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Fragmentation of the Golgi apparatus provides replication membranes for human rhinovirus 1A.

ABSTRACT: All viruses with a positive-stranded RNA genome replicate their genomic RNA in association with membranes from the host cell. Here we demonstrate a novel organelle source of replication membranes for human rhinovirus 1A (HRV-1A). HRV-1A infection induces fragmentation of the Golgi apparatus, and Golgi membranes are rearranged into vesicles of approximately 250-500 nm diameter. The newly distributed Golgi membranes co-localize with viral RNA replication templates, strongly suggesting that the observed vesicles are the sites of viral RNA replication. Expression of the HRV-1A 3A protein induces alterations in the Golgi staining pattern similar to those seen during viral infection, and expressed 3A localizes to the Golgi-derived membranes. Taken together, these data show that in HRV-1A infection, the 3A protein plays a role in fragmenting the Golgi complex and generating vesicles that are used as the site of viral RNA replication.

SUBMITTER: Quiner CA

PROVIDER: S-EPMC7111317 | biostudies-literature | 2010 Nov

REPOSITORIES: biostudies-literature

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Fragmentation of the Golgi apparatus provides replication membranes for human rhinovirus 1A.

Quiner Claire A CA Jackson William T WT

Virology 20100909 2

All viruses with a positive-stranded RNA genome replicate their genomic RNA in association with membranes from the host cell. Here we demonstrate a novel organelle source of replication membranes for human rhinovirus 1A (HRV-1A). HRV-1A infection induces fragmentation of the Golgi apparatus, and Golgi membranes are rearranged into vesicles of approximately 250-500 nm diameter. The newly distributed Golgi membranes co-localize with viral RNA replication templates, strongly suggesting that the obs ...[more]

PMID: 20825962

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Project description:The replication of picornaviruses has been described to cause fragmentation of the Golgi apparatus that blocks the secretory pathway. The inhibition of major histocompatibility complex class I upregulation and cytokine, chemokine and interferon secretion may have important implications for host defense. Previous studies have shown that disruption of the secretory pathway can be replicated by expression of individual nonstructural proteins; however the situation with different serotypes of human rhinovirus (HRV) is unclear. The expression of 3A protein from HRV14 or HRV2 did not cause Golgi apparatus disruption or a block in secretion, whereas other studies showed that infection of cells with HRV1A did cause Golgi apparatus disruption which was replicated by the expression of 3A. HRV16 is the serotype most widely used in clinical HRV challenge studies; consequently, to address the issue of Golgi apparatus disruption for HRV16, we have systematically and quantitatively examined the effect of HRV16 on both Golgi apparatus fragmentation and protein secretion in HeLa cells. First, we expressed each individual nonstructural protein and examined their cellular localization and their disruption of endoplasmic reticulum and Golgi apparatus architecture. We quantified their effects on the secretory pathway by measuring secretion of the reporter protein Gaussia luciferase. Finally, we examined the same outcomes following infection of cells with live virus. We demonstrate that expression of HRV16 3A and 3AB and, to a lesser extent, 2B caused dispersal of the Golgi structure, and these three nonstructural proteins also inhibited protein secretion. The infection of cells with HRV16 also caused significant Golgi apparatus dispersal; however, this did not result in the inhibition of protein secretion. Importance: The ability of replicating picornaviruses to influence the function of the secretory pathway has important implications for host defense. However, there appear to be differences between different members of the family and inconsistent results when comparing infection with live virus to expression of individual nonstructural proteins. We demonstrate that individual nonstructural HRV16 proteins, when expressed in HeLa cells, can both fragment the Golgi apparatus and block secretion, whereas viral infection fragments the Golgi apparatus without blocking secretion. This has major implications for how we interpret mechanistic evidence derived from the expression of single viral proteins.

Dataset Information

Fragmentation of the Golgi apparatus provides replication membranes for human rhinovirus 1A.

Publications

Fragmentation of the Golgi apparatus provides replication membranes for human rhinovirus 1A.

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