The growth of Semliki Forest virus in cultured mosquito cells: Ultrastructural observations

Raghow, Rajendra; Davey, Mary W.; Dalgarno, L.

doi:10.1007/bf01249360

Cited by 25 publications

(13 citation statements)

References 5 publications

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“…It is well known that the outcome of infection is fundamentally different between the two hosts, as mammalian infection is acute whereas arthropod infection creates a persistent infection (5,6,(8)(9)(10)(40)(41)(42). Perhaps these differences between the host species, for instance, the shutoff of host macromolecular synthesis, are a determinant of noncapped viral RNA production.…”

Section: Discussionmentioning

confidence: 99%

Noncapped Alphavirus Genomic RNAs and Their Role during Infection

Sokoloski

Haist

Morrison

et al. 2015

J Virol

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Alphaviruses are enveloped positive-sense RNA viruses that exhibit a wide host range consisting of vertebrate and invertebrate species. Previously we have reported that the infectivity of Sindbis virus (SINV), the model alphavirus, was largely a function of the cell line producing the viral particles. Mammalian-cell-derived SINV particles, on average, exhibit a higher particle-to-PFU ratio than mosquito cell-derived SINV particles. Nevertheless, the outcome of nonproductive infection, the molecular traits that determine particle infectivity and the biological importance of noninfectious particles were, prior to this study, unknown. Here, we report that the incoming genomic RNAs of noninfectious SINV particles undergo rapid degradation following infection. Moreover, these studies have led to the identification of the absence of the 5= cap structure as a primary molecular determinant of particle infectivity. We show that the genomic RNAs of alphaviruses are not universally 5= capped, with a significant number of noncapped genomic RNA produced early in infection. The production of noncapped viral genomic RNAs is important to the establishment and maintenance of alphaviral infection. IMPORTANCEThis report is of importance to the field of virology for three reasons. First, these studies demonstrate that noncapped Sindbis virus particles are produced as a result of viral RNA synthesis. Second, this report is, to our knowledge, the first instance of the direct measurement of the half-life of an incoming genomic RNA from a positive-sense RNA virus. Third, these studies indicate that alphaviral infection is likely a concerted effort of infectious and noninfectious viral particles.A lphaviruses are enveloped, positive-sense RNA viruses that are cyclically transmitted between sylvatic vertebrate reservoir hosts and a mosquito vector during the enzootic cycle. The maintenance of this cyclical transmission is vital to viral fitness, as prolonged serial passage within a single host results in attenuation in the alternate host (1-4). Moreover, the ultimate outcome of alphaviral infection differs between vertebrate and invertebrate hosts, as infection of a vertebrate host results in acute cytolytic infection whereas infection of invertebrate hosts often results in persistent infection with minimal cell death (5-11). The widespread geographic distribution of competent vector mosquito species leading to contact with immunologically naive human populations has resulted in several significant outbreaks of alphaviral disease (12)(13)(14). Perhaps most notable is the ongoing reemergence of chikungunya virus, which caused significant morbidity during the height of the 2006 epidemic, with as many as 40,000 new cases per week (13).Despite the range of diseases and morbidity associated within the genus, the underlying molecular life cycles are highly similar in the two hosts. Since alphaviruses are positive-sense RNA viruses, they function similarly to cellular mRNAs, relying on the translation of the incoming viral genome to ini...

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Section: Discussionmentioning

confidence: 99%

Noncapped Alphavirus Genomic RNAs and Their Role during Infection

Sokoloski

Haist

Morrison

et al. 2015

J Virol

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“…Togaviruses are maintained in nature as a result of transmission between vertebrate hosts by haemophagous arthropods; they multiply in both their vertebrate and invertebrate hosts (Dalgarno & Davey, 1973). Infection of cultured vertebrate cells by alphaviruses is generally cytopathic, whereas infection of cultured mosquito cells generally results in a persistent infection with little evidence of c.p.e.…”

Section: Introductionmentioning

confidence: 99%

“…In contrast, Enzmann (I973) concluded that the maintenance of the cell-virus equilibrium in Sindbis-infected Aedes albopictus cells was related to the presence of interferon-like substances. Ultrastructural studies show that during SFV and Ross River virus (RRV) infection of cultured A. albopictus cells, virus maturation may occur both at the cell membrane and within dense, membrane-bound, cytoplasmic inclusions (Raghow, Davey & Dalgarno, 1973 a;Raghow et al ~ 973 b). This is noteworthy since a characteristic feature of the mumps virus carrier state in mammalian cells is the localization of virus-specific antigens in a small number of discrete, cytoplasmic masses (Walker & Hinze,I962).…”

Section: Introductionmentioning

confidence: 99%

Semliki Forest Virus Replication in Cultured Aedes albopictus Cells: studies on the Establishment of Persistence

Davey

Dalgarno

1974

Journal of General Virology

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SUMMARY Semliki Forest virus (SFV) established a persistent, non-cytopathic infection incultured Aedes albopictus cells with no effect on cumulative cell number as compared with control cultures. All cells were initially infected by SFV as judged by infective centre and immunofluorescence assay and released approx. 5o to 7o p.f.u./cell in the initial a4 h after infection. At 12 h after infection there was a 'shut-down' of virus-specific RNA synthesis followed by a sharp decline in the percentage of cells infected, stabilizing at about 2 % by 48 h. Significant amounts of virus were released from about 2 % of cells in persistently infected cultures. At 8 to lO days a small-plaque, attenuated variant of SFV appeared in infected cultures; it replaced 'wild-type' virus completely by day 16.The establishment of persistence could not be related to (i) the release of interferon-like activity from infected cells, (ii) the presence of a directly antiviral agent in infected cells or medium, or (iii) changes in the total levels or subcellular distribution of acid phosphatase.Subculturing persistently infected cells stimulated cell division and promoted a (reduced) burst of virus production; simultaneous superinfection with SFV gave no increase in virus yields.

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“…The outcome of alphaviral infection is dependent on the host system (6)(7)(8)(9)(10)(11)(12). Infection of mosquito cells does not result in the shutoff of host macromolecular synthesis and often culminates in persistent infection for the majority of mosquito cell lines (12)(13)(14)(15). Nevertheless, cell death as a result of infection has been reported for several members of the genus in whole mosquitoes (16)(17)(18)(19)(20)(21).…”

mentioning

confidence: 99%

Encapsidation of Host-Derived Factors Correlates with Enhanced Infectivity of Sindbis Virus

Sokoloski

Snyder²,

Liu

et al. 2013

J Virol

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The genus Alphavirus consists of a group of enveloped, single-stranded RNA viruses, many of which are transmitted by arthropods to a wide range of vertebrate host species. Here we report that Sindbis virus (SINV) produced from a representative mammalian cell line consists of at least two unique particle subpopulations, separable on the basis of virion density. In contrast, mosquito-derived SINV consists of a homogeneous population of particles. Our findings indicate that the denser particle subpopulation, SINV Heavy , is more infectious on a per-particle basis than SINV Light . SINV produced in mosquito cell lines (SINV C6/36 ) exhibited particle-to-PFU ratios similar to those observed for SINV Heavy . In mammalian cells, viral RNA was synthesized and accumulated more rapidly following infection with SINV Heavy or SINV C6/36 than following infection with SINV Light , due partly to enhanced translation of viral genomic RNA early in infection. Analysis of the individual particle subpopulations indicated that SINV Heavy and SINV C6/36 contain host-derived factors whose presence correlates with the enhanced translation, RNA synthesis, and infectivity observed for these particles. Members of the genus Alphavirus, of the family Togaviridae, are a group of enveloped positive-sense RNA viruses with a wide host range. For the mosquito-borne species, the virus is maintained in the enzootic cycle through transmission between a sylvatic reservoir and the mosquito host (1). The maintenance of this cycle directly affects the genetic fitness of the mosquito-borne alphaviruses. Prolonged disruption of this cycle leads to deleterious effects on viral transmission as the virus becomes adapted to a single host (2-5). Spillover from the enzootic cycle often results in the tangential infection of both humans and equines, which can result in significant outbreaks of disease. The outcome of alphaviral infection is dependent on the host system (6-12). Infection of mosquito cells does not result in the shutoff of host macromolecular synthesis and often culminates in persistent infection for the majority of mosquito cell lines (12-15). Nevertheless, cell death as a result of infection has been reported for several members of the genus in whole mosquitoes (16)(17)(18)(19)(20)(21). In contrast, infection of mammalian cells induces the shutoff of host macromolecular synthesis, resulting in a predominantly cytolytic infection. In vertebrates, the immune response to infection generally results in virus clearance. This is initiated by the recognition of viral doublestranded RNA and a rapid type I interferon (IFN-␣/␤) response (22)(23)(24)(25).Previously, we reported that the infectivity of Sindbis virus (SINV), as measured by the ratio of particles to infectious units, depends on the host cell line from which it is derived (26). SINV derived from mammalian cell lines exhibited a higher particle-to-PFU ratio, on average, than SINV generated from mosquito cell lines. This was due largely to differences in the quantity of total virus particles pr...

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The growth of Semliki Forest virus in cultured mosquito cells: Ultrastructural observations

Cited by 25 publications

References 5 publications

Noncapped Alphavirus Genomic RNAs and Their Role during Infection

Noncapped Alphavirus Genomic RNAs and Their Role during Infection

Semliki Forest Virus Replication in Cultured Aedes albopictus Cells: studies on the Establishment of Persistence

Encapsidation of Host-Derived Factors Correlates with Enhanced Infectivity of Sindbis Virus

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