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Viruses rely on host cell metabolism to provide the necessary energy and biosynthetic precursors for successful viral replication. Infection of the silkworm, Bombyx mori, by Bombyx mori nucleopolyhedrovirus (BmNPV), has been studied extensively in the past to unravel interactions between baculoviruses and their lepidopteran hosts. To understand the interaction between the host metabolic responses and BmNPV infection, we analyzed global metabolic changes associated with BmNPV infection in silkworm hemolymph. Our metabolic profiling data suggests that amino acid metabolism is strikingly altered during a time course of BmNPV infection. Amino acid consumption is increased during BmNPV infection at 24 h post infection (hpi), but their abundance recovered at 72 hpi. Central carbon metabolism, on the other hand, particularly glycolysis and glutaminolysis, did not show obvious changes during BmNPV infection. Pharmacologically inhibiting the glycolytic pathway and glutaminolysis also failed to reduce BmNPV replication, revealing that glycolysis and glutaminolysis are not essential during BmNPV infection. This study reveals a unique amino acid utilization process that is implemented during BmNPV infection. Our metabolomic analysis of BmNPV-infected silkworm provides insights as to how baculoviruses induce alterations in host metabolism during systemic infection.
Min Feng; Shigang Fei; Junming Xia; Mengmeng Zhang; Hongyun Wu; Luc Swevers; Jingchen Sun. Global Metabolic Profiling of Baculovirus Infection in Silkworm Hemolymph Shows the Importance of Amino-Acid Metabolism. Viruses 2021, 13, 841 .
AMA StyleMin Feng, Shigang Fei, Junming Xia, Mengmeng Zhang, Hongyun Wu, Luc Swevers, Jingchen Sun. Global Metabolic Profiling of Baculovirus Infection in Silkworm Hemolymph Shows the Importance of Amino-Acid Metabolism. Viruses. 2021; 13 (5):841.
Chicago/Turabian StyleMin Feng; Shigang Fei; Junming Xia; Mengmeng Zhang; Hongyun Wu; Luc Swevers; Jingchen Sun. 2021. "Global Metabolic Profiling of Baculovirus Infection in Silkworm Hemolymph Shows the Importance of Amino-Acid Metabolism." Viruses 13, no. 5: 841.
A wide range of hemocyte types exist in insects but a full definition of the different subclasses is not yet established. The current knowledge of the classification of silkworm hemocytes mainly comes from morphology rather than specific markers, so our understanding of the detailed classification, hemocyte lineage and functions of silkworm hemocytes is very incomplete. Bombyx mori nucleopolyhedrovirus (BmNPV) is a representative member of the baculoviruses and a major pathogen that specifically infects silkworms (Bombyx mori) and causes serious losses in sericulture industry. Here, we performed single-cell RNA sequencing (scRNA-seq) of hemocytes in BmNPV and mock-infected larvae to comprehensively identify silkworm hemocyte subsets and determined specific molecular and cellular characteristics in each hemocyte subset before and after viral infectmadion. A total of 20 cell clusters and their potential marker genes were identified in silkworm hemocytes. All of the hemocyte clusters were infected by BmNPV at 3 days after inoculation. Interestingly, BmNPV infection can cause great changes in the distribution of hemocyte types. The cells appearing in the infection group mainly belong to prohemocytes (PR), while plasmatocytes (PL) and granulocytes (GR) are very much reduced. Furthermore, we found that BmNPV infection suppresses the RNA interference (RNAi) and immune response in the major hemocyte types. In summary, our results revealed the diversity of silkworm hemocytes and provided a rich resource of gene expression profiles for a systems-level understanding of their functions in the uninfected condition and as a response to BmNPV.
Min Feng; Junming Xia; Shigang Fei; Ruoxuan Peng; Xiong Wang; Yaohong Zhou; Pengwei Wang; Luc Swevers; Jingchen Sun. Identification of Silkworm Hemocyte Subsets and Analysis of Their Response to Baculovirus Infection Based on Single-Cell RNA Sequencing. Frontiers in Immunology 2021, 12, 645359 .
AMA StyleMin Feng, Junming Xia, Shigang Fei, Ruoxuan Peng, Xiong Wang, Yaohong Zhou, Pengwei Wang, Luc Swevers, Jingchen Sun. Identification of Silkworm Hemocyte Subsets and Analysis of Their Response to Baculovirus Infection Based on Single-Cell RNA Sequencing. Frontiers in Immunology. 2021; 12 ():645359.
Chicago/Turabian StyleMin Feng; Junming Xia; Shigang Fei; Ruoxuan Peng; Xiong Wang; Yaohong Zhou; Pengwei Wang; Luc Swevers; Jingchen Sun. 2021. "Identification of Silkworm Hemocyte Subsets and Analysis of Their Response to Baculovirus Infection Based on Single-Cell RNA Sequencing." Frontiers in Immunology 12, no. : 645359.
Varroa destructor is one of the main problems in modern beekeeping. Highly selective acaricides with low toxicity to bees are used internationally to control this mite. One of the key acaricides is the organophosphorus (OP) proinsecticide coumaphos, that becomes toxic after enzymatic activation inside Varroa. We show here that mites from the island Andros (AN-CR) exhibit high levels of coumaphos resistance. Resistance is not mediated by decreased coumaphos uptake, target-site resistance, or increased detoxification. Reduced proinsecticide activation by a cytochrome P450 enzyme was the main resistance mechanism, a powerful and rarely encountered evolutionary solution to insecticide selection pressure. After treatment with sublethal doses of [14C] coumaphos, susceptible mite extracts had substantial amounts of coroxon, the activated metabolite of coumaphos, while resistant mites had only trace amounts. This indicates a suppression of the P450 (CYP)-mediated activation step in the AN-CR mites. Bioassays with coroxon to bypass the activation step showed that resistance was dramatically reduced. There are 26 CYPs present in the V. destructor genome. Transcriptome analysis revealed overexpression in resistant mites of CYP4DP24 and underexpression of CYP3012A6 and CYP4EP4. RNA interference of CYP4EP4 in the susceptible population, to mimic underexpression seen in the resistant mites, prevented coumaphos activation and decreased coumaphos toxicity.
Spyridon Vlogiannitis; Konstantinos Mavridis; Wannes Dermauw; Simon Snoeck; Evangelia Katsavou; Evangelia Morou; Paschalis Harizanis; Luc Swevers; Janet Hemingway; René Feyereisen; Thomas Van Leeuwen; John Vontas. Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor. Proceedings of the National Academy of Sciences 2021, 118, 1 .
AMA StyleSpyridon Vlogiannitis, Konstantinos Mavridis, Wannes Dermauw, Simon Snoeck, Evangelia Katsavou, Evangelia Morou, Paschalis Harizanis, Luc Swevers, Janet Hemingway, René Feyereisen, Thomas Van Leeuwen, John Vontas. Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor. Proceedings of the National Academy of Sciences. 2021; 118 (6):1.
Chicago/Turabian StyleSpyridon Vlogiannitis; Konstantinos Mavridis; Wannes Dermauw; Simon Snoeck; Evangelia Katsavou; Evangelia Morou; Paschalis Harizanis; Luc Swevers; Janet Hemingway; René Feyereisen; Thomas Van Leeuwen; John Vontas. 2021. "Reduced proinsecticide activation by cytochrome P450 confers coumaphos resistance in the major bee parasite Varroa destructor." Proceedings of the National Academy of Sciences 118, no. 6: 1.
A wide range of hemocyte types exist in insects but a full definition of the different subclasses is not yet established. The current knowledge of the classification of silkworm hemocytes mainly comes from morphology rather than specific markers, so our understanding of the detailed classification, hemocyte lineage and functions of silkworm hemocytes is very incomplete. Bombyx mori nucleopolyhedrovirus (BmNPV) is a representative member of the baculoviruses, which are a major pathogens that specifically infects silkworms and cause serious loss in sericulture industry. Here, we performed single-cell RNA sequencing (scRNA-seq) of silkworm hemocytes in BmNPV and mock-infected larvae to comprehensively identify silkworm hemocyte subsets and determined specific molecular and cellular characteristics in each hemocyte subset before and after viral infection. A total of 19 cell clusters and their potential marker genes were identified in silkworm hemocytes. Among these hemocyte clusters, clusters 0, 1, 2, 5 and 9 might be granulocytes (GR); clusters 14 and 17 were predicted as plasmatocytes (PL); cluster 18 was tentatively identified as spherulocytes (SP); and clusters 7 and 11 could possibly correspond to oenocytoids (OE). In addition, all of the hemocyte clusters were infected by BmNPV and some infected cells carried high viral-load in silkworm larvae at 3 day post infection (dpi). Interestingly, BmNPV infection can cause severe and diverse changes in gene expression in hemocytes. Cells belonging to the infection group mainly located at the early stage of the pseudotime trajectories. Furthermore, we found that BmNPV infection suppresses the immune response in the major hemocyte types. In summary, our scRNA-seq analysis revealed the diversity of silkworm hemocytes and provided a rich resource of gene expression profiles for a systems-level understanding of their functions in the uninfected condition and as a response to BmNPV.
Min Feng; Junming Xia; Shigang Fei; Xiong Wang; Yaohong Zhou; Pengwei Wang; Luc Swevers; Jingchen Sun. Identification of silkworm hemocyte subsets and analysis of their response to BmNPV infection based on single-cell RNA sequencing. 2020, 1 .
AMA StyleMin Feng, Junming Xia, Shigang Fei, Xiong Wang, Yaohong Zhou, Pengwei Wang, Luc Swevers, Jingchen Sun. Identification of silkworm hemocyte subsets and analysis of their response to BmNPV infection based on single-cell RNA sequencing. . 2020; ():1.
Chicago/Turabian StyleMin Feng; Junming Xia; Shigang Fei; Xiong Wang; Yaohong Zhou; Pengwei Wang; Luc Swevers; Jingchen Sun. 2020. "Identification of silkworm hemocyte subsets and analysis of their response to BmNPV infection based on single-cell RNA sequencing." , no. : 1.
Antimicrobial peptides (AMPs) with antiviral activity (antiviral peptides: AVPs) have become a research hotspot and already show immense potential to become pharmaceutically available antiviral drugs. AVPs have exhibited huge potential in inhibiting viruses by targeting various stages of their life cycle. Insects are the most speciose group of animals that inhabit almost all ecosystems and habitats on the land and are a rich source of natural AMPs. However, insect AVP mining, functional research, and drug development are still in their infancy. This review aims to summarize the currently validated insect AVPs, explore potential new insect AVPs and to discuss their possible mechanism of synthesis and action, with a view to providing clues to unravel the mechanisms of insect antiviral immunity and to develop insect AVP-derived antiviral drugs.
Min Feng; Shigang Fei; Junming Xia; Vassiliki Labropoulou; Luc Swevers; Jingchen Sun. Antimicrobial Peptides as Potential Antiviral Factors in Insect Antiviral Immune Response. Frontiers in Immunology 2020, 11, 1 .
AMA StyleMin Feng, Shigang Fei, Junming Xia, Vassiliki Labropoulou, Luc Swevers, Jingchen Sun. Antimicrobial Peptides as Potential Antiviral Factors in Insect Antiviral Immune Response. Frontiers in Immunology. 2020; 11 ():1.
Chicago/Turabian StyleMin Feng; Shigang Fei; Junming Xia; Vassiliki Labropoulou; Luc Swevers; Jingchen Sun. 2020. "Antimicrobial Peptides as Potential Antiviral Factors in Insect Antiviral Immune Response." Frontiers in Immunology 11, no. : 1.
Mammalian intestinal organoids are multicellular structures that resemble closely the structure of the intestinal epithelium and can be generated in vitro from intestinal stem cells under appropriate culture conditions. This technology has transformed pharmaceutical research and drug development in human medicine. For the insect gut, no biotechnological platform equivalent to organoid cultures has been described yet. Comparison of the regulation of intestinal homeostasis and growth between insects and mammals has revealed significant similarities but also important differences. In contrast to mammals, the differentiation potential of available insect cell lines is limited and can not be exploited for in vitro permeability assays to measure the uptake of insecticides. The successful development of in vitro models could be a result of the emergence of molecular mechanisms of self‐organization and signaling in the intestine that are unique to mammals. It is nevertheless considered that the technology gap is a consequence of vast differences in knowledge, particularly with respect to culture conditions that maintain the differentation potential of insect midgut cells. From the viewpoint of pest control, advanced in vitro models of the insect midgut would be very desirable because of its key barrier function for orally ingested insecticides with hemolymphatic target and its role in insecticide resistance. This article is protected by copyright. All rights reserved.
Luc Swevers; Shane Denecke; Kathrin Vogelsang; Sven Geibel; John Vontas. Can the mammalian organoid technology be applied to the insect gut? Pest Management Science 2020, 77, 55 -63.
AMA StyleLuc Swevers, Shane Denecke, Kathrin Vogelsang, Sven Geibel, John Vontas. Can the mammalian organoid technology be applied to the insect gut? Pest Management Science. 2020; 77 (1):55-63.
Chicago/Turabian StyleLuc Swevers; Shane Denecke; Kathrin Vogelsang; Sven Geibel; John Vontas. 2020. "Can the mammalian organoid technology be applied to the insect gut?" Pest Management Science 77, no. 1: 55-63.
Bombyx mori nucleopolyhedrovirus (BmNPV) is a DNA virus that causes huge losses to the silkworm industry but the piRNA responses during BmNPV infection in the silkworm remain uninvestigated. Here, silkworm piRNA profiles of uninfected and BmNPV‐infected fat body and midgut were determined by high‐through sequencing in the early stages of BmNPV infection. A total of 2675 and 3396 genome‐derived piRNAs were identified from fat body and midgut, respectively. These genome‐derived piRNAs mainly originated from unannotated instead of transposon regions in the silkworm genome. In total, 572 piRNAs were associated with 280 putative target genes in fat body and 805 piRNAs with 380 target genes in midgut. Compared to uninfected tissues, 322 and 129 piRNAs were significantly up‐regulated in BmNPV‐infected fat body and midgut, respectively. In addition, 276 and 117 piRNAs were significantly down‐regulated. Moreover, differentially expressed (DE) piRNAs during BmNPV infection differed significantly between fat body and midgut. Putative DE piRNA–targeted genes were associated with “response to stimulus” and “environmental information processing” in fat body after infection with BmNPV, which may indicate an active piRNA response to BmNPV infection in fat body. This study may lay the foundation for future research of the potential roles of the piRNA pathway and specific piRNAs in BmNPV pathogenesis. This article is protected by copyright. All rights reserved
Min Feng; Anna Kolliopoulou; Yao‐Hong Zhou; Shi‐Gang Fei; Jun‐Ming Xia; Luc Swevers; Jing‐Chen Sun. The piRNA response to BmNPV infection in the silkworm fat body and midgut. Insect Science 2020, 28, 662 -679.
AMA StyleMin Feng, Anna Kolliopoulou, Yao‐Hong Zhou, Shi‐Gang Fei, Jun‐Ming Xia, Luc Swevers, Jing‐Chen Sun. The piRNA response to BmNPV infection in the silkworm fat body and midgut. Insect Science. 2020; 28 (3):662-679.
Chicago/Turabian StyleMin Feng; Anna Kolliopoulou; Yao‐Hong Zhou; Shi‐Gang Fei; Jun‐Ming Xia; Luc Swevers; Jing‐Chen Sun. 2020. "The piRNA response to BmNPV infection in the silkworm fat body and midgut." Insect Science 28, no. 3: 662-679.
High-throughput approaches have opened new opportunities for understanding biological processes such as persistent virus infections, which are widespread. However, the potential of persistent infections to develop towards pathogenesis remains to be investigated, particularly with respect to the role of host metabolism. To explore the interactions between cellular metabolism and persistent/pathogenic virus infection, we performed untargeted and targeted metabolomic analysis to examine the effects of Cricket paralysis virus (CrPV, Dicistroviridae) in persistently infected silkworm Bm5 cells and acutely infected Drosophila S2 cells. Our previous study (Viruses 2019, 11, 861) established that both glucose and glutamine levels significantly increased during the persistent period of CrPV infection of Bm5 cells, while they decreased steeply during the pathogenic stages. Strikingly, in this study, an almost opposite pattern in change of metabolites was observed during different stages of acute infection of S2 cells. More specifically, a significant decrease in amino acids and carbohydrates was observed prior to pathogenesis, while their abundance significantly increased again during pathogenesis. Our study illustrates the occurrence of diametrically opposite changes in central carbon mechanisms during CrPV infection of S2 and Bm5 cells that is possibly related to the type of infection (acute or persistent) that is triggered by the virus.
Luo-Luo Wang; Luc Swevers; Lieven Van Meulebroek; Ivan Meeus; Lynn Vanhaecke; Guy Smagghe. Metabolomic Analysis of Cricket paralysis virus Infection in Drosophila S2 Cells Reveals Divergent Effects on Central Carbon Metabolism as Compared with Silkworm Bm5 Cells. Viruses 2020, 12, 393 .
AMA StyleLuo-Luo Wang, Luc Swevers, Lieven Van Meulebroek, Ivan Meeus, Lynn Vanhaecke, Guy Smagghe. Metabolomic Analysis of Cricket paralysis virus Infection in Drosophila S2 Cells Reveals Divergent Effects on Central Carbon Metabolism as Compared with Silkworm Bm5 Cells. Viruses. 2020; 12 (4):393.
Chicago/Turabian StyleLuo-Luo Wang; Luc Swevers; Lieven Van Meulebroek; Ivan Meeus; Lynn Vanhaecke; Guy Smagghe. 2020. "Metabolomic Analysis of Cricket paralysis virus Infection in Drosophila S2 Cells Reveals Divergent Effects on Central Carbon Metabolism as Compared with Silkworm Bm5 Cells." Viruses 12, no. 4: 393.
How a host metabolism responds to infection with insect viruses and how it relates to pathogenesis, is little investigated. Our previous study observed that Cricket paralysis virus (CrPV, Dicistroviridae) causes short term persistence in silkworm Bm5 cells before proceeding to acute infection. In this study, a metabolomics approach based on high resolution mass spectrometry was applied to investigate how a host metabolism is altered during the course of CrPV infection in Bm5 cells and which changes are characteristic for the transition from persistence to pathogenicity. We observed that CrPV infection led to significant and stage-specific metabolic changes in Bm5 cells. Differential metabolites abundance and pathway analysis further identified specific metabolic features at different stages in the viral life cycle. Notably, both glucose and glutamine levels significantly increased during CrPV persistent infection followed by a steep decrease during the pathogenic stages, suggesting that the central carbon metabolism was significantly modified during CrPV infection in Bm5 cells. In addition, dynamic changes in levels of polyamines were detected. Taken together, this study characterized for the first time the metabolic dynamics of CrPV infection in insect cells, proposing a central role for the regulation of both amino acid and carbohydrate metabolism during the period of persistent infection of CrPV in Bm5 cells.
Luo-Luo Wang; Luc Swevers; Caroline Rombouts; Ivan Meeus; Lieven Van Meulebroek; Lynn Vanhaecke; Guy Smagghe. A Metabolomics Approach to Unravel Cricket Paralysis Virus Infection in Silkworm Bm5 Cells. Viruses 2019, 11, 861 .
AMA StyleLuo-Luo Wang, Luc Swevers, Caroline Rombouts, Ivan Meeus, Lieven Van Meulebroek, Lynn Vanhaecke, Guy Smagghe. A Metabolomics Approach to Unravel Cricket Paralysis Virus Infection in Silkworm Bm5 Cells. Viruses. 2019; 11 (9):861.
Chicago/Turabian StyleLuo-Luo Wang; Luc Swevers; Caroline Rombouts; Ivan Meeus; Lieven Van Meulebroek; Lynn Vanhaecke; Guy Smagghe. 2019. "A Metabolomics Approach to Unravel Cricket Paralysis Virus Infection in Silkworm Bm5 Cells." Viruses 11, no. 9: 861.
Recent years have shown a large increase in studies of infection of the silkworm (Bombyx mori) with Cypovirus 1 (previously designated as B. mori cytoplasmic polyhedrosis virus), that causes serious damage in sericulture. Cypovirus 1 has a single‐layered capsid that encapsulates a segmented double‐strand RNA (dsRNA) genome which are attractive features for the establishment of a biotechnological platform for the production of specialized gene silencing agents, either as recombinant viruses or as viral‐like particles with nonreplicative dsRNA cargo. For both combatting viral disease and application of Cypovirus‐based pest control, however, a better understanding is needed of the innate immune response caused by Cypovirus infection of the midgut of lepidopteran larvae. Studies of deep sequencing of viral small RNAs have indicated the importance of the RNA interference pathway in the control of Cypovirus infection although many functional aspects still need to be elucidated and conclusive evidence is lacking. A considerable number of transcriptome studies were carried out that revealed a complex response that hitherto remains uncharacterized because of a dearth in functional studies. Also, the uptake mechanism of Cypovirus by the midgut cells remains unclarified because of contrasting mechanisms revealed by electron microscopy and functional studies. The field will benefit from an increase in functional studies that will depend on transgenic silkworm technology and reverse genetics systems for Cypovirus 1.
Luc Swevers; Min Feng; Feifei Ren; Jingchen Sun. Antiviral defense against Cypovirus 1 ( Reoviridae ) infection in the silkworm, Bombyx mori. Archives of Insect Biochemistry and Physiology 2019, 103, e21616 .
AMA StyleLuc Swevers, Min Feng, Feifei Ren, Jingchen Sun. Antiviral defense against Cypovirus 1 ( Reoviridae ) infection in the silkworm, Bombyx mori. Archives of Insect Biochemistry and Physiology. 2019; 103 (3):e21616.
Chicago/Turabian StyleLuc Swevers; Min Feng; Feifei Ren; Jingchen Sun. 2019. "Antiviral defense against Cypovirus 1 ( Reoviridae ) infection in the silkworm, Bombyx mori." Archives of Insect Biochemistry and Physiology 103, no. 3: e21616.
Double-stranded RNA (dsRNA) molecules of viral origin trigger a post-transcriptional gene-silencing mechanism called RNA interference (RNAi). Specifically, virally derived dsRNA is recognized and cleaved by the enzyme Dicer2 into short interfering RNAs (siRNAs), which further direct sequence-specific RNA silencing, ultimately silencing replication of the virus. Notably, RNAi can also be artificially triggered by the delivery of gene-specific dsRNA, thereby leading to endogenous gene silencing. This is a widely used technology that holds great potential to contribute to novel pest control strategies. In this regard, research efforts have been set to find methods to efficiently trigger RNAi in the field. In this article, we demonstrate the generation of dsRNA- and/or virus-derived siRNAs—the main RNAi effectors—in six insect species belonging to five economically important orders (Lepidoptera, Orthoptera, Hymenoptera, Coleoptera, and Diptera). In addition, we describe that the siRNA length distribution is species-dependent. Taken together, our results reveal interspecies variability in the (antiviral) RNAi mechanism in insects and show promise to contribute to future research on (viral-based) RNAi-triggering mechanisms in this class of animals.
Dulce Santos; Lina Mingels; Elise Vogel; Luoluo Wang; Olivier Christiaens; Kaat Cappelle; Niels Wynant; Yannick Gansemans; Filip Van Nieuwerburgh; Guy Smagghe; Luc Swevers; Jozef Vanden Broeck. Generation of Virus- and dsRNA-Derived siRNAs with Species-Dependent Length in Insects. Viruses 2019, 11, 738 .
AMA StyleDulce Santos, Lina Mingels, Elise Vogel, Luoluo Wang, Olivier Christiaens, Kaat Cappelle, Niels Wynant, Yannick Gansemans, Filip Van Nieuwerburgh, Guy Smagghe, Luc Swevers, Jozef Vanden Broeck. Generation of Virus- and dsRNA-Derived siRNAs with Species-Dependent Length in Insects. Viruses. 2019; 11 (8):738.
Chicago/Turabian StyleDulce Santos; Lina Mingels; Elise Vogel; Luoluo Wang; Olivier Christiaens; Kaat Cappelle; Niels Wynant; Yannick Gansemans; Filip Van Nieuwerburgh; Guy Smagghe; Luc Swevers; Jozef Vanden Broeck. 2019. "Generation of Virus- and dsRNA-Derived siRNAs with Species-Dependent Length in Insects." Viruses 11, no. 8: 738.
Arboviruses are capable to establish long-term persistent infections in mosquitoes that do not affect significantly the physiology of the insect vectors. Arbovirus infections are controlled by the RNAi machinery via the production of viral siRNAs and the formation of RISC complexes targeting viral genomes and mRNAs. Engineered arboviruses that contain cellular gene sequences can therefore be transformed to "viral silencing vectors" for studies of gene function in reverse genetics approaches. More specifically, "ideal" viral silencing vectors must be competent to induce robust RNAi effects while other interactions with the host immune system should be kept at a minimum to reduce non-specific effects. Because of their inconspicuous nature, arboviruses may approach the "ideal" viral silencing vectors in insects and it is therefore worthwhile to study the mechanisms by which the interactions with the RNAi machinery occur. In this review, an analysis is presented of the antiviral RNAi response in mosquito vectors with respect to the major types of arboviruses (alphaviruses, flaviviruses, bunyaviruses, and others). With respect to antiviral defense, the exo-RNAi pathway constitutes the major mechanism while the contribution of both miRNAs and viral piRNAs remains a contentious issue. However, additional mechanisms exist in mosquitoes that are capable to enhance or restrict the efficiency of viral silencing vectors such as the amplification of RNAi effects by DNA forms, the existence of incorporated viral elements in the genome and the induction of a non-specific systemic response by Dicer-2. Of significance is the observation that no major "viral suppressors of RNAi" (VSRs) seem to be encoded by arboviral genomes, indicating that relatively tight control of the activity of the RNA-dependent RNA polymerase (RdRp) may be sufficient to maintain the persistent character of arbovirus infections. Major strategies for improvement of viral silencing vectors therefore are proposed to involve engineering of VSRs and modifying of the properties of the RdRp. Because of safety issues (pathogen status), however, arbovirus-based silencing vectors are not well suited for practical applications, such as RNAi-based mosquito control. In that case, related mosquito-specific viruses that also establish persistent infections and may cause similar RNAi responses may represent a valuable alternative solution.
Jisheng Liu; Luc Swevers; Anna Kolliopoulou; Guy Smagghe. Arboviruses and the Challenge to Establish Systemic and Persistent Infections in Competent Mosquito Vectors: The Interaction With the RNAi Mechanism. Frontiers in Physiology 2019, 10, 890 .
AMA StyleJisheng Liu, Luc Swevers, Anna Kolliopoulou, Guy Smagghe. Arboviruses and the Challenge to Establish Systemic and Persistent Infections in Competent Mosquito Vectors: The Interaction With the RNAi Mechanism. Frontiers in Physiology. 2019; 10 ():890.
Chicago/Turabian StyleJisheng Liu; Luc Swevers; Anna Kolliopoulou; Guy Smagghe. 2019. "Arboviruses and the Challenge to Establish Systemic and Persistent Infections in Competent Mosquito Vectors: The Interaction With the RNAi Mechanism." Frontiers in Physiology 10, no. : 890.
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 transposon‐targeting, 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. This article is categorized under: Regulatory RNAs/RNAi/Riboswitches > RNAi: Mechanisms of Action Regulatory RNAs/RNAi/Riboswitches > Biogenesis of Effector Small RNAs
Anna Kolliopoulou; Dulce Santos; Clauvis Nji Tizi Taning; Niels Wynant; Jozef Vanden Broeck; Guy Smagghe; Luc Swevers. PIWI pathway against viruses in insects. WIREs RNA 2019, 10, e1555 .
AMA StyleAnna Kolliopoulou, Dulce Santos, Clauvis Nji Tizi Taning, Niels Wynant, Jozef Vanden Broeck, Guy Smagghe, Luc Swevers. PIWI pathway against viruses in insects. WIREs RNA. 2019; 10 (6):e1555.
Chicago/Turabian StyleAnna Kolliopoulou; Dulce Santos; Clauvis Nji Tizi Taning; Niels Wynant; Jozef Vanden Broeck; Guy Smagghe; Luc Swevers. 2019. "PIWI pathway against viruses in insects." WIREs RNA 10, no. 6: e1555.
The published genome sequence of Antheraea yamamai (Saturnnidae) was used to construct a library of long terminal repeat (LTR)-retrotransposons that is representative of the wild silkmoth (Antherea) genus, and that includes 22,666 solo LTRs and 541 full-length LTRs. The LTR retrotransposons of Antheraea yamamai (AyLTRs) could be classified into the three canonical groups of Gypsy, Copia and Belpao. Eleven AyLTRs contained the env gene element, but the relationship with the env element of baculovirus, particularly A. yamamai and pernyi nucleopolyhedrovirus (AyNPV and ApNPV), was distant. A total of 251 “independent” full-length AyLTRs were identified that were located within 100 kb distance (downstream or upstream) of 406 neighboring genes in A. yamamai. Regulation of these genes might occur in cis by the AyLTRs, and the neighboring genes were found to be enriched in GO terms such as “response to stimulus”, and KEGG terms such as “mTOR signaling pathway” among others. Furthermore, the library of LTR-retrotransposons and the A. yamamai genome were used to identify and analyze the expression of LTR-retrotransposons and genes in ApNPV-infected and non-infected A. pernyi larval midguts, using raw data of a published transcriptome study. Our analysis demonstrates that 93 full-length LTR-retrotransposons are transcribed in the midgut of A. pernyi of which 12 significantly change their expression after ApNPV infection (differentially expressed LTR-retrotransposons or DELs). In addition, the expression of differentially expressed genes (DEGs) and neighboring DELs on the chromosome following ApNPV infection suggests the possibility of regulation of expression of DEGs by DELs through a cis mechanism, which will require experimental verification. When examined in more detail, it was found that genes involved in Notch signaling and stress granule (SG) formation were significantly up-regulated in ApNPV-infected A. pernyi larval midgut. Moreover, several DEGs in the Notch and SG pathways were found to be located in the neighborhood of particular DELs, indicating the possibility of DEG-DEL cross-regulation in cis for these two pathways.
Min Feng; Feifei Ren; Yaohong Zhou; Nan Zhang; Qiuyuan Lu; Luc Swevers; Jingchen Sun. Correlation in Expression between LTR Retrotransposons and Potential Host Cis-Targets during Infection of Antherea pernyi with ApNPV Baculovirus. Viruses 2019, 11, 421 .
AMA StyleMin Feng, Feifei Ren, Yaohong Zhou, Nan Zhang, Qiuyuan Lu, Luc Swevers, Jingchen Sun. Correlation in Expression between LTR Retrotransposons and Potential Host Cis-Targets during Infection of Antherea pernyi with ApNPV Baculovirus. Viruses. 2019; 11 (5):421.
Chicago/Turabian StyleMin Feng; Feifei Ren; Yaohong Zhou; Nan Zhang; Qiuyuan Lu; Luc Swevers; Jingchen Sun. 2019. "Correlation in Expression between LTR Retrotransposons and Potential Host Cis-Targets during Infection of Antherea pernyi with ApNPV Baculovirus." Viruses 11, no. 5: 421.
In insects, RNAi is considered the major antiviral immune defense pathway. DsRNAs produced during viral infection are processed by Dicer enzymes into small RNAs that function as specificity determinants to silence viral genes. By contrast, in mammals, recognition of molecules associated with viral infection, such as dsRNA, by pattern recognition receptors (PRRs) initiates a signaling cascade that culminates in the production and release of signaling proteins with antiviral function such as interferons. However, in insects, the hypothesis that components of virions can be recognized as pathogen-activated molecular patterns (PAMPs) to activate the innate immune response has not been investigated systematically. In this study, the potential of VP1, that constitutes the major capsid protein of cytoplasmic polyhedrosis virus (CPV; Reoviridae), to activate a collection of immune-related genes was examined in silkworm-derived Bm5 cells. Two different methods of VP1 administration were tested, either through endogenous expression in transformed cell lines, or through addition of purified VP1-based viral-like particles to the extracellular medium. In addition, exposure to CPV virions isolated from purified polyhedra was also performed. In general, our results do not show a robust transcriptional response of immune-related genes to VP1 or CPV virions, but two exceptions were noted. First, the expression of the antimicrobial peptide (AMP) gene Attacin was strongly induced after 24 h of exposure to VP1-based VLPs. Second, the expression levels of dcr-2, an essential gene in the RNAi pathway, were greatly increased in VP1-expressing transformed Sf21 cells but not transformed Bm5 cells, indicating the existence of species-specific effects. However, the increased expression of dcr-2 did not result in increased silencing efficiency when tested in an RNAi reporter assay. Our study indicates that the capsid protein VP1 of CPV has the potential to act as a PAMP and to induce a transcriptional response in insect cells that relate both to RNAi and protein effectors such as AMPs. The identity of the PRRs and the signaling cascade that are potentially triggered by VP1 remain to be elucidated in future experiments. While this study was performed on a small scale, it can encourage more comprehensive studies with high-throughput approaches (microarray, deep sequencing) to search more systematically whether viral capsid proteins can act as PAMPs in insects and whether their production results in the induction of immune-related genes with potential antiviral function.
Yongchao Zhao; Anna Kolliopoulou; Feifei Ren; Qiuyuan Lu; Vassiliki Labropoulou; Luc Swevers; Jingchen Sun. Transcriptional response of immune-related genes after endogenous expression of VP1 and exogenous exposure to VP1-based VLPs and CPV virions in lepidopteran cell lines. Molecular Genetics and Genomics 2019, 294, 887 -899.
AMA StyleYongchao Zhao, Anna Kolliopoulou, Feifei Ren, Qiuyuan Lu, Vassiliki Labropoulou, Luc Swevers, Jingchen Sun. Transcriptional response of immune-related genes after endogenous expression of VP1 and exogenous exposure to VP1-based VLPs and CPV virions in lepidopteran cell lines. Molecular Genetics and Genomics. 2019; 294 (4):887-899.
Chicago/Turabian StyleYongchao Zhao; Anna Kolliopoulou; Feifei Ren; Qiuyuan Lu; Vassiliki Labropoulou; Luc Swevers; Jingchen Sun. 2019. "Transcriptional response of immune-related genes after endogenous expression of VP1 and exogenous exposure to VP1-based VLPs and CPV virions in lepidopteran cell lines." Molecular Genetics and Genomics 294, no. 4: 887-899.
Next generation sequencing has revealed the widespread occurrence of persistent virus infections in insects but little is known regarding to what extent persistent infections can affect cellular physiology and how they might contribute to the development of disease. In contrast to the pathogenic infections occurring in Drosophila S2 cells, it was observed that Cricket Paralysis virus (CrPV; Dicistroviridae) causes persistent infections in 9 lepidopteran and 2 coleopteran cell lines. The status of the persistent infection was subsequently investigated in more detail using silkworm-derived Bm5 cells, where the infection eventually becomes pathogenic after 3-4 weeks. The short-term persistence period in Bm5 cells is characterized by low levels of viral replication and virion production as well as by the production of viral siRNAs. However, during this period cellular physiology also becomes altered since the cells become susceptible to infection by the nodavirus Flock House virus (FHV). Pathogenicity and widespread mortality at 4 weeks is preceded by a large increase in virion production and the transcriptional activation of immune-related genes encoding RNAi factors and transcription factors in the Toll, Imd and Jak-STAT pathways. During the infection of Bm5 cells, the infective properties of CrPV are not altered, indicating changes in the physiology of the host cells during the transition from short-term persistence to pathogenicity. The in vitro system of Bm5 cells persistently infected with CrPV can therefore be presented as an easily accessible model to study the nature of persistent virus infections and the processes that trigger the transition to pathogenicity, for instance through the application of different “omics” approaches (transcriptomics, proteomics, metabolomics). The different factors that can cause the transition from persistence to pathogenicity in the Bm5-CrPV infection model are discussed.
Luo-Luo Wang; Kaat Cappelle; Dulce Santos; Jozef Vanden Broeck; Guy Smagghe; Luc Swevers. Short-term persistence precedes pathogenic infection: Infection kinetics of cricket paralysis virus in silkworm-derived Bm5 cells. Journal of Insect Physiology 2019, 115, 1 -11.
AMA StyleLuo-Luo Wang, Kaat Cappelle, Dulce Santos, Jozef Vanden Broeck, Guy Smagghe, Luc Swevers. Short-term persistence precedes pathogenic infection: Infection kinetics of cricket paralysis virus in silkworm-derived Bm5 cells. Journal of Insect Physiology. 2019; 115 ():1-11.
Chicago/Turabian StyleLuo-Luo Wang; Kaat Cappelle; Dulce Santos; Jozef Vanden Broeck; Guy Smagghe; Luc Swevers. 2019. "Short-term persistence precedes pathogenic infection: Infection kinetics of cricket paralysis virus in silkworm-derived Bm5 cells." Journal of Insect Physiology 115, no. : 1-11.
An overview is presented of the different functions of ecdysone signaling during insect oogenesis. An extensive genetic toolkit allowed analysis with unprecedented temporal and spatial detail in Drosophila where functions were revealed in stem cell proliferation and niche maintenance, germline cyst differentiation and follicle formation, integration of nutrient and lipid signaling, follicle maturation and ovulation. Besides putative autocrine/paracrine signaling, hormonal networks were identified that integrate ecdysone with other endocrine signaling pathways. In other insects, progress in oogenesis has lagged behind although recently RNAi emerged as a new tool to analyze gene function in ovaries in hemimetabolous insects and Tribolium.
Luc Swevers. An update on ecdysone signaling during insect oogenesis. Current Opinion in Insect Science 2018, 31, 8 -13.
AMA StyleLuc Swevers. An update on ecdysone signaling during insect oogenesis. Current Opinion in Insect Science. 2018; 31 ():8-13.
Chicago/Turabian StyleLuc Swevers. 2018. "An update on ecdysone signaling during insect oogenesis." Current Opinion in Insect Science 31, no. : 8-13.
RNAi is considered a major antiviral defense mechanism in insects, but its relative importance as compared to other antiviral pathways has not been evaluated comprehensively. Here, it is attempted to give an overview of the antiviral defense mechanisms in Drosophila that involve both RNAi and non-RNAi. While RNAi is considered important in most viral infections, many other pathways can exist that confer antiviral resistance. It is noted that very few direct recognition mechanisms of virus infections have been identified in Drosophila and that the activation of immune pathways may be accomplished indirectly through cell damage incurred by viral replication. In several cases, protection against viral infection can be obtained in RNAi mutants by non-RNAi mechanisms, confirming the variability of the RNAi defense mechanism according to the type of infection and the physiological status of the host. This analysis is aimed at more systematically investigating the relative contribution of RNAi in the antiviral response and more specifically, to ask whether RNAi efficiency is affected when other defense mechanisms predominate. While Drosophila can function as a useful model, this issue may be more critical for economically important insects that are either controlled (agricultural pests and vectors of diseases) or protected from parasite infection (beneficial insects as bees) by RNAi products.
Luc Swevers; Jisheng Liu; Guy Smagghe. Defense Mechanisms against Viral Infection in Drosophila: RNAi and Non-RNAi. Viruses 2018, 10, 230 .
AMA StyleLuc Swevers, Jisheng Liu, Guy Smagghe. Defense Mechanisms against Viral Infection in Drosophila: RNAi and Non-RNAi. Viruses. 2018; 10 (5):230.
Chicago/Turabian StyleLuc Swevers; Jisheng Liu; Guy Smagghe. 2018. "Defense Mechanisms against Viral Infection in Drosophila: RNAi and Non-RNAi." Viruses 10, no. 5: 230.
RNAi is applied as a new and safe method for pest control in agriculture but efficiency and specificity of delivery of dsRNA trigger remains a critical issue. Various agents have been proposed to augment dsRNA delivery, such as engineered micro-organisms and synthetic nanoparticles, but the use of viruses has received relatively little attention. Here we present a critical view of the potential of the use of recombinant viruses for efficient and specific delivery of dsRNA. First of all, it requires the availability of plasmid-based reverse genetics systems for virus production, of which an overview is presented. For RNA viruses, their application seems to be straightforward since dsRNA is produced as an intermediate molecule during viral replication, but DNA viruses also have potential through the production of RNA hairpins after transcription. However, application of recombinant virus for dsRNA delivery may not be straightforward in many cases, since viruses can encode RNAi suppressors, and virus-induced silencing effects can be determined by the properties of the encoded RNAi suppressor. An alternative is virus-like particles that retain the efficiency and specificity determinants of natural virions but have encapsidated non-replicating RNA. Finally, the use of viruses raises important safety issues which need to be addressed before application can proceed.
Anna Kolliopoulou; Clauvis N. T. Taning; Guy Smagghe; Luc Swevers. Viral Delivery of dsRNA for Control of Insect Agricultural Pests and Vectors of Human Disease: Prospects and Challenges. Frontiers in Physiology 2017, 8, 399 -399.
AMA StyleAnna Kolliopoulou, Clauvis N. T. Taning, Guy Smagghe, Luc Swevers. Viral Delivery of dsRNA for Control of Insect Agricultural Pests and Vectors of Human Disease: Prospects and Challenges. Frontiers in Physiology. 2017; 8 ():399-399.
Chicago/Turabian StyleAnna Kolliopoulou; Clauvis N. T. Taning; Guy Smagghe; Luc Swevers. 2017. "Viral Delivery of dsRNA for Control of Insect Agricultural Pests and Vectors of Human Disease: Prospects and Challenges." Frontiers in Physiology 8, no. : 399-399.
Anna Kourti; Luc Swevers; Dimitrios Kontogiannatos. In Search of New Methodologies for Efficient Insect Pest Control: “The RNAi “Movement”. Biological Control of Pest and Vector Insects 2017, 1 .
AMA StyleAnna Kourti, Luc Swevers, Dimitrios Kontogiannatos. In Search of New Methodologies for Efficient Insect Pest Control: “The RNAi “Movement”. Biological Control of Pest and Vector Insects. 2017; ():1.
Chicago/Turabian StyleAnna Kourti; Luc Swevers; Dimitrios Kontogiannatos. 2017. "In Search of New Methodologies for Efficient Insect Pest Control: “The RNAi “Movement”." Biological Control of Pest and Vector Insects , no. : 1.