Small RNA responses of Culex mosquitoes and cell lines during acute and persistent virus infection

Rückert, Claudia; Prasad, Abhishek N.; Garcia-Luna, Selene; Robison, Alexis; Grubaugh, Nathan D.; Weger-Lucarelli, James; Ebel, Gregory D.

doi:10.1016/j.ibmb.2019.04.008

Cited by 47 publications

(77 citation statements)

References 72 publications

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“…The production of different types of small RNAs is in agreement with previous studies on Aedes or Culex mosquito cell lines persistently infected with ISVs showing production of ISV-derived siRNAs and/or piRNAs [28, 30, 32]. While vsiRNA production was observed for all three ISVs, vpiRNAs with a clear ping-pong signature were only derived from MERV in both reproductive tissues and carcasses.…”

Section: Discussionsupporting

confidence: 90%

“…While vsiRNA production was observed for all three ISVs, vpiRNAs with a clear ping-pong signature were only derived from MERV in both reproductive tissues and carcasses. Previous studies in Aedes and Culex mosquito cell lines [28, 30, 48, 49] showed that infection with Phasi Charoen-like virus ( Phenuiviriade) , Merida virus ( Rhabdoviridae ), La Crosse virus, and Rift Valley fever virus (both Bunyaviridae ), all of them negative-sense single-stranded viruses, produce vpiRNAs with ping-pong signature. In addition, both primary and secondary vpiRNAs were generated from some alphaviruses, positive-sense single-stranded virus, such as SINV, SFV and chikungunya virus in vitro and/or in vivo in Aedes mosquitoes [15, 26, 27, 48, 50].…”

Section: Discussionmentioning

confidence: 99%

“…Cx. quinquefasciatus cell lines infected with Merida virus, also a rhabdovirus, showed a similar vpiRNA profile, suggesting that the regions that generate vpiRNAs are conserved regardless of the mosquito species and depend on the viral replication strategy [30]. Rhabdoviruses, in general, transcribe their mRNA from the 3’ UTR, which is closer to structural genes.…”

Section: Discussionmentioning

confidence: 99%

“…Due to their mode of transmission, ISVs provide a great opportunity to better understand the mosquito antiviral response in females as well as in males, especially the antiviral responses such as the piRNA pathway in reproductive organs and germ line. To date, studies on ISV-derived small RNA production have been limited to mosquito cell lines [28, 30]. Here, we investigated the small RNA responses to ISVs in individual mosquitoes.…”

Section: Introductionmentioning

confidence: 99%

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Differential small RNA responses against co-infecting insect-specific viruses inAedes albopictusmosquitoes

Frangeul

Blanc

Saleh

et al. 2020

Preprint

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AbstractThe mosquito antiviral response has been mainly studied in the case of arthropod-borne virus (arbovirus) infection in female mosquitoes. However, in nature, both female and male mosquitoes are abundantly infected with insect-specific viruses (ISVs). ISVs are capable of infecting the reproductive organs of both sexes and are maintained primarily by vertical transmission. Since the RNA interference (RNAi)-mediated antiviral response plays an important antiviral role in mosquitoes, ISVs constitute a relevant model to study sex-dependent antiviral responses. Using a naturally generated viral stock containing three distinct ISVs, Aedes flavivirus (AEFV), Menghai Rhabdovirus (MERV) and Shinobi tetra virus (SHTV), we infected adult Aedes albopictus females and males and generated small RNA libraries from ovaries, testes, and the remainder of the body. Overall, both female and male mosquitoes showed unique small RNA profiles to each co-infecting ISV regardless the sex or tissue tested. While all three ISVs generated virus-derived siRNAs, only MERV generated virus-derived piRNAs. We also studied the expression of PIWI genes in reproductive tissues and carcasses. Piwi1-4 were abundantly expressed in ovaries and testes in contrast to Piwi5-9, suggesting that Piwi 5-9 are involved in exogenous viral piRNA production. Together, our results show that ISV-infected Aedes albopictus produce viral small RNAs in a virus-specific manner and that male mosquitoes mount a similar small RNA-mediated antiviral response to that of females.

show abstract

Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

Differential small RNA responses against co-infecting insect-specific viruses inAedes albopictusmosquitoes

Frangeul

Blanc

Saleh

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…Secondary piRNAs are produced by cleavage of complementary transcripts directed by primary piRNAs and often contain an adenine at the 10th nucleotide position, called the 10A bias. In addition to piRNA cluster-derived piRNAs, mosquitoes have been shown to produce viral piRNAs (vpiRNAs) from different replicating viruses such as flaviviruses, alphaviruses and rhabdoviruses [15,[26][27][28][29][30][31][32]. This is in contrast with Drosophila melanogaster, where vpiRNAs are not produced during virus infections [33].…”

Section: Introductionmentioning

confidence: 99%

Differential Small RNA Responses against Co-Infecting Insect-Specific Viruses in Aedes albopictus Mosquitoes

Frangeul

Blanc

Saleh

et al. 2020

Viruses

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The mosquito antiviral response has mainly been studied in the context of arthropod-borne virus (arbovirus) infection in female mosquitoes. However, in nature, both female and male mosquitoes are frequently infected with insect-specific viruses (ISVs). ISVs are capable of infecting the reproductive organs of both sexes and are primarily maintained by vertical transmission. Since the RNA interference (RNAi)-mediated antiviral response plays an important antiviral role in mosquitoes, ISVs constitute a relevant model to study sex-dependent antiviral responses. Using a naturally generated viral stock containing three distinct ISVs, Aedes flavivirus (AEFV), Menghai rhabdovirus (MERV), and Shinobi tetra virus (SHTV), we infected adult Aedes albopictus females and males and generated small RNA libraries from ovaries, testes, and the remainder of the body. Overall, both female and male mosquitoes showed unique small RNA profiles to each co-infecting ISV regardless of the sex or tissue tested. While all three ISVs generated virus-derived siRNAs, only MERV generated virus-derived piRNAs. We also studied the expression of PIWI genes in reproductive tissues and carcasses. In contrast to Piwi5-9, Piwi1-4 were abundantly expressed in ovaries and testes, suggesting that Piwi5-9 are involved in exogenous viral piRNA production. Together, our results show that ISV-infected Aedes albopictus produce viral small RNAs in a virus-specific manner and that male mosquitoes mount a similar small RNA-mediated antiviral response to that of females.

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PIWI pathway against viruses in insects

et al. 2019

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Piwi-interacting RNAs (piRNAs) are an animal-specific class of small non-coding RNAs that are generated via a biogenesis pathway distinct from small interfering RNAs (siRNAs) and microRNAs (miRNAs). There are variations in piRNA biogenesis that depend on several factors, such as the cell type (germline or soma), the organism, and the purpose for which they are being produced, such as transposontargeting, viral-targeting, or gene-derived piRNAs. Interestingly, the genes involved in the PIWI/piRNA pathway are more rapidly evolving compared with other RNA interference (RNAi) genes. In this review, the role of the piRNA pathway in the antiviral response is reviewed based on recent findings in insect models such as Drosophila, mosquitoes, midges and the silkworm, Bombyx mori. We extensively discuss the special features that characterize host-virus piRNA responses with respect to the proteins and the genes involved, the viral piRNAs' sequence characteristics, the target strand orientation biases as well as the viral piRNA target hotspots across the viral genomes.

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Small RNA responses of Culex mosquitoes and cell lines during acute and persistent virus infection

Cited by 47 publications

References 72 publications

Differential small RNA responses against co-infecting insect-specific viruses inAedes albopictusmosquitoes

Differential small RNA responses against co-infecting insect-specific viruses inAedes albopictusmosquitoes

Differential Small RNA Responses against Co-Infecting Insect-Specific Viruses in Aedes albopictus Mosquitoes

PIWI pathway against viruses in insects

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