Viral Infection and Stress Affect Protein Levels of Dicer 2 and Argonaute 2 in Drosophila melanogaster

Torri, Alessandro; Mongelli, Vanesa; Mondotte, Juan A.; Saleh, Maria-Carla

doi:10.3389/fimmu.2020.00362

Cited by 8 publications

(7 citation statements)

References 51 publications

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“…RNAi-mediated knockdown of Ago2, a component of the RISC complex ( Song and Joshua-Tor 2006 ), and Dcr2, a ribonuclease involved in siRNA synthesis ( Elbashir et al 2001 ), was successfully conducted in the western corn rootworm, Diabrotica virgifera virgifera (Coleoptera: Chrysomelidae) and mitigated the effects of lethal dsRNA consumption ( Vélez et al 2016 ). Protein levels of the former were increased following viral infection in D. melanogaster ( Torri et al 2020 ) while the latter has notably been associated with a role in stress defense in D. melanogaster ( Lim et al 2011 ) further supporting their likely relevance in stress mitigation. Even though RNAi-mediated Ago2 knockdown has been reported before in lepidopterans such as the European corn borer Ostrinia nubilalis (Lepidoptera: Crambidae) ( Cooper et al 2021 ), modulation of Ago2 to investigate its potential role in cold response has not been reported in L. decemlineata prior to this work.…”

Section: Discussionmentioning

confidence: 88%

“…Further investigation is thus envisioned to better delineate, if any, the function of Ago2 and other transcripts relevant to small RNA biogenesis for cold and heat adaptation in this potato pest. Given that Ago2 protein levels have been reported as modulated in conditions not evaluated here, such as infection procedure-related stress ( Torri et al 2020 ), status of targets of interest in additional stress should also be considered. Additional work to assess the optimal window to conduct cold and heat treatments in dsRNA-injected L. decemlineata would also be of interest.…”

Section: Discussionmentioning

confidence: 99%

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Exposure to Temperature and Insecticides Modulates the Expression of Small Noncoding RNA-Associated Transcripts in the Colorado Potato Beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

Youssef

Ouédraogo

Bastarache

et al. 2022

Journal of Insect Science

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The Colorado potato beetle (Leptinotarsa decemlineata (Say)) is an insect that can adapt to various challenges, including temperature fluctuations or select insecticide treatments. This pest is also an ongoing threat to the potato industry. Small noncoding RNAs such as miRNAs, which can control posttranscriptionally the expression of various genes, and piRNAs, which can notably impact mRNA turnover, are modulated in insects under different conditions. Unfortunately, information regarding the expression status of key players involved in their synthesis and function is for the most part lacking. The current study thus aims at assessing the levels of such targets in L. decemlineata exposed to hot and cold temperatures as well as treated to the insecticides chlorantraniliprole, clothianidin, imidacloprid, and spinosad. Transcript expression levels of Ago1, Ago2, Ago3, Dcr2a, Dcr2b, Expo-5, Siwi-1, and Siwi-2, components of pathways associated with small noncoding RNA production or function, were measured by qRT-PCR and revealed modulation of select transcripts in response to temperature challenges and to select insecticides. RNAi-mediated reduction of Ago2 transcript levels in L. decemlineata injected with Ago2-targeting dsRNA and exposed to cold and warm temperatures was also conducted. Changes in survival rates were observed for the latter condition in dsRNA- versus saline-injected insects. These results showcase the differential expression of select targets involved in small noncoding RNA homeostasis and provide leads for the subsequent assessment of their involvement during stress response in L. decemlineata using RNAi-based approaches.

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Section: Discussionmentioning

confidence: 88%

Section: Discussionmentioning

confidence: 99%

Exposure to Temperature and Insecticides Modulates the Expression of Small Noncoding RNA-Associated Transcripts in the Colorado Potato Beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

Youssef

Ouédraogo

Bastarache

et al. 2022

Journal of Insect Science

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“…The impact of viral infection on the siRNA and Argonaute /PIWI pathway has mainly been reported in insects [47,48]. However, little is known regarding genes and proteins involved in this insect Ago-2/RNAi antiviral/stress defense response [49].…”

Section: Discussionmentioning

confidence: 99%

PIWI silencing mechanism involving the retrotransposon nimbus orchestrates resistance to infection with Schistosoma mansoni in the snail vector, Biomphalaria glabrata

et al. 2021

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Background Schistosomiasis remains widespread in many regions despite efforts at its elimination. By examining changes in the transcriptome at the host-pathogen interface in the snail Biomphalaria glabrata and the blood fluke Schistosoma mansoni, we previously demonstrated that an early stress response in juvenile snails, manifested by induction of heat shock protein 70 (Hsp 70) and Hsp 90 and of the reverse transcriptase (RT) domain of the B. glabrata non-LTR- retrotransposon, nimbus, were critical for B. glabrata susceptibility to S. mansoni. Subsequently, juvenile B. glabrata BS-90 snails, resistant to S. mansoni at 25°C become susceptible by the F2 generation when maintained at 32°C, indicating an epigenetic response. Methodology/Principal findings To better understand this plasticity in susceptibility of the BS-90 snail, mRNA sequences were examined from S. mansoni exposed juvenile BS-90 snails cultured either at 25°C (non-permissive temperature) or 32°C (permissive). Comparative analysis of transcriptomes from snails cultured at the non-permissive and permissive temperatures revealed that whereas stress related transcripts dominated the transcriptome of susceptible BS-90 juvenile snails at 32°C, transcripts encoding proteins with a role in epigenetics, such as PIWI (BgPiwi), chromobox protein homolog 1 (BgCBx1), histone acetyltransferase (BgHAT), histone deacetylase (BgHDAC) and metallotransferase (BgMT) were highly expressed in those cultured at 25°C. To identify robust candidate transcripts that will underscore the anti-schistosome phenotype in B. glabrata, further validation of the differential expression of the above transcripts was performed by using the resistant BS-90 (25°C) and the BBO2 susceptible snail stock whose genome has now been sequenced and represents an invaluable resource for molecular studies in B. glabrata. A role for BgPiwi in B. glabrata susceptibility to S. mansoni, was further examined by using siRNA corresponding to the BgPiwi encoding transcript to suppress expression of BgPiwi, rendering the resistant BS-90 juvenile snail susceptible to infection at 25°C. Given transposon silencing activity of PIWI as a facet of its role as guardian of the integrity of the genome, we examined the expression of the nimbus RT encoding transcript at 120 min after infection of resistant BS90 piwi-siRNA treated snails. We observed that nimbus RT was upregulated, indicating that modulation of the transcription of the nimbus RT was associated with susceptibility to S. mansoni in BgPiwi-siRNA treated BS-90 snails. Furthermore, treatment of susceptible BBO2 snails with the RT inhibitor lamivudine, before exposure to S. mansoni, blocked S. mansoni infection concurrent with downregulation of the nimbus RT transcript and upregulation of the BgPiwi encoding transcript in the lamivudine-treated, schistosome-exposed susceptible snails. Conclusions and significance These findings support a role for the interplay of BgPiwi and nimbus in the epigenetic modulation of plasticity of resistance/susceptibility in the snail-schistosome relationship.

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“…However, little is known regarding genes and proteins involved in this insect Ago-2/RNAi antiviral/stress defense response [49]. glabrata endogenous non-LTR-retrotransposable element, nimbus, was linked to the early differential stress response observed between juvenile resistant and susceptible snails [18].…”

Section: Discussionmentioning

confidence: 99%

PIWI silencing mechanism involving the retrotransposonnimbusorchestrates resistance to infection withSchistosoma mansoniin the snail vector,Biomphalaria glabrata

Smith

Yadav

Akinyele

et al. 2021

Preprint

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BackgroundSchistosomiasis remains widespread in many regions despite efforts at its elimination. By examining changes in the transcriptome at the host-pathogen interface in the snail Biomphalaria glabrata and the blood fluke Schistosoma mansoni, we previously demonstrated that an early stress response in juvenile snails, manifested by induction of heat shock protein 70 (Hsp 70) and Hsp 90 and of the reverse transcriptase (RT) domain of the B. glabrata non-LTR-retrotransposon, nimbus, were critical for B. glabrata susceptibility to S. mansoni. Subsequently, juvenile B. glabrata BS90 snails, resistant to S. mansoni at 25°C become susceptible by the F2 generation when maintained at 32°C, indicating an epigenetic response.Methodology/Principal FindingsTo better understand this plasticity in susceptibility of the BS90 snail, mRNA sequences were examined from S. mansoni exposed juvenile BS90 snails cultured either at 25°C (permissive temperature) or 32°C (non-permissive). Comparative analysis of transcriptomes from snails cultured at the non-permissive and permissive temperatures revealed that whereas stress related transcripts dominated the transcriptome of susceptible BS90 juvenile snails at 32°C, transcripts encoding proteins with a role in epigenetics, such as PIWI (BgPiwi), chromobox protein homolog 1 (BgCBx1), histone acetyl transferase histone deacetylase (HDAC) and metallotransferase (MT) were highly expressed in those cultured at 25°C. To further determine a role for BgPiwi in B. glabrata susceptibility to S. mansoni, siRNA corresponding to the BgPiwi encoding transcript was utilized to suppress expression of BgPiwi, rendering the resistant BS90 juvenile snail susceptible to infection at 25°C. Given transposon silencing activity of PIWI as a facet of its role as guardian of the integrity of the genome, we examined the expression of the nimbus RT encoding transcript at 120 min after infection of resistant BS90 piwi-siRNA treated snails. We observed that nimbus RT was upregulated, indicating that modulation of the transcription of the nimbus RT was associated with susceptibility to S. mansoni in BgPiwi- siRNA treated BS90 snails. Furthermore, treatment of susceptible snails with the RT inhibitor lamivudine, before exposure to S. mansoni, blocked S. mansoni infection concurrent with downregulation of the nimbus RT transcript and upregulation of the BgPiwi encoding transcript in the lamivudine-treated, schistosome-exposed susceptible snails.Conclusions and SignificanceThese findings support a role for the interplay of BgPiwi and nimbus in the epigenetic modulation of plasticity of resistance/susceptibility in the snail-schistosome relationship.

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Viral Infection and Stress Affect Protein Levels of Dicer 2 and Argonaute 2 in Drosophila melanogaster

Cited by 8 publications

References 51 publications

Exposure to Temperature and Insecticides Modulates the Expression of Small Noncoding RNA-Associated Transcripts in the Colorado Potato Beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

Exposure to Temperature and Insecticides Modulates the Expression of Small Noncoding RNA-Associated Transcripts in the Colorado Potato Beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

PIWI silencing mechanism involving the retrotransposon nimbus orchestrates resistance to infection with Schistosoma mansoni in the snail vector, Biomphalaria glabrata

PIWI silencing mechanism involving the retrotransposonnimbusorchestrates resistance to infection withSchistosoma mansoniin the snail vector,Biomphalaria glabrata

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