A Unique Role for the Host ESCRT Proteins in Replication of Tomato bushy stunt virus

Barajas, Daniel; Jiang, Yi; Nagy, Peter D.

doi:10.1371/journal.ppat.1000705

Cited by 170 publications

(227 citation statements)

References 56 publications

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“…In contrast, RNA polymerase activity is required for the formation of replication complex spherules by Flock House virus and Semliki Forest virus (50,51). In a certain host mutant, negative-strand RNA of tomato bushy stunt virus accumulates to levels similar to that in wild-type cells, but the negative-strand RNA is sensitive to nucleases, unlike in wild-type cells (52). Thus, the requirement for negative-strand RNA synthesis in membrane rearrangement/template sequestration differs from one virus to another.…”

Section: Discussionmentioning

confidence: 97%

The Resistance Protein Tm-1 Inhibits Formation of a Tomato Mosaic Virus Replication Protein-Host Membrane Protein Complex

Ishibashi

Ishikawa

2013

J Virol

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The Tm-1 gene of tomato confers resistance to Tomato mosaic virus (ToMV). Tm-1 encodes a protein that binds ToMV replication proteins and inhibits the RNA-dependent RNA replication of ToMV. The replication proteins of resistance-breaking mutants of ToMV do not bind Tm-1, indicating that the binding is important for inhibition. In this study, we analyzed how Tm-1 inhibits ToMV RNA replication in a cell-free system using evacuolated tobacco protoplast extracts. In this system, ToMV RNA replication is catalyzed by replication proteins bound to membranes, and the RNA polymerase activity is unaffected by treatment with 0.5 M NaCl-containing buffer and remains associated with membranes. We show that in the presence of Tm-1, negative-strand RNA synthesis is inhibited; the replication proteins associate with membranes with binding that is sensitive to 0.5 M NaCl; the viral genomic RNA used as a translation template is not protected from nuclease digestion; and host membrane proteins TOM1, TOM2A, and ARL8 are not copurified with the membrane-bound 130K replication protein. Deletion of the polymerase read-through domain or of the 3= untranslated region (UTR) of the genome did not prevent the formation of complexes between the 130K protein and the host membrane proteins, the 0.5 M NaCl-resistant binding of the replication proteins to membranes, and the protection of the genomic RNA from nucleases. These results indicate that Tm-1 binds ToMV replication proteins to inhibit key events in replication complex formation on membranes that precede negative-strand RNA synthesis. Tomato mosaic virus (ToMV) is a positive-strand RNA virus in the genus Tobamovirus, family Virgaviridae (1). The genome of a tobamovirus encodes at least four proteins (2). The 130K protein and its read-through product, the 180K protein, are involved in RNA replication and thus are referred to as replication proteins (3). The 130K protein contains the methyltransferase and helicase domains, and the read-through region of the 180K protein contains the polymerase domain. The other two tobamoviral proteins, movement protein and coat protein, are not required for RNA replication (4, 5).When the genomic RNA of a positive-strand RNA virus enters host cells, the replication proteins are translated from the genomic RNA, recognize the genomic RNA as a template for replication, and form replication complexes on intracellular membranes. Replication of all known eukaryotic positive-strand RNA viruses occurs in replication complexes formed on host membranes (6-10), which contain viral genomic RNAs, replication proteins, and host factors (11). To avoid elicitation of host defense systems triggered by viral double-stranded RNA (12), the activity of eukaryotic positive-strand RNA virus RNA-dependent RNA polymerases (RdRps) must be strictly regulated so that they synthesize negative-strand RNA only in the replication complexes that are sequestered from the cytoplasm. Many host factors, including chaperones and enzymes, and cellular membranes are hijacked by viruses for rep...

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Section: Discussionmentioning

confidence: 97%

The Resistance Protein Tm-1 Inhibits Formation of a Tomato Mosaic Virus Replication Protein-Host Membrane Protein Complex

Ishibashi

Ishikawa

2013

J Virol

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“…Ubiquitination of p33 seems to have no effect on its metabolic stability (Barajas and Nagy, 2010). Instead, it was found to contribute to the interaction with ESCRT (for endosomal sorting complexes required for transport) proteins (Barajas and Nagy, 2010), whose temporary recruitment to sites of viral replication is required for optimal replicase activity and protection of the viral RNA template (Barajas et al, 2009a). Ubiquitination of p33 thus appears to be required for the proper targeting of TBSV replication complexes.…”

Section: Monoubiquitination Of Viral Replication Proteinsmentioning

confidence: 99%

Ubiquitin and Plant Viruses, Let’s Play Together!

2012

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“…This viral protein was shown to interact with yeast ESCRT-I component, Vps23 in a ubiquitylation-dependent manner, thus suggesting that ESCRT recruitment by the virus occurs via this interaction (Barajas and Nagy 2010). Overexpression of dominant negative versions of AtVPS4/SKD1 and ESCRT-III components have been shown to interfere with tomato bushy stunt virus replication and assembly in plant models of viral infection, further supporting a role for ESCRT function in these processes (Barajas, et al 2009). The regulation of ion homeostasis by the ESCRT pathway can also be related to disease.…”

Section: Endocytic Trafficking and Diseasementioning

confidence: 92%

Endocytic regulation of alkali metal transport proteins in mammals, yeast and plants

et al. 2013

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Mulet Salort, JM.; Llopis Torregrosa, V.; Primo Planta, C.; Marques Romero, MC.; Yenush, L. (2013) The relative concentrations of ions and solutes inside cells are actively maintained by several classes of transport proteins, in many cases against their concentration gradient. These transport processes, which consume a large portion of cellular energy, must be constantly regulated. Many structurally distinct families of channels, carriers, and pumps have been characterized in considerable detail during the past decades and defects in the function of some of these proteins have been linked to a growing list of human diseases. The dynamic regulation of the transport proteins present at the cell surface is vital for both normal cellular function and for the successful adaptation to changing environments. The composition of proteins present at the cell surface is controlled on both the transcriptional and post-translational level. Post-translational regulation involves highly conserved mechanisms of phosphorylation-and ubiquitylation-dependent signal transduction routes used to modify the cohort of receptors and transport proteins present under any given circumstances. In this review, we will summarize what is currently known about one facet of this regulatory process: the endocytic regulation of alkali metal transport proteins. The physiological relevance, major contributors, parallels and missing pieces of the puzzle in mammals, yeast and plants will be discussed.

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A Unique Role for the Host ESCRT Proteins in Replication of Tomato bushy stunt virus

Cited by 170 publications

References 56 publications

The Resistance Protein Tm-1 Inhibits Formation of a Tomato Mosaic Virus Replication Protein-Host Membrane Protein Complex

The Resistance Protein Tm-1 Inhibits Formation of a Tomato Mosaic Virus Replication Protein-Host Membrane Protein Complex

Ubiquitin and Plant Viruses, Let’s Play Together!

Endocytic regulation of alkali metal transport proteins in mammals, yeast and plants

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