A silencing suppressor protein (NSs) of a tospovirus enhances baculovirus replication in permissive and semipermissive insect cell lines

Oliveira, Virgínia Carla de; Bartasson, Lorrainy Anastácio; Castro, M. E. B.; Corrêa, José R.; Ribeiro, Bergmann Morais; Resende, Renato O.

doi:10.1016/j.virusres.2010.10.019

Cited by 28 publications

(28 citation statements)

References 57 publications

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“…A recombinant Semliki Forest virus expressing the nonstructural protein NSs, the VSR of TSWV in plant hosts, could suppress silencing in tick cells (53). The NSs of TSWV also enhanced baculovirus replication in lepidopteran cells (54). Furthermore, adults thrips infected with an NSs-defective TSWV isolate carried a significantly lighter viral load, resulting in absence of transmission (55).…”

Section: Discussionmentioning

confidence: 99%

Small Interfering RNA Pathway Modulates Initial Viral Infection in Midgut Epithelium of Insect after Ingestion of Virus

Lan

Chen

Liu

et al. 2016

J Virol

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IMPORTANCE Many viral pathogens that cause significant global health and agricultural problems are transmitted via insect vectors. The first bottleneck in viral infection, the midgut epithelium, is a principal determinant of the ability of an insect species to transmit a virus. Southern rice black streaked dwarf virus (SRBSDV) is restricted exclusively to the midgut epithelium of an incompetent vector, the small brown planthopper (SBPH).Here, we show that silencing of the core component Dicer-2 of the small interfering RNA (siRNA) pathway increases viral titers in the midgut epithelium past the threshold (1.99 ؋ 10 9 copies of the SRBSDV P10 gene/g of midgut RNA) for viral dissemination into the midgut muscles and then into the salivary glands, allowing the SBPH to become a competent vector of SRBSDV. This result is the first evidence that the siRNA antiviral pathway has a direct role in the control of viral dissemination from the midgut epithelium and that it affects the competence of the virus's vector. Many viral pathogens that cause significant global health and agricultural problems are arthropod borne and transmitted via an insect vector. Many plant viruses are transmitted in a persistent manner by sap-sucking insects, including planthoppers, leafhoppers, thrips, and aphids (1-3). Plant viruses, when ingested by their insect vectors, establish their initial infection in the midgut epithelium, from where they disseminate to the midgut visceral muscles (1-3). The viruses then move from the midgut muscles into the hemolymph and finally into the salivary glands, from where they can be introduced into plant hosts (1-3). Efficient viral infection of the midgut epithelium, where initial infection is established, is thus a determinative factor in the ability of an insect species to transmit a certain plant virus.This ability of an insect species to transmit a virus, which has been described as vector competence, is common in nature (4, 5). For many years, the midgut barrier has been believed to be the principal determinant of vector competence (1-9). For example, infection of the incompetent insect vectors of Rice dwarf virus and SRBSDV, two plant reoviruses, and Tomato spotted wilt virus (TSWV), a tospovirus, is restricted to the midgut epithelium (7-10). The inability of incompetent insect vectors to transmit these viruses may be caused by a failure of the virus to efficiently replicate in or disseminate from the midgut epithelium (1-5). It is possible that viral titers in the midgut epithelium of incompetent vectors are unable to reach the threshold needed for viral dissemination. The innate immune response in the midgut epithelium may effectively control viral accumulation, thus blocking viral transmission by incompetent vectors. However, whether the initial antiviral immune pathway(s) in the insect midgut can modulate the competence of plant virus vectors is not unknown.Several mosquito and Drosophila innate immune responses have been reported to have an antiviral effect. These responses include RNA interfere...

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Section: Discussionmentioning

confidence: 99%

Small Interfering RNA Pathway Modulates Initial Viral Infection in Midgut Epithelium of Insect after Ingestion of Virus

Lan

Chen

Liu

et al. 2016

J Virol

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“…A recombinant Semliki Forest virus expressing the NSs of TSWV was able to suppress silencing in tick cells (47). The NSs of TSWV also enhanced baculovirus replication in different lepidopteran cell lines (48) as well as in insects in vivo (R. Oliveira Resende, Universidade de Brasilia, personal communication). A role for the TSWV NSs protein in suppressing silencing in both plant and insect hosts is also supported by the ability of the homologous NS3 protein of Rice hoja blanca tenuivirus (a phylogenetically related virus) to bind to siRNA and microRNA (miRNA) in both hosts (49,50).…”

Section: Effects Of Deletion In the Nss Coding Region On Virus Titer mentioning

confidence: 99%

The NSs Protein of Tomato spotted wilt virus Is Required for Persistent Infection and Transmission by Frankliniella occidentalis

Margaria¹,

Bosco

Vallino³

et al. 2014

J Virol

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Tomato spotted wilt virus (TSWV) is the type member of tospoviruses (genus Tospovirus), plant-infecting viruses that cause severe damage to ornamental and vegetable crops. Tospoviruses are transmitted by thrips in the circulative propagative mode. We generated a collection of NSs-defective TSWV isolates and showed that TSWV coding for truncated NSs protein could not be transmitted by Frankliniella occidentalis. Quantitative reverse transcription (RT)-PCR and immunostaining of individual insects detected the mutant virus in second-instar larvae and adult insects, demonstrating that insects could acquire and accumulate the NSs-defective virus. Nevertheless, adults carried a significantly lower viral load, resulting in the absence of transmission. Genome sequencing and analyses of reassortant isolates showed genetic evidence of the association between the loss of competence in transmission and the mutation in the NSs coding sequence. Our findings offer new insight into the TSWV-thrips interaction and Tospovirus pathogenesis and highlight, for the first time in the Bunyaviridae family, a major role for the S segment, and specifically for the NSs protein, in virulence and efficient infection in insect vector individuals. IMPORTANCEOur work is the first to show a role for the NSs protein in virus accumulation in the insect vector in the Bunyaviridae family: demonstration was obtained for the system TSWV-F. occidentalis, arguably one of the most damaging combination for vegetable crops. Genetic evidence of the involvement of the NSs protein in vector transmission was provided with multiple approaches.

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“…This limitation led us to focus on the RNAi suppressors that have the potential to enhance baculovirus yield in insects (Oliveiraa et al 2011). P19 protein derived from tombusvirus (TBSV) is a strong suppressor of induced RNA silencing not only in nonendogenous host plant cells (Qu and Morris 2002;Siddiqui et al 2008) but also in animal cells such as Drosophila, Drosophila embryo extracts and Yangkun Liu and Lei Zhang have contributed equally to this work.…”

Section: Introductionmentioning

confidence: 99%

Functional analysis of RNAi suppressor P19 on improving baculovirus yield and transgene expression in Sf9 cells

Liu

Zhang

et al. 2015

Biotechnol Lett

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A silencing suppressor protein (NSs) of a tospovirus enhances baculovirus replication in permissive and semipermissive insect cell lines

Cited by 28 publications

References 57 publications

Small Interfering RNA Pathway Modulates Initial Viral Infection in Midgut Epithelium of Insect after Ingestion of Virus

Small Interfering RNA Pathway Modulates Initial Viral Infection in Midgut Epithelium of Insect after Ingestion of Virus

The NSs Protein of Tomato spotted wilt virus Is Required for Persistent Infection and Transmission by Frankliniella occidentalis

Functional analysis of RNAi suppressor P19 on improving baculovirus yield and transgene expression in Sf9 cells

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