Structural perspective on the formation of ribonucleoprotein complex in negative-sense single-stranded RNA viruses

Trends in Microbiology

Volumn 21, Issue 9, 2013, Pages 475-484

  Zhou, Honggang ^a,b   Sun, Yuna ^c   Guo, Yu ^a   Lou, Zhiyong ^b  

^a NANKAI UNIVERSITY   (China)

^b Tsinghua University   (China)

^c INSTITUTE OF BIOPHYSICS   (China)

Author keywords

Antiviral drugs; Formation; Negative sense single stranded RNA virus; Ribonucleoprotein complex; Structure

Indexed keywords

RIBONUCLEOPROTEIN; VIRUS NUCLEOPROTEIN;

ARENAVIRUS; BUNYAVIRUS; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CRYSTALLOGRAPHY; ELECTRON MICROSCOPY; INFLUENZA VIRUS; NEGATIVE SENSE SINGLE STRANDED RNA VIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN FUNCTION; REVIEW; RNA VIRUS; STRUCTURE ANALYSIS;

RNA VIRUSES;

ANTIVIRAL DRUGS; FORMATION; NEGATIVE-SENSE SINGLE-STRANDED RNA VIRUS; RIBONUCLEOPROTEIN COMPLEX; STRUCTURE;

ANIMALS; HUMANS; RIBONUCLEOPROTEINS; RNA VIRUSES; RNA, VIRAL; VIRAL PROTEINS; VIRUS DISEASES;

EID: 84883795344     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2013.07.006     Document Type: Review

References (54)

1. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses 2012, Academic Press. A.M.Q. King (Ed.).
2. Kranzusch P.J., Whelan S.P. Architecture and regulation of negative-strand viral enzymatic machinery. RNA Biol. 2012, 9:941-948.
3. Hastie K.M., et al. Structure of the Lassa virus nucleoprotein reveals a dsRNA-specific 3? to 5? exonuclease activity essential for immune suppression. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:2396-2401.
4. Hastie K.M., et al. Crystal structure of the Lassa virus nucleoprotein-RNA complex reveals a gating mechanism for RNA binding. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:19365-19370.
5. Qi X., et al. Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 2011, 468:779-783.
6. Dong H., et al. Structure of Schmallenberg orthobunyavirus nucleoprotein suggests a novel mechanism of genome encapsidation. J. Virol. 2013, 87:5593-5601.
7. Ferron F., et al. The hexamer structure of Rift Valley fever virus nucleoprotein suggests a mechanism for its assembly into ribonucleoprotein complexes. PLoS Pathog. 2011, 7:e1002030.
8. Guo Y., et al. Crimean-Congo hemorrhagic fever virus nucleoprotein reveals endonuclease activity in bunyaviruses. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:5046-5051.
9. Jiao L., et al. Structure of severe Fever with thrombocytopenia syndrome virus nucleocapsid protein in complex with suramin reveals therapeutic potential. J. Virol. 2013, 87:6829-6839.
10. Li B., et al. Bunyamwera virus possesses a distinct nucleocapsid protein to facilitate genome encapsidation. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:9048-9053.
11. Niu F., et al. Structure of the Leanyer orthobunyavirus nucleoprotein-RNA complex reveals unique architecture for RNA encapsidation. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:9054-9059.
12. Raymond D.D., et al. Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:11769-11774.
13. Ng A.K., et al. Structure of the influenza virus A H5N1 nucleoprotein: implications for RNA binding, oligomerization, and vaccine design. FASEB J. 2008, 22:3638-3647.
14. Ye Q., et al. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 2006, 444:1078-1082.
15. Arranz R., et al. The structure of native influenza virion ribonucleoproteins. Science 2013, 338:1634-1637.
16. Chenavas S., et al. Monomeric nucleoprotein of influenza a virus. PLoS Pathog. 2013, 9:e1003275.
17. Moeller A., et al. Organization of the influenza virus replication machinery. Science 2013, 338:1631-1634.
18. Green T.J., et al. Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 2006, 313:357-360.
19. Albertini A.A., et al. Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 2006, 313:360-363.
20. Tawar R.G., et al. Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 2009, 326:1279-1283.
21. Ge P., et al. Cryo-EM model of the bullet-shaped vesicular stomatitis virus. Science 2010, 327:689-693.
22. Desfosses A., et al. Self-organization of the vesicular stomatitis virus nucleocapsid into a bullet shape. Nat. Commun. 2013, 4:1429.
23. Buchmeier M.J., et al. Arenaviridae: the viruses and their replication. Fields Virology 2007, 1791-1827. Lippincott Williams & Wilkins. 5th edn. D.M. Knipe, P.M. Howley (Eds.).
24. Martinez-Sobrido L., et al. Differential inhibition of type I interferon induction by arenavirus nucleoproteins. J. Virol. 2007, 81:12696-12703.
25. Brunotte L., et al. Structure of the Lassa virus nucleoprotein revealed by X-ray crystallography, small-angle X-ray scattering, and electron microscopy. J. Biol. Chem. 2011, 286:38748-38756.
26. Raymond D.D., et al. Phleboviruses encapsidate their genomes by sequestering RNA bases. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:19208-19213.
27. Yu X.J., et al. Fever with thrombocytopenia associated with a novel bunyavirus in China. N. Engl. J. Med. 2011, 364:1523-1532.
28. Zhou H., et al. The nucleoprotein of severe fever with thrombocytopenia syndrome virus processes a stable hexameric ring to facilitate RNA encapsidation. Protein Cell 2013, 4:445-455.
29. Carter S.D., et al. Structure, function, and evolution of the Crimean-Congo hemorrhagic Fever virus nucleocapsid protein. J. Virol. 2012, 86:10914-10923.
30. Wang Y., et al. Structure of Crimean-Congo hemorrhagic fever virus nucleoprotein: superhelical homo-oligomers and the role of caspase-3 cleavage. J. Virol. 2012, 86:12294-12303.
31. Reguera J., et al. Structural basis for encapsidation of genomic RNA by La Crosse Orthobunyavirus nucleoprotein. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:7246-7251.
32. Dong H., et al. Crystal structure of Schmallenberg orthobunyavirus nucleoprotein-RNA complex reveals a novel RNA sequestration mechanism. RNA 2013, 19:1129-1136.
33. Ariza A., et al. Nucleocapsid protein structures from orthobunyaviruses reveal insight into ribonucleoprotein architecture and RNA polymerization. Nucleic Acids Res. 2013, 41:5912-5926.
34. Yuan P., et al. Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 2009, 458:909-913.
35. Zhao C., et al. Nucleoside monophosphate complex structures of the endonuclease domain from the influenza virus polymerase PA subunit reveal the substrate binding site inside the catalytic center. J. Virol. 2009, 83:9024-9030.
36. Liu Y., et al. Structure-function studies of the influenza virus RNA polymerase PA subunit. Sci. China C: Life Sci. 2009, 52:450-458.
37. Morin B., et al. The polymerase of negative-stranded RNA viruses. Curr. Opin. Virol. 2013, 3:103-110.
38. Ng A.K., et al. Structural basis for RNA binding and homo-oligomer formation by influenza B virus nucleoprotein. J. Virol. 2012, 86:6758-6767.
39. Jiang X., et al. Structures of arenaviral nucleoproteins with triphosphate dsRNA reveal a unique mechanism of immune suppression. J. Biol. Chem. 2013, 288:16949-16959.
40. Hastie K.M., et al. Structural basis for the dsRNA specificity of the Lassa virus NP exonuclease. PLoS ONE 2012, 7:e44211.
41. Kao R.Y., et al. Identification of influenza A nucleoprotein as an antiviral target. Nat. Biotechnol. 2010, 28:600-605.
42. Gerritz S.W., et al. Inhibition of influenza virus replication via small molecules that induce the formation of higher-order nucleoprotein oligomers. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:15366-15371.
43. He X., et al. Crystal structure of the polymerase PA(C)-PB1(N) complex from an avian influenza H5N1 virus. Nature 2008, 454:1123-1126.
44. Wunderlich K., et al. Identification of high-affinity PB1-derived peptides with enhanced affinity to the PA protein of influenza A virus polymerase. Antimicrob. Agents Chemother. 2011, 55:696-702.
45. Wunderlich K., et al. Identification of a PA-binding peptide with inhibitory activity against influenza A and B virus replication. PLoS ONE 2009, 4:e7517.
46. Manz B., et al. Disruption of the viral polymerase complex assembly as a novel approach to attenuate influenza A virus. J. Biol. Chem. 2011, 286:8414-8424.
47. Ruigrok R.W., et al. Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr. Opin. Microbiol. 2011, 14:504-510.
48. Kranzusch P.J., Whelan S.P. Arenavirus Z protein controls viral RNA synthesis by locking a polymerase-promoter complex. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:19743-19748.
49. Guu T.S., et al. Bunyavirus: structure and replication. Adv. Exp. Med. Biol. 2012, 726:245-266.
50. Robb N.C., et al. The influenza A virus NS1 protein interacts with the nucleoprotein of viral ribonucleoprotein complexes. J. Virol. 2011, 85:5228-5231.
51. Rizzetto M. Hepatitis D: thirty years after. J. Hepatol. 2009, 50:1043-1050.
52. Mielke-Ehret N., Muhlbach H.P. Emaravirus: a novel genus of multipartite, negative strand RNA plant viruses. Viruses 2012, 4:1515-1536.
53. Kormelink R., et al. Negative-strand RNA viruses: the plant-infecting counterparts. Virus Res. 2011, 162:184-202.
54. Mir M.A., Panganiban A.T. Trimeric hantavirus nucleocapsid protein binds specifically to the viral RNA panhandle. J. Virol. 2004, 78:8281-8288.