Characterization of PA-N terminal domain of Influenza A polymerase reveals sequence specific RNA cleavage

Nucleic Acids Research

Volumn 41, Issue 17, 2013, Pages 8289-8299

  Datta, Kausiki ^a   Wolkerstorfer, Andrea ^b   Szolar, Oliver H J ^b   Cusack, Stephen ^c   Klumpp, Klaus ^a,d  

^a HOFFMANN LA ROCHE INC   (United States)

^b Savira Pharmaceuticals GmbH   (Austria)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^d RiboScience LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPPED RNA; ENDONUCLEASE; GUANINE NUCLEOTIDE BINDING PROTEIN; INFLUENZA A POLYMERASE; MICROBIAL ENZYME; PA PROTEIN; PB2 PROTEIN; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; VIRUS ENZYME; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME LOCALIZATION; MOLECULAR DYNAMICS; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RNA CLEAVAGE; SEQUENCE ANALYSIS;

BASE SEQUENCE; ENDORIBONUCLEASES; INFLUENZA A VIRUS; PROTEIN STRUCTURE, TERTIARY; RIBONUCLEOPROTEINS; RNA; RNA CAPS; RNA CLEAVAGE; RNA REPLICASE; SUBSTRATE SPECIFICITY; VIRAL PROTEINS;

EID: 84884961327     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt603     Document Type: Article

References (29)

1. Ruigrok,R.W., Crepin,T., Hart,D.J. and Cusack,S. (2010) Towards an atomic resolution understanding of the influenza virus replication machinery. Curr. Opin. Struct. Biol., 20, 104-113.
2. Das,K., Aramini,J.M., Ma,L.C., Krug,R.M. and Arnold,E. (2010) Structures of influenza A proteins and insights into antiviral drug targets. Nat. Struct. Mol. Biol., 17, 530-538.
3. Boivin,S., Cusack,S., Ruigrok,R.W. and Hart,D.J. (2010) Influenza A virus polymerase: structural insights into replication and host adaptation mechanisms. J. Biol. Chem., 285, 28411-28417.
4. Newcomb,L.L., Kuo,R.L., Ye,Q., Jiang,Y., Tao,Y.J. and Krug,R.M. (2009) Interaction of the influenza a virus nucleocapsid protein with the viral RNA polymerase potentiates unprimed viral RNA replication. J. Virol., 83, 29-36.
5. Guilligay,D., Tarendeau,F., Resa-Infante,P., Coloma,R., Crepin,T., Sehr,P., Lewis,J., Ruigrok,R.W., Ortin,J., Hart,D.J. et al. (2008) The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat. Struct. Mol. Biol., 15, 500-506. (Pubitemid 351653591)
6. Dias,A., Bouvier,D., Crepin,T., McCarthy,A.A., Hart,D.J., Baudin,F., Cusack,S. and Ruigrok,R.W. (2009) The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature, 458, 914-918.
7. Yuan,P., Bartlam,M., Lou,Z., Chen,S., Zhou,J., He,X., Lv,Z., Ge,R., Li,X., Deng,T. et al. (2009) Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature, 458, 909-913.
8. DuBois,R.M., Slavish,P.J., Baughman,B.M., Yun,M.K., Bao,J., Webby,R.J., Webb,T.R. and White,S.W. (2012) Structural and biochemical basis for development of influenza virus inhibitors targeting the PA endonuclease. PLoS Pathog., 8, e1002830.
9. Kowalinski,E., Zubieta,C., Wolkerstorfer,A., Szolar,O.H., Ruigrok,R.W. and Cusack,S. (2012) Structural analysis of specific metal chelating inhibitor binding to the endonuclease domain of influenza pH1N1 (2009) polymerase. PLoS Pathog., 8, e1002831.
10. Doan,L., Handa,B., Roberts,N.A. and Klumpp,K. (1999) Metal ion catalysis of RNA cleavage by the influenza virus endonuclease. Biochemistry, 38, 5612-5619.
11. Crepin,T., Dias,A., Palencia,A., Swale,C., Cusack,S. and Ruigrok,R.W. (2010) Mutational and metal binding analysis of the endonuclease domain of the influenza virus polymerase PA subunit. J. Virol., 84, 9096-9104.
12. Klumpp,K., Hooker,L. and Handa,B. (2001) Influenza virus endoribonuclease. Methods Enzymol., 342, 451-466. (Pubitemid 32911964)
13. Klumpp,K., Doan,L., Roberts,N.A. and Handa,B. (2000) RNA and DNA hydrolysis are catalyzed by the influenza virus endonuclease. J. Biol. Chem., 275, 6181-6188. (Pubitemid 30129904)
14. Kennedy,W.P., Momand,J.R. and Yin,Y.W. (2007) Mechanism for de novo RNA synthesis and initiating nucleotide specificity by t7 RNA polymerase. J. Mol. Biol., 370, 256-268. (Pubitemid 46829207)
15. Datta,K., Johnson,N.P., LiCata,V.J. and von Hippel,P.H. (2009) Local conformations and competitive binding affinities of singleand double-stranded primer-template DNA at the polymerization and editing active sites of DNA polymerases. J. Biol. Chem., 284, 17180-17193.
16. Datta,K., Johnson,N.P. and von Hippel,P.H. (2006) Mapping the conformation of the nucleic acid framework of the T7 RNA polymerase elongation complex in solution using low-energy CD and fluorescence spectroscopy. J. Mol. Biol., 360, 800-813. (Pubitemid 43993923)
17. Jose,D., Datta,K., Johnson,N.P. and von Hippel,P.H. (2009) Spectroscopic studies of position-specific DNA ''breathing'' fluctuations at replication forks and primer-template junctions. Proc. Natl Acad. Sci. USA, 106, 4231-4236.
18. Geerts-Dimitriadou,C., Zwart,M.P., Goldbach,R. and Kormelink,R. (2011) Base-pairing promotes leader selection to prime in vitro influenza genome transcription. Virology, 409, 17-26.
19. Rao,P., Yuan,W. and Krug,R.M. (2003) Crucial role of CA cleavage sites in the cap-snatching mechanism for initiating viral mRNA synthesis. EMBO J., 22, 1188-1198. (Pubitemid 36313602)
20. Shaw,M.W. and Lamb,R.A. (1984) A specific sub-set of host-cell mRNAs prime influenza virus mRNA synthesis. Virus Res., 1, 455-467. (Pubitemid 14047970)
21. Caton,A.J. and Robertson,J.S. (1980) Structure of the hostderived sequences present at the 50 ends of influenza virus mRNA. Nucleic Acids Res., 8, 2591-2603. (Pubitemid 10023569)
22. Beaton,A.R. and Krug,R.M. (1981) Selected host cell capped RNA fragments prime influenza viral RNA transcription in vivo. Nucleic Acids Res., 9, 4423-4436. (Pubitemid 12195777)
23. Plotch,S.J., Bouloy,M., Ulmanen,I. and Krug,R.M. (1981) A unique cap(m7GpppXm)-dependent influenza virion endonuclease cleaves capped RNAs to generate the primers that initiate viral RNA transcription. Cell, 23, 847-858. (Pubitemid 11156997)
24. Zhao,C., Lou,Z., Guo,Y., Ma,M., Chen,Y., Liang,S., Zhang,L., Chen,S., Li,X., Liu,Y. et al. (2009) 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., 83, 9024-9030.
25. Cheng,E. and Mir,M.A. (2012) Signatures of host mRNA 50 terminus for efficient hantavirus cap snatching. J. Virol., 86, 10173-10185.
26. Duijsings,D., Kormelink,R. and Goldbach,R. (2001) In vivo analysis of the TSWV cap-snatching mechanism: single base complementarity and primer length requirements. EMBO J., 20, 2545-2552. (Pubitemid 32452873)
27. Jin,H. and Elliott,R.M. (1993) Non-viral sequences at the 50 ends of Dugbe nairovirus S mRNAs. J. Gen. Virol., 74(Pt 10), 2293-2297. (Pubitemid 23299911)
28. Jin,H. and Elliott,R.M. (1993) Characterization of Bunyamwera virus S RNA that is transcribed and replicated by the L protein expressed from recombinant vaccinia virus. J. Virol., 67, 1396-1404. (Pubitemid 23067646)
29. Bouloy,M., Plotch,S.J. and Krug,R.M. (1980) Both the 7-methyl and the 20-O-methyl groups in the cap of mRNA strongly influence its ability to act as primer for influenza virus RNA transcription. Proc. Natl Acad. Sci. USA, 77, 3952-3956. (Pubitemid 10015498)