Hsp90 Interacts Specifically with Viral RNA and Differentially Regulates Replication Initiation of Bamboo mosaic virus and Associated Satellite RNA

Huang, Ying; Hu, Chung Chi; Liou, Ming Ru; Chang, Ban Yang; Tsai, Ching Hsiu; Meng, Menghsiao; Lin, Na; Hsu, Yau-Heiu

doi:10.1371/journal.ppat.1002726

Cited by 82 publications

(70 citation statements)

References 79 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Recently, Huang et al, (20) showed that Hsp90 of N. benthamiana binds to the 3= UTR of BaMV genomic RNA and is required for the efficient accumulation of the genomic RNA during the early stages of infection. This finding suggests a potential function of Hsp90 in regulating viral RNA replication through interaction with viral RNAs.…”

Section: Discussionmentioning

confidence: 99%

“…For instance, Hsp70 facilitates the assembly and disassembly of viral capsids (7,26,46), promotes the subcellular transport of tombusvirus replicase proteins and affects the activity or assembly of tombusvirus replicase complexes (71,90), controls potyvirus gene expression in cooperation with its cochaperone CPIP (17), and positively and negatively affects the genome replication of various viruses (5,45,91). Hsp90 affects the early stages of Bamboo mosaic virus (BaMV) infection by binding to the genomic RNA (20), increases the synthesis or stability of viral proteins (4,8), supports the assembly and nuclear import of influenza A virus RNA polymerase complex (59,63), and tightly regulates hepatitis C virus replication in cooperation with FKBP8 and hB-ind1 cochaperones (67,79,88).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Differential Roles of Hsp70 and Hsp90 in the Assembly of the Replicase Complex of a Positive-Strand RNA Plant Virus

Mine

Hyodo

Tajima

et al. 2012

J Virol

View full text Add to dashboard Cite

Japan bAssembly of viral replicase complexes of eukaryotic positive-strand RNA viruses is a regulated process: multiple viral and host components must be assembled on intracellular membranes and ordered into quaternary complexes capable of synthesizing viral RNAs. However, the molecular mechanisms underlying this process are poorly understood. In this study, we used a model virus, Red clover necrotic mosaic virus (RCNMV), whose replicase complex can be detected readily as the 480-kDa functional protein complex. We found that host heat shock proteins Hsp70 and Hsp90 are required for RCNMV RNA replication and that they interact with p27, a virus-encoded component of the 480-kDa replicase complex, on the endoplasmic reticulum membrane. Using a cell-free viral translation/replication system in combination with specific inhibitors of Hsp70 and Hsp90, we found that inhibition of p27-Hsp70 interaction inhibits the formation of the 480-kDa complex but instead induces the accumulation of large complexes that are nonfunctional in viral RNA synthesis. In contrast, inhibition of p27-Hsp90 interaction did not induce such large complexes but rendered p27 incapable of binding to a specific viral RNA element, which is a critical step for the assembly of the 480-kDa replicase complex and viral RNA replication. Together, our results suggest that Hsp70 and Hsp90 regulate different steps in the assembly of the RCNMV replicase complex. Most plant and animal viruses are positive-strand RNA viruses, which have single-stranded messenger-sense genomic RNAs. These viruses often induce host membrane rearrangements to form organelle-like compartments in which viral genomic RNAs are replicated via negative-strand RNA intermediates by the viral replicase complexes (10). Viral replicase complexes comprise multiple proteins, including viral auxiliary proteins, viral RNAdependent RNA polymerase (RdRP), and host proteins (61). Viral replicase complexes have been studied extensively by characterizing their RdRP activities and the functions of the viral and host components of the complexes. These studies have provided important information about the mechanisms regulating genome replication (15, 19, 47, 89), viral pathogenicity (68, 69), and virushost interactions (24,25,32,33). However, an important question remains: how do multiple viral and host components assemble properly into the replicase complex?Molecular chaperones are essential for cell viability by ensuring folding of newly synthesized proteins, refolding of misfolded or aggregated proteins, protein complex assembly and disassembly, membrane translocation of organellar and secretory proteins, protein degradation, and activities of regulatory proteins in signal transduction pathways (12,18,51). In eukaryotic cells, the abundant and highly conserved molecular chaperones heat shock proteins Hsp70 and Hsp90 play central roles in the biological processes mentioned above, and the activities of Hsp70 and Hsp90 are modulated by a variety of cochaperones (37,80). Considering their pivotal roles i...

show abstract

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

Differential Roles of Hsp70 and Hsp90 in the Assembly of the Replicase Complex of a Positive-Strand RNA Plant Virus

Mine

Hyodo

Tajima

et al. 2012

J Virol

View full text Add to dashboard Cite

show abstract

“…Fibrillarin is required for only satBaMV, but not HV long-distance trafficking, which suggests that HV and satRNA may have evolved distinct methods for trafficking. A previous study also found a differential requirement for the host factor heat shock protein 90 in the replication of HV and satBaMV (Huang et al, 2012).…”

Section: Discussionmentioning

confidence: 67%

The Nucleolar Fibrillarin Protein Is Required for Helper Virus-Independent Long-Distance Trafficking of a Subviral Satellite RNA in Plants

et al. 2016

View full text Add to dashboard Cite

RNA trafficking plays pivotal roles in regulating plant development, gene silencing, and adaptation to environmental stress. Satellite RNAs (satRNAs), parasites of viruses, depend on their helper viruses (HVs) for replication, encapsidation, and efficient spread. However, it remains largely unknown how satRNAs interact with viruses and the cellular machinery to undergo trafficking. Here, we show that the P20 protein of Bamboo mosaic potexvirus satRNA (satBaMV) can functionally complement in trans the systemic trafficking of P20-defective satBaMV in infected Nicotiana benthamiana. The transgenederived satBaMV, uncoupled from HV replication, was able to move autonomously across a graft union identified by RT-qPCR, RNA gel blot, and in situ RT-PCR analyses. Coimmunoprecipitation experiments revealed that the major nucleolar protein fibrillarin is coprecipitated in the P20 protein complex. Notably, silencing fibrillarin suppressed satBaMV-, but not HV-, phloem-based movement following grafting or coinoculation with HV. Confocal microscopy revealed that the P20 protein colocalized with fibrillarin in the nucleoli and formed punctate structures associated with plasmodesmata. The mobile satBaMV RNA appears to exist as ribonucleoprotein (RNP) complex composed of P20 and fibrillarin, whereas BaMV movement proteins, capsid protein, and BaMV RNA are recruited with HV coinfection. Taken together, our findings provide insight into movement of satBaMV via the fibrillarin-satBaMV-P20 RNP complex in phloem-mediated systemic trafficking.

show abstract

“…One important conclusion from these studies is that different viruses require different sets of host genes for multiplication. Molecular chaperones are a class of widely utilized host factors (53,97,118,128,136). In ToMV, heat shock protein 70 (Hsp70) copurifies with the replication proteins (Figure 3c), but its roles in virus multiplication have not been clarified.…”

Section: Host Factors Involved In Tobamovirus Rna Replicationmentioning

confidence: 99%

Replication of Tobamovirus RNA

Ishibashi

Ishikawa

2016

Annu. Rev. Phytopathol.

View full text Add to dashboard Cite

Tobacco mosaic virus and other tobamoviruses have served as models for studying the mechanisms of viral RNA replication. In tobamoviruses, genomic RNA replication occurs via several steps: (a) synthesis of viral replication proteins by translation of the genomic RNA; (b) translation-coupled binding of the replication proteins to a 5'-terminal region of the genomic RNA; (c) recruitment of the genomic RNA by replication proteins onto membranes and formation of a complex with host proteins TOM1 and ARL8; (d) synthesis of complementary (negative-strand) RNA in the complex; and (e) synthesis of progeny genomic RNA. This article reviews current knowledge on tobamovirus RNA replication, particularly regarding how the genomic RNA is specifically selected as a replication template and how the replication proteins are activated. We also focus on the roles of the replication proteins in evading or suppressing host defense systems.

show abstract

Hsp90 Interacts Specifically with Viral RNA and Differentially Regulates Replication Initiation of Bamboo mosaic virus and Associated Satellite RNA

Cited by 82 publications

References 79 publications

Differential Roles of Hsp70 and Hsp90 in the Assembly of the Replicase Complex of a Positive-Strand RNA Plant Virus

Differential Roles of Hsp70 and Hsp90 in the Assembly of the Replicase Complex of a Positive-Strand RNA Plant Virus

The Nucleolar Fibrillarin Protein Is Required for Helper Virus-Independent Long-Distance Trafficking of a Subviral Satellite RNA in Plants

Replication of Tobamovirus RNA

Contact Info

Product

Resources

About