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The DNA Virus Invertebrate Iridescent Virus 6 Is a Target of the Drosophila Rnai Machinery

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The DNA Virus Invertebrate Iridescent Virus 6 Is a Target of the Drosophila Rnai Machinery The DNA virus Invertebrate iridescent virus 6 is a target of the Drosophila RNAi machinery Alfred W. Bronkhorsta,1, Koen W. R. van Cleefa,1, Nicolas Vodovarb,2, Ikbal_ Agah Ince_ c,d,e, Hervé Blancb, Just M. Vlakc, Maria-Carla Salehb,3, and Ronald P. van Rija,3 aDepartment of Medical Microbiology, Nijmegen Centre for Molecular Life Sciences, Nijmegen Institute for Infection, Inflammation, and Immunity, Radboud University Nijmegen Medical Centre, 6500 HB Nijmegen, The Netherlands; bViruses and RNA Interference Group, Institut Pasteur, Centre National de la Recherche Scientifique, Unité de Recherche Associée 3015, 75015 Paris, France; cLaboratory of Virology, Wageningen University, 6708 PB Wageningen, The Netherlands; dDepartment of Genetics and Bioengineering, Yeditepe University, Istanbul 34755, Turkey; and eDepartment of Biosystems Engineering, Faculty of Engineering, Giresun University, Giresun 28100, Turkey Edited by Peter Palese, Mount Sinai School of Medicine, New York, NY, and approved October 19, 2012 (received for review April 28, 2012) RNA viruses in insects are targets of an RNA interference (RNAi)- sequently, are hypersensitive to virus infection and succumb more based antiviral immune response, in which viral replication inter- rapidly than their wild-type (WT) controls (11–14). mediates or viral dsRNA genomes are processed by Dicer-2 (Dcr-2) Small RNA cloning and next-generation sequencing provide into viral small interfering RNAs (vsiRNAs). Whether dsDNA virus detailed insights into vsiRNA biogenesis. In several studies in infections are controlled by the RNAi pathway remains to be insects, the polarity of the vsiRNA population deviates strongly determined. Here, we analyzed the role of RNAi in DNA virus from the highly skewed distribution of positive strand (+) over infection using Drosophila melanogaster infected with Invertebrate negative (−) viral RNAs that is generally observed in (+) RNA iridescent virus 6 (IIV-6) as a model. We show that Dcr-2 and Argo- virus infection. Indeed, vsiRNAs mapped in similar proportions to naute-2 mutant flies are more sensitive to virus infection, suggest- (+) and (−) viral RNA strands in Aedes aegypti, Aedes albopictus, ing that vsiRNAs contribute to the control of DNA virus infection. and Culex pipiens mosquitoes infected with a number of arthropod- Indeed, small RNA sequencing of IIV-6–infected WT and RNAi mu- borne viruses, including Sindbis virus, Semliki Forest virus, West tant flies identified abundant vsiRNAs that were produced in a Dcr- Nile virus, Dengue virus, and Chikungunya virus, as well as in 2–dependent manner. We observed a highly uneven distribution Drosophila infected with (+) RNA viruses from different families with strong clustering of vsiRNAs to small defined regions (hot- (5, 15–24). In addition, in infections of Drosophila with the nega- spots) and modest coverage at other regions (coldspots). vsiRNAs tive-strand RNA virus vesicular stomatitis virus, similar numbers of mapped in similar proportions to both strands of the viral genome, (+) over (−) vsiRNAs were recovered (14). These results, together suggesting that long dsRNA derived from convergent overlapping with the distribution of vsiRNAs all along the viral genome, imply transcripts serves as a substrate for Dcr-2. In agreement, strand-spe- that viral replication intermediates of RNA viruses are the main cific RT-PCR and Northern blot analyses indicated that antisense targets for Dcr-2. Also in dsRNA virus infections, similar amounts transcripts are produced during infection. Moreover, we show that of vsiRNAs of both polarities were generated, most likely by Dcr-2– vsiRNAs are functional in silencing reporter constructs carrying frag- dependent processing of viral genomic dsRNA (18). Thus, differ- ments of the IIV-6 genome. Together, our data indicate that RNAi ent classes of viruses seem to be processed by a similar vsiRNA provides antiviral defense against dsDNA viruses in animals. Thus, biogenesis pathway. These studies have focused on RNA viruses, RNAi is the predominant antiviral defense mechanism in insects that because all well-established model viruses of Drosophila and all provides protection against all major classes of viruses. known mosquito-transmitted viruses are RNA viruses. More re- cently, a next-generation sequencing approach identified small insect immunity | Iridoviridae | siRNA | antiviral immunity | RNAs derived from a novel densovirus, a single-stranded (ss) DNA small RNA profiling | next-generation sequencing virus, in wild-caught C. pipiens molestus (25). These observations suggest that ssDNA viruses are a target for Dicer in mosquitoes, ouble-stranded RNA (dsRNA) is a danger signal: It cannot although the biogenesis and function of the viral small RNAs Dbe detected in healthy, noninfected cells, but it is produced remain unclear. during infection by many RNA and DNA viruses (1). It is thus not surprising that dsRNA is a central trigger of innate immune responses. In vertebrates, recognition of dsRNA by the cytosolic Author contributions: A.W.B., K.W.R.v.C., M.-C.S., and R.P.v.R. designed research; A.W.B., sensors RIG-I and MDA-5 initiates a cascade of events culminating K.W.R.v.C., N.V., and H.B. performed research; I.A._ I._ and J.M.V. contributed new reagents/ in the production of type I IFN and the subsequent induction of analytic tools; A.W.B., K.W.R.v.C., N.V., M.-C.S., and R.P.v.R. analyzed data; and A.W.B., M.-C.S., and R.P.v.R. wrote the paper. an antiviral state (2). Likewise, dsRNA triggers a sequence-in- fl dependent antiviral response in penaeid shrimp that is distinct from The authors declare no con ict of interest. the vertebrate IFN pathway (3). In plants, fungi, and arthropods, This article is a PNAS Direct Submission. viral dsRNA triggers an antiviral RNAi response (4, 5). Freely available online through the PNAS open access option. Studies in insects like Drosophila melanogaster and mosquitoes Data deposition: The sequence reported in this paper has been deposited in the Sequence Read Archive database (accession no. SRA048623). support a model in which viral dsRNA is processed by Dicer-2 1A.W.B. and K.W.R.v.C. contributed equally to this work. (Dcr-2) into viral small interfering RNAs (vsiRNAs). These 2Present address: Institut National de la Santé et de la Recherche Médicale, Unité Mixte de vsiRNAs are then incorporated into Argonaute-2 (AGO2) in the Recherche S 942, Hôpital Lariboisière, 75010 Paris, France; Département de Biologie, RNA-induced silencing complex (RISC), where they guide the Institut de Biologie Génétique et Bio Informatique, Université d’Evry-Val-d’Essonne, recognition and endonucleic cleavage of viral target RNAs (6–8). 91025 Evry, France; Assistance Publique-Hôpitaux de Paris, Groupe Hospitalo-Universi- taire Saint Louis-Lariboisière-Fernand Widal, Hôpital Lariboisière, Service de Biochimie Indeed, early seminal work in mosquitoes and Drosophila cells et de Biologie Moléculaire, Unité de Biologie Clinique Structurale, 75010 Paris, France. directly detected viral small RNAs by Northern blot analysis and 3To whom correspondence may be addressed. E-mail: [email protected] or r.vanrij@ demonstrated that knockdown of core RNAi genes resulted in an ncmls.ru.nl. – increase in virus replication (8 10). In accordance, in the genetic See Author Summary on page 20792 (volume 109, number 51). fl model organism D. melanogaster, ies with defects in Dcr-2, R2D2, This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. or AGO2 are unable to control RNA virus replication and, con- 1073/pnas.1207213109/-/DCSupplemental. E3604–E3613 | PNAS | Published online November 14, 2012 www.pnas.org/cgi/doi/10.1073/pnas.1207213109 Downloaded by guest on September 30, 2021 dsDNA viruses produce dsRNA during their replication, pre- PNAS PLUS sumably due to base pairing of convergent overlapping transcripts from both strands of the DNA genome (26–28). Whether such dsRNA is a bona fide target for Dcr-2 remains to be established. Although a dsDNA virus has recently been identified in wild- caught Drosophila innubila (29), a dsDNA virus that naturally infects D. melanogaster has yet to be discovered. Invertebrate iri- descent virus 6 (IIV-6), a member of the Iridovirus genus within the Iridoviridae family, has a broad host range; under experimental conditions it replicates in a number of Dipteran species, including D. melanogaster (30–32). We therefore used IIV-6, also known as Chilo iridescent virus, as a model to analyze the RNAi response against dsDNA viruses in Drosophila. IIV-6 is a large, complex virus with a dsDNA genome of 212,482 bp that encodes 211 pu- tative ORFs distributed along the two strands of the viral genome (33, 34). Here, we report that IIV-6 is a target of the RNAi ma- chinery. We demonstrate that Dcr-2 and AGO2 mutant flies are more sensitive to IIV-6 infection. Moreover, we identified Dcr-2– dependent vsiRNAs that map to both strands of the viral genome, show an uneven distribution across the viral genome, but are re- markably conserved between independent libraries. In accor- dance, we showed that both sense and antisense transcripts are generated in vivo and in vitro during IIV-6 replication, supporting a model in which viral dsRNA that is produced by bidirectional overlapping transcription is a target for Dcr-2. Together, our results indicate that RNAi provides antiviral defense against DNA viruses in Drosophila. Results IIV-6 as a Model to Study Antiviral Immunity Against DNA Viruses in Drosophila. We investigated the replication kinetics of IIV-6 in w1118 and Oregon-R (OR) WT flies. We inoculated adult flies intraabdominally with IIV-6 and monitored survival and viral titers over time. IIV-6 established a productive infection as revealed by iridescence in the eyes, thorax, and abdomen, which is the result of light reflection by assemblies of paracrystalline arrays of IIV-6 particles (35) (Fig. 1A). Accordingly, IIV-6 virion coat proteins were detected by Western blot analysis in total lysates of IIV-6– infected flies (Fig.
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