Vesicle-Cloaked Virus Clusters Are Optimal Units for Inter-organismal Viral Transmission

Santiana, Marianita; Ghosh, Sourish; Ho, Brian A.; Rajasekaran, Vignesh; Du, Wenli; Mutsafi, Yael; Jesús-Díaz, Dennise A. de; Sosnovtsev, Stanislav V.; Levenson, Eric A.; Parra, Gabriel I.; Takvorian, Peter M.; Cali, Ann; Bleck, Christopher K. E.; Vlasova, Anastasia N.; Saif, Linda J.; Patton, John T.; Lopalco, Patrizia; Corcelli, Angela; Green, Kim Y.; Altan‐Bonnet, Nihal

doi:10.1016/j.chom.2018.07.006

Cited by 235 publications

(344 citation statements)

References 56 publications

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“…Recent work has revealed several distinct mechanisms by which multiple viral genomes are co-delivered to a target cell 4–8 . Various mechanisms of direct cell-to-cell spread yield a similar outcome 9–11 .…”

Section: Introductionmentioning

confidence: 99%

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Collective interactions augment influenza A virus replication in a host-dependent manner

Phipps

Ganti

Jacobs

et al. 2019

Preprint

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22implicated the PA gene segment as a major driver of this phenotype and quantification of viral 33RNA synthesis indicated that both replication and transcription were affected. These findings 34 indicate that multiple distinct mechanisms underlie IAV reliance on multiple infection and 35 underscore the importance of virus-virus interactions in IAV infection, evolution and emergence. 36Importantly, multiple infection with identical viral genomes can also alter infection 58 outcomes. Such cooperation was documented for VSV and HIV, where rates of transcription and 59 replication were enhanced with increasing multiplicity of infection (MOI) 23,24 . Similarly, faster 60 kinetics of virus production were seen at high MOI for poliovirus and IAV 19,25 . In these instances, 61 it is thought that increased copy number of infecting viral genomes provides a kinetic benefit 62 important in the race to establish infection before innate antiviral responses take hold. Indeed, it 63 has been suggested that multiple infection may be particularly relevant for facilitating viral growth 64 under adverse conditions, such as antiviral drug treatment 3,26 . 65For IAV, an important adverse condition to consider is that of a novel host environment. 66IAVs occupy a broad host range, including multiple species of wild waterfowl, poultry, swine, 67 humans and other mammals 27,28 . Host barriers to infection typically confine a given lineage to 68 circulation in one species or a small number of related species 29,30 . Spillovers occur occasionally, 69 however, and can seed novel lineages. When a novel IAV lineage is established in humans, the 70 result is a pandemic of major public health consequence 31,32 . The likelihood of successful cross-71 species transfer of IAV is determined largely by the presence, absence, and compatibility of host 72 factors on which the virus relies to complete its life cycle, and on the viruses' ability to overcome 73 antiviral defenses in the novel host [33][34][35] . 74Our objective herein was to assess the degree to which IAV relies on the delivery of 75 multiple viral genomes to a cell to ensure production of progeny. In particular, we sought to 76 determine whether this phenotype varies with host species. We therefore examined the 77 multiplicity dependence of one human and a panel of avian-origin viruses in multiple host systems. 78Results from all virus/cell combinations tested confirm prior reports that cells multiply-infected with 79 IAV produce more viral progeny than singly-infected cells. Importantly, however, the extent to 80 which viral progeny production is concentrated within the multiply-infected fraction of a cell 81 population varies greatly with virus-host context. Two poultry-adapted H9N2 viruses (A/guinea 82 fowl/HK/WF10/99 (GFHK99) and A/quail/HK/A28945/88 (QaHK88)) exhibit an acute dependence 83 on multiple infection in mammalian systems that is greatly diminished in natural host systems. 84This strong dependence on multiple infection is not seen for the human strain, influenza 85 ...

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Section: Introductionmentioning

confidence: 99%

“…The implications of multiple infection in these diverse systems are still being explored. In a number of cases, however, collective delivery was demonstrated to increase the efficiency of infection relative to free virus particles 4, 5 , or to increase the rate of genetic exchange through recombination 6 .…”

Section: Introductionmentioning

confidence: 99%

Collective interactions augment influenza A virus replication in a host-dependent manner

Phipps

Ganti

Jacobs

et al. 2019

Preprint

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“…Our models have assumed that CIUs evolve due to the benefits of collective transmission. However, an alternative possibility is that collective transmission could be a by-product of selection for infectious units that are favoured for other reasons, such as increased infectivity or particle stability (Sanjuán 2017; Santiana et al 2018). In that case, collective infection would be a consequence, but not a cause, of the evolution of CIUs, and so different kinds of explanations would be required to explain when CIUs evolve in nature.…”

Section: R a F Tmentioning

confidence: 99%

The evolution of collective infectious units in viruses

Leeks

Sanjuán

West

2019

Preprint

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Viruses frequently spread among cells or hosts in groups, with multiple viral genomes inside the same infectious unit. These collective infectious units can consist of multiple viral genomes inside the same virion, or multiple virions inside a larger structure such as a vesicle. Collective infectious units deliver multiple viral genomes to the same cell simultaneously, which can have important implications for viral pathogenesis, antiviral resistance, and social evolution. However, little is known about why some viruses transmit in collective infectious units, whereas others do not. We used a simple evolutionary approach to model the potential costs and benefits of transmitting in a collective infectious unit. We found that collective infectious units could be favoured if cells infected by multiple viral genomes were significantly more productive than cells infected by just one viral genome, and especially if there were also efficiency benefits to packaging multiple viral genomes inside the same infectious unit. We also found that if some viral sequences are defective, then collective infectious units could evolve to become very large, but that if these defective sequences interfered with wild-type virus replication, then collective infectious units were disfavoured.

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“…Recent studies suggest instead that enteric viruses travel in groups (5). In particular, they cluster i) in vesicles with inverted phosphatidilserine (PS) topology (6,7), and ii) at the surface of selected bacterial species (8,9). Both mechanisms promote the concentration of viral particles at the surface of the epithelial monolayer of the GI tract, in turn increasing locally the multiplicity of infection and the chances of a successful infection.…”

Section: Novel Concepts In Enteric Virus Infection Open Avenues For Tmentioning

confidence: 99%

“…Both mechanisms promote the concentration of viral particles at the surface of the epithelial monolayer of the GI tract, in turn increasing locally the multiplicity of infection and the chances of a successful infection. In addition, a recent report suggests that viruscloaked vesicles are also found in stools and those confer an advantage also in viral transmission (7).…”

Section: Novel Concepts In Enteric Virus Infection Open Avenues For Tmentioning

confidence: 99%

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2018

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Vesicle-Cloaked Virus Clusters Are Optimal Units for Inter-organismal Viral Transmission

Cited by 235 publications

References 56 publications

Collective interactions augment influenza A virus replication in a host-dependent manner

Collective interactions augment influenza A virus replication in a host-dependent manner

The evolution of collective infectious units in viruses

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