Intercellular Transmission of Viral Populations with Vesicles

Altan‐Bonnet, Nihal; Chen, Ying-Han

doi:10.1128/jvi.01452-15

Cited by 43 publications

(40 citation statements)

References 21 publications

(23 reference statements)

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“…Indeed, we have demonstrated here that being wrapped inside vesicles may confer to the virus a number of advantages, including a greater efficiency of infection and the ability to stimulate phagocytosis. Therefore, these vesicles can facilitate the spread of the virus to other susceptible cells by collectively transferring multiple viral genomes into the cytoplasm (21). Also, we demonstrated that the vesicles confer to MsV resistance to high temperature.…”

Section: Discussionmentioning

confidence: 65%

“…This represented a breakthrough in virology as, until then, a virus was considered either enveloped or nonenveloped, without the useful in repelling specific antibodies, thus providing an important advantage to those viruses within their hosts (20,21). Given the natural hosts of marseilleviruses, this does not seem to be applicable, as amoebas do not possess an adaptive immune system.…”

Section: Discussionmentioning

confidence: 99%

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The Large Marseillevirus Explores Different Entry Pathways by Forming Giant Infectious Vesicles

Arantes

Rodrigues

Silva

et al. 2016

J Virol

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Triggering the amoebal phagocytosis process is a sine qua non condition for most giant viruses to initiate their replication cycle and consequently to promote their progeny formation. It is well known that the amoebal phagocytosis process requires the recognition of particles of >500 nm, and most amoebal giant viruses meet this requirement, such as mimivirus, pandoravirus, pithovirus, and mollivirus. However, in the context of the discovery of amoebal giant viruses in the last decade, Marseillevirus marseillevirus (MsV) has drawn our attention, because despite its ability to successfully replicate in Acanthamoeba, remarkably it does not fulfill the >500-nm condition, since it presents an ϳ250-nm icosahedrally shaped capsid. We deeply investigated the MsV cycle by using a set of methods, including virological, molecular, and microscopic (immunofluorescence, scanning electron microscopy, and transmission electron microscopy) assays. Our results revealed that MsV is able to form giant vesicles containing dozens to thousands of viral particles wrapped by membranes derived from amoebal endoplasmic reticulum. Remarkably, our results strongly suggested that these giant vesicles are able to stimulate amoebal phagocytosis and to trigger the MsV replication cycle by an acidification-independent process. Also, we observed that MsV entry may occur by the phagocytosis of grouped particles (without surrounding membranes) and by an endosome-stimulated pathway triggered by single particles. Taken together, not only do our data deeply describe the main features of MsV replication cycle, but this is the first time, to our knowledge, that the formation of giant infective vesicles related to a DNA virus has been described. IMPORTANCETriggering the amoebal phagocytosis process is a sine qua non condition required by most giant viruses to initiate their replication cycle. This process requires the recognition of particles of >500 nm, and many giant viruses meet this requirement. However, MsV is unusual, as despite having particles of ϳ250 nm it is able to replicate in Acanthamoeba. Our results revealed that MsV is able to form giant vesicles, containing dozens to thousands of viral particles, wrapped in membranes derived from amoebal endoplasmic reticulum. Remarkably, our results strongly suggest that these giant vesicles are able to stimulate phagocytosis using an acidification-independent process. Our work not only describes the main features of the MsV replication cycle but also describes, for the first time to our knowledge, the formation of huge infective vesicles in a large DNA viruses. T he discovery of the amoebal giant virus Acanthamoeba polyphaga mimivirus (APMV) in 2003 (1) raised new and exciting questions regarding the virosphere and boosted the hunt for new giant viruses. Owing to these efforts, an increasing number of remarkable giant viruses have been described (2-6).Recent data suggest that giant viruses initiate their replication cycles after being phagocytosed by amoebas or other phagocytic cells (1, 7). Th...

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Section: Discussionmentioning

confidence: 65%

Section: Discussionmentioning

confidence: 99%

The Large Marseillevirus Explores Different Entry Pathways by Forming Giant Infectious Vesicles

Arantes

Rodrigues

Silva

et al. 2016

J Virol

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“…not in vesicle) viral particles [11••]. This brings up the intriguing possibility that vesicular travel of viral populations may be nature's way of generating high multiplicities of infection in order to enhance viral propagation and survival [33]. In particular for RNA viruses, having a high multiplicity of infection can provide greater opportunities for genetic cooperativity [34•,35•].…”

Section: Vesicles Enable High Multiplicity Of Infection and Can Facilmentioning

confidence: 99%

Extracellular vesicles are the Trojan horses of viral infection

Altan‐Bonnet

2016

Current Opinion in Microbiology

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112

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Extracellular vesicles have recently emerged as a novel mode of viral propagation exploited by both enveloped and non-enveloped viruses. In particular non-enveloped viruses utilize the hosts' production of extracellular vesicles to exit from cells non-lytically and to hide and manipulate the immune system. Moreover, challenging the long held idea that viruses behave as independent genetic units, extracellular vesicles enable multiple viral particles and genomes to collectively traffic in and out of cells, which can promote genetic cooperativity among viral quasispecies and enhance the fitness of the overall viral population.

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“…Furthermore, after replication and assembly into new viral particles, all (+) ssRNA viruses can coopt membranes as carriers to be transported out of cells non-lytically and be transmitted to other susceptible hosts. These newly synthesized viruses can emerge as single membrane enveloped particles or as populations of viral particles, transported together to the next cell within membrane-bound vesicles [3,4]. In particular, the latter which enables trafficking of viral populations en masse from cell to cell can significantly enhance viral infectivity and replicative fitness [3,4].…”

Section: Introductionmentioning

confidence: 99%

Lipid Tales of Viral Replication and Transmission

Altan‐Bonnet

2017

Trends in Cell Biology

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118

106

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Positive strand RNA viruses are the largest group of RNA viruses on the planet and include many human, animal and plant pathogens. Cellular membranes are key players in all aspects of their life cycle, from entry and replication to assembly and exit. In particular, membranes are virally harnessed to serve as platforms for replication and as carriers to transmit viruses to other cells either as the envelope of a single virus or as the vesicle transporting a population of viruses. Studies have revealed significant convergence among different viruses to utilize membranes with specific lipid blueprints for replication and transmission. For replication many animal/human viruses utilize membranes enriched phosphatidylinositol 4-phosphate/cholesterol whereas many plant and insect-vectored animal viruses exploit ones with phosphatidylethanolamine/cholesterol. For transmission, phosphatidylserine enriched membranes are widely used as carriers for RNA and DNA viruses. Here we discuss the role of these membranes for viral pathogenesis and therapeutic development.

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Intercellular Transmission of Viral Populations with Vesicles

Cited by 43 publications

References 21 publications

The Large Marseillevirus Explores Different Entry Pathways by Forming Giant Infectious Vesicles

The Large Marseillevirus Explores Different Entry Pathways by Forming Giant Infectious Vesicles

Extracellular vesicles are the Trojan horses of viral infection

Lipid Tales of Viral Replication and Transmission

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