Reovirus σNS and μNS Proteins Remodel the Endoplasmic Reticulum to Build Replication Neo-Organelles

ABSTRACT Like most viruses that replicate in the cytoplasm, mammalian reoviruses assemble membranous neo-organelles called inclusions that serve as sites of viral genome replication and particle morphogenesis. Viral inclusion formation is essential for viral infection, but how these organelles form...

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Autores principales:	Raquel Tenorio, Isabel Fernández de Castro, Jonathan J. Knowlton, Paula F. Zamora, Christopher H. Lee, Bernardo A. Mainou, Terence S. Dermody, Cristina Risco
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	endoplasmic reticulum membrane remodeling reovirus virus factory biogenesis Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/220f31bdbe884567803468aa348bcc8f
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spelling	oai:doaj.org-article:220f31bdbe884567803468aa348bcc8f2021-11-15T16:00:16ZReovirus σNS and μNS Proteins Remodel the Endoplasmic Reticulum to Build Replication Neo-Organelles10.1128/mBio.01253-182150-7511https://doaj.org/article/220f31bdbe884567803468aa348bcc8f2018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01253-18https://doaj.org/toc/2150-7511ABSTRACT Like most viruses that replicate in the cytoplasm, mammalian reoviruses assemble membranous neo-organelles called inclusions that serve as sites of viral genome replication and particle morphogenesis. Viral inclusion formation is essential for viral infection, but how these organelles form is not well understood. We investigated the biogenesis of reovirus inclusions. Correlative light and electron microscopy showed that endoplasmic reticulum (ER) membranes are in contact with nascent inclusions, which form by collections of membranous tubules and vesicles as revealed by electron tomography. ER markers and newly synthesized viral RNA are detected in inclusion internal membranes. Live-cell imaging showed that early in infection, the ER is transformed into thin cisternae that fragment into small tubules and vesicles. We discovered that ER tubulation and vesiculation are mediated by the reovirus σNS and μNS proteins, respectively. Our results enhance an understanding of how viruses remodel cellular compartments to build functional replication organelles. IMPORTANCE Viruses modify cellular structures to build replication organelles. These organelles serve as sites of viral genome replication and particle morphogenesis and are essential for viral infection. However, how these organelles are constructed is not well understood. We found that the replication organelles of mammalian reoviruses are formed by collections of membranous tubules and vesicles derived from extensive remodeling of the peripheral endoplasmic reticulum (ER). We also observed that ER tubulation and vesiculation are triggered by the reovirus σNS and μNS proteins, respectively. Our results enhance an understanding of how viruses remodel cellular compartments to build functional replication organelles and provide functions for two enigmatic reovirus replication proteins. Most importantly, this research uncovers a new mechanism by which viruses form factories for particle assembly.Raquel TenorioIsabel Fernández de CastroJonathan J. KnowltonPaula F. ZamoraChristopher H. LeeBernardo A. MainouTerence S. DermodyCristina RiscoAmerican Society for Microbiologyarticleendoplasmic reticulummembrane remodelingreovirusvirus factory biogenesisMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	endoplasmic reticulum membrane remodeling reovirus virus factory biogenesis Microbiology QR1-502
spellingShingle	endoplasmic reticulum membrane remodeling reovirus virus factory biogenesis Microbiology QR1-502 Raquel Tenorio Isabel Fernández de Castro Jonathan J. Knowlton Paula F. Zamora Christopher H. Lee Bernardo A. Mainou Terence S. Dermody Cristina Risco Reovirus σNS and μNS Proteins Remodel the Endoplasmic Reticulum to Build Replication Neo-Organelles
description	ABSTRACT Like most viruses that replicate in the cytoplasm, mammalian reoviruses assemble membranous neo-organelles called inclusions that serve as sites of viral genome replication and particle morphogenesis. Viral inclusion formation is essential for viral infection, but how these organelles form is not well understood. We investigated the biogenesis of reovirus inclusions. Correlative light and electron microscopy showed that endoplasmic reticulum (ER) membranes are in contact with nascent inclusions, which form by collections of membranous tubules and vesicles as revealed by electron tomography. ER markers and newly synthesized viral RNA are detected in inclusion internal membranes. Live-cell imaging showed that early in infection, the ER is transformed into thin cisternae that fragment into small tubules and vesicles. We discovered that ER tubulation and vesiculation are mediated by the reovirus σNS and μNS proteins, respectively. Our results enhance an understanding of how viruses remodel cellular compartments to build functional replication organelles. IMPORTANCE Viruses modify cellular structures to build replication organelles. These organelles serve as sites of viral genome replication and particle morphogenesis and are essential for viral infection. However, how these organelles are constructed is not well understood. We found that the replication organelles of mammalian reoviruses are formed by collections of membranous tubules and vesicles derived from extensive remodeling of the peripheral endoplasmic reticulum (ER). We also observed that ER tubulation and vesiculation are triggered by the reovirus σNS and μNS proteins, respectively. Our results enhance an understanding of how viruses remodel cellular compartments to build functional replication organelles and provide functions for two enigmatic reovirus replication proteins. Most importantly, this research uncovers a new mechanism by which viruses form factories for particle assembly.
format	article
author	Raquel Tenorio Isabel Fernández de Castro Jonathan J. Knowlton Paula F. Zamora Christopher H. Lee Bernardo A. Mainou Terence S. Dermody Cristina Risco
author_facet	Raquel Tenorio Isabel Fernández de Castro Jonathan J. Knowlton Paula F. Zamora Christopher H. Lee Bernardo A. Mainou Terence S. Dermody Cristina Risco
author_sort	Raquel Tenorio
title	Reovirus σNS and μNS Proteins Remodel the Endoplasmic Reticulum to Build Replication Neo-Organelles
title_short	Reovirus σNS and μNS Proteins Remodel the Endoplasmic Reticulum to Build Replication Neo-Organelles
title_full	Reovirus σNS and μNS Proteins Remodel the Endoplasmic Reticulum to Build Replication Neo-Organelles
title_fullStr	Reovirus σNS and μNS Proteins Remodel the Endoplasmic Reticulum to Build Replication Neo-Organelles
title_full_unstemmed	Reovirus σNS and μNS Proteins Remodel the Endoplasmic Reticulum to Build Replication Neo-Organelles
title_sort	reovirus σns and μns proteins remodel the endoplasmic reticulum to build replication neo-organelles
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/220f31bdbe884567803468aa348bcc8f
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Reovirus σNS and μNS Proteins Remodel the Endoplasmic Reticulum to Build Replication Neo-Organelles

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