RNase III nucleases from diverse kingdoms serve as antiviral effectors

Nature

Volumn 547, Issue 7661, 2017, Pages 114-117

  Aguado, Lauren C ^a   Schmid, Sonja ^a   May, Jared ^b   Sabin, Leah R ^c   Panis, Maryline ^a   Blanco Melo, Daniel ^a   Shim, Jaehee V ^a   Sachs, David ^a   Cherry, Sara ^c   Simon, Anne E ^b   Levraud, Jean Pierre ^d   TenOever, Benjamin R ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Bldg 142   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; RIBONUCLEASE III; VIRUS RNA; RNA DIRECTED RNA POLYMERASE;

BIOCHEMISTRY; COMPARTMENTALIZATION; DNA; GENETIC ANALYSIS; MEMBRANE; PROKARYOTE; PROTEIN; RNA; TRANSLOCATION; VIRUS;

ALLELE; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EUKARYOTE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA VIRUS; LANGAT VIRUS; NEGATIVE-STRAND RNA VIRUS; NONHUMAN; NORTHERN BLOTTING; PRIORITY JOURNAL; PROKARYOTE; PROTOPLAST; RNA BINDING; RNA INTERFERENCE; RNA SEQUENCE; RNA SYNTHESIS; RNA-BINDING DOMAIN; ROSS RIVER VIRUS; SENDAI VIRUS; SEQUENCE ALIGNMENT; STEREOSPECIFICITY; STOP CODON; WESTERN BLOTTING; ZEBRA FISH; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; CONFORMATION; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR EVOLUTION; PROTEIN DOMAIN; RNA VIRUS; VIRUS REPLICATION;

ARTHROPODA; EUKARYOTA; MAMMALIA; PROKARYOTA; RNA VIRUSES;

ANIMALS; ANTIVIRAL AGENTS; EVOLUTION, MOLECULAR; HUMANS; NUCLEIC ACID CONFORMATION; PROTEIN DOMAINS; RIBONUCLEASE III; RNA REPLICASE; RNA VIRUSES; RNA, VIRAL; VIRUS REPLICATION;

EID: 85022324533     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature22990     Document Type: Article

References (39)

1. Koonin, E. V., Wolf, Y. I., Nagasaki, K. & Dolja, V. V. The Big Bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat. Rev. Microbiol. 6, 925-939 (2008).
2. tenOever, B. R. The evolution of antiviral defense systems. Cell Host Microbe 19, 142-149 (2016).
3. tenOever, B. R. RNA viruses and the host microRNA machinery. Nat. Rev. Microbiol. 11, 169-180 (2013).
4. Cerutti, H. & Casas-Mollano, J. A. On the origin and functions of RNA-mediated silencing: from protists to man. Curr. Genet. 50, 81-99 (2006).
5. Obbard, D. J., Jiggins, F. M., Halligan, D. L. & Little, T. J. Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr. Biol. 16, 580-585 (2006).
6. Shapiro, J. S., Langlois, R. A., Pham, A. M. & Tenoever, B. R. Evidence for a cytoplasmic microprocessor of pri-miRNAs. RNA 18, 1338-1346 (2012).
7. Shapiro, J. S., Varble, A., Pham, A. M. & Tenoever, B. R. Noncanonical cytoplasmic processing of viral microRNAs. RNA 16, 2068-2074 (2010).
8. Rouha, H., Thurner, C. & Mandl, C. W. Functional microRNA generated from a cytoplasmic RNA virus. Nucleic Acids Res. 38, 8328-8337 (2010).
9. Bogerd, H. P., Whisnant, A. W., Kennedy, E. M., Flores, O. & Cullen, B. R. Derivation and characterization of Dicer- and microRNA-deficient human cells. RNA 20, 923-937 (2014).
10. Han, J. et al. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 18, 3016-3027 (2004).
11. Triboulet, R., Chang, H. M., Lapierre, R. J. & Gregory, R. I. Post-transcriptional control of DGCR8 expression by the Microprocessor. RNA 15, 1005-1011 (2009).
12. Tang, X., Zhang, Y., Tucker, L. & Ramratnam, B. Phosphorylation of the RNase III enzyme Drosha at serine300 or serine302 is required for its nuclear localization. Nucleic Acids Res. 38, 6610-6619 (2010).
13. Court, D. L. et al. RNase III: genetics and function; structure and mechanism. Annu. Rev. Genet. 47, 405-431 (2013).
14. Shirako, Y., Strauss, E. G. & Strauss, J. H. Modification of the 5′ terminus of Sindbis virus genomic RNA allows nsP4 RNA polymerases with nonaromatic amino acids at the N terminus to function in RNA replication. J. Virol. 77, 2301-2309 (2003).
15. Tsetsarkin, K. A., Liu, G., Shen, K. & Pletnev, A. G. Kissing-loop interaction between 5′ and 3′ ends of tick-borne Langat virus genome 'bridges the gap' between mosquito- and tick-borne flaviviruses in mechanisms of viral RNA cyclization: applications for virus attenuation and vaccine development. Nucleic Acids Res. 44, 3330-3350 (2016).
16. Bick, M. J. et al. Expression of the zinc-finger antiviral protein inhibits alphavirus replication. J. Virol. 77, 11555-11562 (2003).
17. Rupp, J. C., Jundt, N. & Hardy, R. W. Requirement for the amino-terminal domain of sindbis virus nsP4 during virus infection. J. Virol. 85, 3449-3460 (2011).
18. Moy, R. H. et al. Stem-loop recognition by DDX17 facilitates miRNA processing and antiviral defense. Cell 158, 764-777 (2014).
19. Shapiro, J. S. et al. Drosha as an interferon-independent antiviral factor. Proc. Natl Acad. Sci. USA 111, 7108-7113 (2014).
20. Sabin, L. R. et al. Dicer-2 processes diverse viral RNA species. PLoS ONE 8, e55458 (2013).
21. Sarkar, D., Desalle, R. & Fisher, P. B. Evolution of MDA-5/RIG-I-dependent innate immunity: independent evolution by domain grafting. Proc. Natl Acad. Sci. USA 105, 17040-17045 (2008).
22. Maillard, P. V. et al. Inactivation of the type I interferon pathway reveals long double-stranded RNA-mediated RNA interference in mammalian cells. EMBO J. 35, 2505-2518 (2016).
23. Seo, G. J. et al. Reciprocal inhibition between intracellular antiviral signaling and the RNAi machinery in mammalian cells. Cell Host Microbe 14, 435-445 (2013).
24. Varble, A. et al. An in vivo RNAi screening approach to identify host determinants of virus replication. Cell Host Microbe 14, 346-356 (2013).
25. Cheng, E. H., Levine, B., Boise, L. H., Thompson, C. B. & Hardwick, J. M. Bax-independent inhibition of apoptosis by Bcl-XL. Nature 379, 554-556 (1996).
26. Zhang, F. & Simon, A. E. A novel procedure for the localization of viral RNAs in protoplasts and whole plants. Plant J. 35, 665-673 (2003).
27. Perez, J. T. et al. MicroRNA-mediated species-specific attenuation of influenza A virus. Nat. Biotechnol. 27, 572-576 (2009).
28. Cherry, S. & Perrimon, N. Entry is a rate-limiting step for viral infection in a Drosophila melanogaster model of pathogenesis. Nat. Immunol. 5, 81-87 (2004).
29. Chong, M. M., Rasmussen, J. P., Rudensky, A. Y. & Littman, D. R. The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J. Exp. Med. 205, 2005-2017 (2008).
30. Ossovskaya, V., Lim, S. T., Ota, N., Schlaepfer, D. D. & Ilic, D. FAK nuclear export signal sequences. FEBS Lett. 582, 2402-2406 (2008).
31. Pall, G. S. & Hamilton, A. J. Improved northern blot method for enhanced detection of small RNA. Nat. Protocols 3, 1077-1084 (2008).
32. Robinson, J. T. et al. Integrative genomics viewer. Nat. Biotechnol. 29, 24-26 (2011).
33. Sedano, C. D. & Sarnow, P. Hepatitis C virus subverts liver-specific miR-122 to protect the viral genome from exoribonuclease Xrn2. Cell Host Microbe 16, 257-264 (2014).
34. Manley, J. L. SELEX to identify protein-binding sites on RNA. Cold Spring Harb. Protoc. 2013, 156-163 (2013).
35. Rio, D. C. Electrophoretic mobility shift assays for RNA-protein complexes. Cold Spring Harb. Protoc. 2014, 435-440 (2014).
36. Lee, Y. et al. The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419 (2003).
37. Hardy, R. W. & Rice, C. M. Requirements at the 3′ end of the sindbis virus genome for efficient synthesis of minus-strand RNA. J. Virol. 79, 4630-4639 (2005).
38. McCormack, J. C. & Simon, A. E. in Current Protocols in Microbiology Ch. 16, Unit 16D.1 (Wiley, 2006).
39. Shaffer, S. M., Wu, M. T., Levesque, M. J. & Raj, A. Turbo FISH: a method for rapid single molecule RNA FISH. PLoS ONE 8, e75120 (2013).