Virus-host interactions: insights from the replication cycle of the large<i>Paramecium bursaria chlorella virus</i>

Milrot, Elad; Mutsafi, Yael; Fridmann-Sirkis, Yael; Shimoni, Eyal; Rechav, Katya; Gurnon, James R.; Etten, James L. Van; Minsky, Abraham

doi:10.1111/cmi.12486

Cited by 34 publications

(50 citation statements)

References 77 publications

(176 reference statements)

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“…4); therefore, when the particle was formed a membrane layer was incorporated into the viral capsid. Other large DNA viruses, such as Paramecium bursaria chlorella virus, African swine fever virus, and APMV, also acquire their inner membranes during the morphogenesis step, but these membranes have different origins (26). Altogether, our results fill in some of the gaps regarding the replication cycle of the marseilleviruses, providing some important biological information about these large viruses.…”

Section: Discussionmentioning

confidence: 66%

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: 66%

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

Arantes

Rodrigues

Silva

et al. 2016

J Virol

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“…2) with a diameter of ~190 nm, which is identical to the diameter measured along the five-fold axis for PBCV-1 (Yan et al, 2000). Another characteristic of PBCV-1 is the presence of an internal, single bilayered membrane that is derived from the host endoplasmic reticulum located near the outer nuclear membrane (Milrot et al, 2016). The membrane is located underneath the outer capsid shell and it is required for virus infectivity because PBCV-1 is sensitive to a short exposure to chloroform (Skrdla et al, 1984).…”

Section: Resultsmentioning

confidence: 99%

Characterization of a new chlorovirus type with permissive and non-permissive features on phylogenetically related algal strains

et al. 2017

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A previous report indicated that prototype chlorovirus PBCV-1 replicated in two Chlorella variabilis algal strains, NC64A and Syngen 2-3, that are ex-endosymbionts isolated from the protozoan Paramecium bursaria. Surprisingly, plaque-forming viruses on Syngen 2-3 lawns were often higher than on NC64A lawns from indigenous water samples. These differences led to the discovery of viruses that exclusively replicate in Syngen 2-3 cells, named Only Syngen (OSy) viruses. OSy-NE5, the prototype virus for the proposed new species, had a linear dsDNA genome of 327 kb with 44-nucleotide-long, incompletely base-paired, covalently closed hairpin ends. Each hairpin structure was followed by an identical 2,612 base-paired inverted sequence after which the DNA sequence diverged. OSy-NE5 encoded 357 predicted CDSs and 13 tRNAs. Interestingly, OSy-NE5 attached to and initiated infection in NC64A cells but infectious progeny viruses were not produced; thus OSy-NE5 replication in NC64A is blocked at some later stage of replication.

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“…The Acanthamoeba polyphaga Mimivirus is a member of the nucleocytoplasmic large DNA viruses (NCLDVs) clade. A notable and characteristic feature of the NCLDVs is the generation of large and elaborate viral factories (VFs) . Mimivirus forms VFs within the host cytoplasm, where viral replication and assembly occur.…”

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confidence: 99%

Kinetics of Mimivirus Infection Stages Quantified Using Image Flow Cytometry

et al. 2019

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Due to the heterogeneity of viruses and their hosts, a comprehensive view of viral infection is best achieved by analyzing large populations of infected cells. However, information regarding variation in infected cell populations is lost in bulk measurements. Motivated by an interest in the temporal progression of events in virally infected cells, we used image flow cytometry (IFC) to monitor changes in Acanthamoeba polyphaga cells infected with Mimivirus . This first use of IFC to study viral infection required the development of methods to preserve morphological features of adherent amoeba cells prior to detachment and analysis in suspension. It also required the identification of IFC parameters that best report on key events in the Mimivirus infection cycle. The optimized IFC protocol enabled the simultaneous monitoring of diverse processes including generation of viral factories, transport, and fusion of replication centers within the cell, accumulation of viral progeny, and changes in cell morphology for tens of thousands of cells. After obtaining the time windows for these processes, we used IFC to evaluate the effects of perturbations such as oxidative stress and cytoskeletal disruptors on viral infection. Accurate dose‐response curves could be generated, and we found that mild oxidative stress delayed multiple stages of virus production, but eventually infection processes occurred with approximately the same amplitudes. We also found that functional actin cytoskeleton is required for fusion of viral replication centers and later for the production of viral progeny. Through this report, we demonstrate that IFC offers a quantitative, high‐throughput, and highly robust approach to study viral infection cycles and virus–host interactions. © The Authors. Cytometry Part A published by Wiley Periodicals, Inc. on behalf of International Society for Advancement of Cytometry.

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Virus-host interactions: insights from the replication cycle of the largeParamecium bursaria chlorella virus

Cited by 34 publications

References 77 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

Characterization of a new chlorovirus type with permissive and non-permissive features on phylogenetically related algal strains

Kinetics of Mimivirus Infection Stages Quantified Using Image Flow Cytometry

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