Dicer-2-Dependent Generation of Viral DNA from Defective Genomes of RNA Viruses Modulates Antiviral Immunity in Insects

Autor: Louis Lambrechts, Maria-Carla Saleh, Sophie Lanciano, Marco Vignuzzi, Hyelee Loyd, Lorena Tomé-Poderti, Hervé Blanc, Valérie Gausson, Enzo Z. Poirier, Bertsy Goic, Lionel Frangeul, Thomas Vallet, Laura I. Levi, Sarah H. Merkling, Susan Carpenter, Marie Mirouze, Chloé Baron, Jeremy Boussier
Přispěvatelé: Virus et Interférence ARN - Viruses and RNA Interference, Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS), Populations virales et Pathogenèse - Viral Populations and Pathogenesis, Cellule Pasteur, Université Paris Diderot - Paris 7 (UPD7)-PRES Sorbonne Paris Cité, Immunobiologie des Cellules dendritiques, Institut Pasteur [Paris] (IP)-Institut National de la Santé et de la Recherche Médicale (INSERM), Iowa State University (ISU), Diversité, adaptation, développement des plantes (UMR DIADE), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud]), Interactions Virus-Insectes - Insect-Virus Interactions (IVI), Work was supported by the French Government’s Investissement d’Avenir program, Laboratoire d’Excellence Integrative Biology of Emerging Infectious Diseases (grant ANR-10-LABX-62-IBEID to L.L., M.V., and M.-C.S.), the European Research Council (FP7/2013-2019 ERC CoG 615220 to M.-C.S.), and the DARPA INTERCEPT program managed by Dr. Jim Gimlett and administered though DARPA Cooperative Agreement #HR0011-17-2-0023 to M.V. and M.-C.S. (the content of the information does not necessarily reflect the position or the policy of the U.S. government, and no official endorsement should be inferred). L.L. was supported by the City of Paris Emergence(s) program in Biomedical Research (grant DASES 2013-33) and by the European Union’s Horizon 2020 research and innovation program under ZikaPLAN grant agreement No. 734584. L.T.-P. is a Marie Skłodowska-Curie actions fellow (H2020 MSCA-IF 656398-DDRR)., We thank the Saleh and Vignuzzi labs, especially V. Mongelli, L. Carrau, and G. Moratorio for scientific advice, and B. tenOever for discussions. We thank Jean-Luc Imler for the various fly strains. We thank Catherine Lallemand for mosquito rearing and Alongkot Ponlawat for field collection of mosquitoes, ANR-10-LABX-0062,IBEID,Integrative Biology of Emerging Infectious Diseases(2010), European Project: 615220,EC:FP7:ERC,ERC-2013-CoG,RNAIMMUNITY(2015), European Project: 734584,ZikaPLAN, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris], Institut Pasteur [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM), Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)
Jazyk: angličtina
Rok vydání: 2018
Předmět:
0301 basic medicine
Ribonuclease III
Small interfering RNA
Genes
Viral

MESH: Drosophila
[SDV]Life Sciences [q-bio]
Virus Replication
Dicer-2
DEAD-box RNA Helicases
RNA Virus Infections
MESH: Ribonuclease III
RNA interference
MESH: Arboviruses
MESH: RNA
Small Interfering

Drosophila Proteins
MESH: Animals
RNA
Small Interfering

MESH: Genes
Viral

biology
MESH: RNA Helicases
persistence
Viral Load
3. Good health
Cell biology
MESH: RNA
Viral

Host-Pathogen Interactions
[SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology
RNA
Viral

[SDV.IMM]Life Sciences [q-bio]/Immunology
Drosophila
RNA Interference
MESH: Genome
Viral

MESH: Viral Load
MESH: RNA Viruses
RNA Helicases
MESH: Antiviral Agents
RNA virus
MESH: Drosophila Proteins
MESH: RNA Interference
Genome
Viral

Microbiology
Antiviral Agents
Virus
03 medical and health sciences
Virology
[SDV.BBM.GTP]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Genomics [q-bio.GN]

Animals
Point Mutation
RNA Viruses
MESH: DEAD-box RNA Helicases
[SDV.BBM]Life Sciences [q-bio]/Biochemistry
Molecular Biology

MESH: Point Mutation
030102 biochemistry & molecular biology
MESH: RNA Virus Infections
fungi
MESH: Virus Replication
MESH: Host-Pathogen Interactions
circular viral DNA
RNA
[SDV.BBM.BM]Life Sciences [q-bio]/Biochemistry
Molecular Biology/Molecular biology

biology.organism_classification
Reverse transcriptase
MESH: DNA
Viral

030104 developmental biology
Culicidae
arbovirus
Viral replication
RNAi
DNA
Viral

biology.protein
defective viral genomes
Parasitology
insect
MESH: Culicidae
Arboviruses
Dicer
Zdroj: Cell Host and Microbe
Cell Host and Microbe, 2018, 23 (3), pp.353-365.e8. ⟨10.1016/j.chom.2018.02.001⟩
Cell Host & Microbe
Cell Host and Microbe, Elsevier, 2018, 23 (3), pp.353-365.e8. ⟨10.1016/j.chom.2018.02.001⟩
ISSN: 1931-3128
Popis: International audience; The RNAi pathway confers antiviral immunity in insects. Virus-specific siRNA responses are amplified via the reverse transcription of viral RNA to viral DNA (vDNA). The nature, biogenesis, and regulation of vDNA are unclear. We find that vDNA produced during RNA virus infection of Drosophila and mosquitoes is present in both linear and circular forms. Circular vDNA (cvDNA) is sufficient to produce siRNAs that confer partially protective immunity when challenged with a cognate virus. cvDNAs bear homology to defective viral genomes (DVGs), and DVGs serve as templates for vDNA and cvDNA synthesis. Accordingly, DVGs promote the amplification of vDNA-mediated antiviral RNAi responses in infected Drosophila. Furthermore, vDNA synthesis is regulated by the DExD/H helicase domain of Dicer-2 in a mechanism distinct from its role in siRNA generation. We suggest that, analogous to mammalian RIG-I-like receptors, Dicer-2 functions like a pattern recognition receptor for DVGs to modulate antiviral immunity in insects.
Databáze: OpenAIRE