Influenza virus nucleoprotein: Structure, RNA binding, oligomerization and antiviral drug target

Future Microbiology

Volumn 8, Issue 12, 2013, Pages 1537-1545

  Chenavas, Sylvie ^a,b,c   Cre ́pin, Thibaut ^a,b,c   Delmas, Bernard ^d   Ruigrok, Rob W H ^a,b,c   Slama Schwok, Anny ^d  

^a UNIV GRENOBLE ALPES   (France)

^b CNRS   (France)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^d INRA Institut National de la Recherche Agronomique   (France)

Author keywords

antiviral; nucleoprotein; resistance; RNP; viral RNA

Indexed keywords

ANTIVIRUS AGENT; INFLUENZA VIRUS NUCLEOPROTEIN; MONOMER; NAPROXEN; OLIGOMER; RIBONUCLEOPROTEIN; RNA; TETRAMER; UNCLASSIFIED DRUG; VIRUS NUCLEOPROTEIN; VIRUS RNA;

ANTIVIRAL ACTIVITY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; INFLUENZA VIRUS; MUTANT; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN STRUCTURE; REVIEW; RNA BINDING; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

ANIMALS; ANTIVIRAL AGENTS; HUMANS; INFLUENZA A VIRUS; INFLUENZA, HUMAN; NUCLEOPROTEINS; RNA, VIRAL; VIRAL PROTEINS;

EID: 84889570600     PISSN: 17460913     EISSN: 17460921     Source Type: Journal    
DOI: 10.2217/fmb.13.128     Document Type: Review

References (35)

1. Ruigrok RWH, Crepin T, Kolakofsky D. Nucleoproteins and nucleocapsids of negative-strand RNA viruses. Curr. Opin. Microbiol. 14(4), 504-510 (2011).
2. Klumpp K, Ruigrok RW, Baudin F. Roles of the influenza virus polymerase and nucleoprotein in forming a functional RNP structure. EMBO J. 16(6), 1248-1257 (1997). (Pubitemid 27136091)
3. Fodor E, Pritlove DC, Brownlee GG. The influenza virus panhandle is involved in the initiation of transcription. J. Virol. 68(6), 4092-4096 (1994). (Pubitemid 24177444)
4. Hagen M, Chung TD, Butcher JA, Krystal M. Recombinant influenza virus polymerase: Requirement of both 5 ́ and 3 ́ viral ends for endonuclease activity. J. Virol. 68(3), 1509-1515 (1994).
5. Compans RW, Content J, Duesberg PH. Structure of the ribonucleoprotein of influenza virus. J. Virol. 10(4), 795-800 (1972).
6. Arranz R, Coloma R, Chichon FJ et al. The structure of native influenza virion ribonucleoproteins. Science 338(6114), 1634-1637 (2012).
7. Moeller A, Kirchdoerfer RN, Potter CS, Carragher B, Wilson IA. Organization of the influenza virus replication machinery. Science 338(6114), 1631-1634 (2012).
8. Ruigrok RW, Baudin F. Structure of influenza virus ribonucleoprotein particles. II. Purified RNA-free influenza virus ribonucleoprotein forms structures that are indistinguishable from the intact influenza virus ribonucleoprotein particles. J. Gen. Virol. 76(Pt 4), 1009-1014 (1995).
9. Ye Q, Krug RM, Tao YJ. The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 444(7122), 1078-1082 (2006). (Pubitemid 46018528)
10. Tarus B, Bakowiez O, Chenavas S et al. Oligomerization paths of the nucleoprotein of influenza A virus. Biochimie 94(3), 776-785 (2012).
11. Ye Q, Guu TS, Mata DA et al. Biochemical and structural evidence in support of a coherent model for the formation of the double-helical influenza A virus ribonucleoprotein. MBio 4(1), e00467-12 (2012).
12. Hutchinson EC, Denham EM, Thomas B et al. Mapping the phosphoproteome of influenza A and B viruses by mass spectrometry. PLoS Pathog. 8(11), e1002993 (2012).
13. Chenavas S, Estrozi LF, Slama-Schwok A et al. Monomeric nucleoprotein of influenza A virus. PLoS Pathog. 9(3), e1003275 (2013).
14. Boulo S, Akarsu H, Lotteau V, Muller CW, Ruigrok RWH, Baudin F. Human importin alpha and RNA do not compete for binding to influenza A virus nucleoprotein. Virology 409(1), 84-90 (2011).
15. Coloma R, Valpuesta JM, Arranz R, Carrascosa JL, Ortin J, Martin-Benito J. The structure of a biologically active influenza virus ribonucleoprotein complex. PLoS Pathog. 5(6), e1000491 (2009).
16. Ng AK-L, Zhang H, Tan K et al. Structure of the influenza virus A H5N1 nucleoprotein: Implications for RNA binding, oligomerization, and vaccine design. FASEB J. 22(10), 3638-3647 (2008).
17. Chan W-H, Ng AK-L, Robb NC et al. Functional analysis of the influenza virus H5N1 nucleoprotein tail loop reveals amino acids that are crucial for oligomerization and ribonucleoprotein activities. J. Virol. 84(14), 7337-7345 (2010).
18. Elton D, Medcalf E, Bishop K, Digard P. Oligomerization of the influenza virus nucleoprotein: Identification of positive and negative sequence elements. Virology 260(1), 190-200 (1999). (Pubitemid 29391747)
19. Elton D, Medcalf L, Bishop K, Harrison D, Digard P. Identification of amino acid residues of influenza virus nucleoprotein essential for RNA binding. J. Virol. 73(9), 7357-7367 (1999). (Pubitemid 29383219)
20. Shen Y-F, Chen Y-H, Chu S-Y et al. E339.R416 salt bridge of nucleoprotein as a feasible target for influenza virus inhibitors. Proc. Natl. Acad. Sci. USA 108(40), 16515-16520 (2011).
21. Turrell L, Lyall JW, Tiley LS, Fodor E, Vreede FT. The role and assembly mechanism of nucleoprotein in influenza A virus ribonucleoprotein complexes. Nat. Commun. 4, 1591 (2013).
22. Ng AK-L, Chan W-H, Choi S-T et al. Influenza polymerase activity correlates with the strength of interaction between nucleoprotein and PB2 through the host-specific residue K/E627. PLoS ONE 7(5), e36415 (2012).
23. Ng AK-L, Lam MK-H, Zhang H et al. Structural basis for RNA binding and homo-oligomer formation by influenza B virus nucleoprotein. J. Virol. 86(12), 6758-6767 (2012).
24. Jennings PA, Finch JT, Winter G, Robertson JS. Does the higher order structure of the influenza virus ribonucleoprotein guide sequence rearrangements in influenza viral RNA? Cell 34(2), 619-627 (1983).
25. Muller KH, Kakkola L, Nagaraj AS, Cheltsov AV, Anastasina M, Kainov DE. Emerging cellular targets for influenza antiviral agents. Trends Pharmacol. Sci. 33(2), 89-99 (2012).
26. Cianci C, Gerritz SW, Deminie C, Krystal M. Influenza nucleoprotein: Promising target for antiviral chemotherapy. Antiviral Chem. Chemother. doi:10.3851/IMP2235 (2012) (Epub ahead of print).
27. Cheng H, Wan J, Lin M-I et al. Design, synthesis, and in vitro biological evaluation of 1H-1,2,3-Triazole-4-carboxamide derivatives as new anti-influenza A agents targeting virus nucleoprotein. J. Med. Chem. 55(5), 2144-2153 (2012).
28. Gerritz SW, Cianci C, Kim S et al. Inhibition of influenza virus replication via small molecules that induce the formation of higher-order nucleoprotein oligomers. Proc. Natl. Acad. Sci. USA 108(37), 15366-15371 (2011).
29. Kao RY, Yang D, Lau L-S et al. Identification of influenza A nucleoprotein as an antiviral target. Nat. Biotechnol. 28(6), 600-605 (2010).
30. Su C-Y, Cheng T-JR, Lin M-I et al. High-Throughput identification of compounds targeting influenza RNA-dependent RNA polymerase activity. Proc. Natl. Acad. Sci. USA 107(45), 19151-19156 (2010).
31. Amorim MJ, Kao RY, Digard P. Nucleozin targets cytoplasmic trafficking of viral ribonucleoprotein-Rab11 complexes in influenza A virus infection. J. Virol. 87(8), 4694-4703 (2013).
32. Zimmermann P, Manz B, Haller O, Schwemmle M, Kochs G. The viral nucleoprotein determines Mx sensitivity of influenza A viruses. J. Virol. 85(16), 8133-8140 (2011).
33. Das K, Aramini JM, Ma L-C, Krug RM, Arnold E. Structures of influenza A proteins and insights into antiviral drug targets. Nat. Struct. Mol. Biol. 17(5), 530-538 (2010).
34. Li Z, Watanabe T, Hatta M et al. Mutational analysis of conserved amino acids in the influenza A virus nucleoprotein. J. Virol. 83(9), 4153-4162 (2009).
35. Lejal N, Tarus B, Bouguyon E et al. Structure-based discovery of the novel antiviral properties of naproxen against the nucleoprotein of influenza A virus. Antimicrob. Agents Chemother. 57(5), 2231-2242 (2013).