A Viral Protein Restricts Drosophila RNAi Immunity by Regulating Argonaute Activity and Stability

Arabinda Nayak, Dong Young Kim, Michael J. Trnka, Craig H. Kerr, Peter V. Lidsky, David J. Stanley, Brianna Monique Rivera, Kathy H. Li, Alma L. Burlingame, Eric Jan, Judith Frydman, John D. Gross, Raul Andino*

*Corresponding author for this work

Research output: Journal Publications and ReviewsRGC 21 - Publication in refereed journalpeer-review

32 Citations (Scopus)

Abstract

The dicistrovirus, Cricket paralysis virus (CrPV) encodes an RNA interference (RNAi) suppressor, 1A, which modulates viral virulence. Using the Drosophila model, we combined structural, biochemical, and virological approaches to elucidate the strategies by which CrPV-1A restricts RNAi immunity. The atomic resolution structure of CrPV-1A uncovered a flexible loop that interacts with Argonaute 2 (Ago-2), thereby inhibiting Ago-2 endonuclease-dependent immunity. Mutations disrupting Ago-2 binding attenuates viral pathogenesis in wild-type but not Ago-2-deficient flies. CrPV-1A also contains a BC-box motif that enables the virus to hijack a host Cul2-Rbx1-EloBC ubiquitin ligase complex, which promotes Ago-2 degradation and virus replication. Our study uncovers a viral-based dual regulatory program that restricts antiviral immunity by direct interaction with and modulation of host proteins. While the direct inhibition of Ago-2 activity provides an efficient mechanism to establish infection, the recruitment of a ubiquitin ligase complex enables CrPV-1A to amplify Ago-2 inactivation to restrict further antiviral RNAi immunity. Viruses suppress, and thereby evade, RNAi-mediated immunity via several distinct mechanisms, which are not well understood. In a Drosophila infection model, Nayak et al. reveal that the viral RNAi suppressor protein CrPV-1A utilizes a dual regulatory mechanism to evade RNAi-mediated immunity: direct enzymatic inhibition and E3-ligase-mediated degradation of Ago-2. © 2018
Original languageEnglish
Pages (from-to)542-557.e9
JournalCell Host and Microbe
Volume24
Issue number4
DOIs
Publication statusPublished - 10 Oct 2018
Externally publishedYes

Bibliographical note

Publication details (e.g. title, author(s), publication statuses and dates) are captured on an “AS IS” and “AS AVAILABLE” basis at the time of record harvesting from the data source. Suggestions for further amendments or supplementary information can be sent to [email protected].

Research Keywords

  • Ago-2
  • Ago-2 degradation
  • antiviral immunity
  • CrPV
  • E3 ligase
  • insects
  • RNAi
  • RNAi suppressor

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