins and they repress the expression of phospholipid genes. Accordingly, deletion of OPI1 transcription repressor in yeast has a stimulatory effect on TBSV RNA accumulation and enhanced tombusvirus replicase activity in an in vitro assay. Altogether, the presented data convincingly demonstrate that de novo lipid biosynthesis is required for optimal TBSV replication. Overall, this work reveals that a (+)RNA virus reprograms the phospholipid biosynthesis pathway in a unique way to facilitate its replication in yeast cells.

AB - Positive-stranded RNA viruses induce new membranous structures and promote membrane proliferation in infected cells to facilitate viral replication. In this paper, the authors show that a plant-infecting tombusvirus upregulates transcription of phospholipid biosynthesis genes, such as INO1, OPI3 and CHO1, and increases phospholipid levels in yeast model host. This is accomplished by the viral p33 replication protein, which interacts with Opi1p FFAT domain protein and Scs2p VAP protein. Opi1p and Scs2p are phospholipid sensor proteins and they repress the expression of phospholipid genes. Accordingly, deletion of OPI1 transcription repressor in yeast has a stimulatory effect on TBSV RNA accumulation and enhanced tombusvirus replicase activity in an in vitro assay. Altogether, the presented data convincingly demonstrate that de novo lipid biosynthesis is required for optimal TBSV replication. Overall, this work reveals that a (+)RNA virus reprograms the phospholipid biosynthesis pathway in a unique way to facilitate its replication in yeast cells.

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KW - Phosphatidic acid

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KW - Replicase

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KW - VAP domain

KW - Yeast host

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VL - 471-473

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JO - Virology

JF - Virology

ER -

Tombusviruses upregulate phospholipid biosynthesis via interaction between p33 replication protein and yeast lipid sensor proteins during virus replication in yeast

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

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