The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription

PLoS Pathogens

Volumn 6, Issue 9, 2010, Pages

  Morin, Benjamin ^a   Coutard, Bruno ^a   Lelke, Michaela ^b   Ferron, François ^a   Kerber, Romy ^b   Jamal, Saïd ^a   Frangeul, Antoine ^a   Baronti, Cécile ^c   Charrel, Rémi ^c   de Lamballerie, Xavier ^c   Vonrhein, Clemens ^d   Lescar, Julien ^a,e   Bricogne, Gérard ^d   Günther, Stephan ^b   Canard, Bruno ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^c Aix Marseille University IRD 190 Inserm 1207   (France)

^d GLOBAL PHASING LTD   (United Kingdom)

^e NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ARENAVIRUS L PROTEIN; MESSENGER RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

AMINO TERMINAL SEQUENCE; ARENAVIRUS; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MUTAGENESIS; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN CROSS LINKING; REPLICON; RNA BINDING; RNA REPLICATION; RNA TRANSCRIPTION; VIRUS CHARACTERIZATION;

BUNYAVIRIDAE; CATALYTIC DOMAIN; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; ENDONUCLEASES; ENDORIBONUCLEASES; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MODELS, MOLECULAR; MUTAGENESIS; ORTHOMYXOVIRIDAE; PROTEIN STRUCTURE, TERTIARY; RNA, MESSENGER; RNA, VIRAL; TRANSCRIPTION, GENETIC;

ARENAVIRIDAE; ARENAVIRUS; BUNYAVIRIDAE; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; ORTHOMYXOVIRIDAE;

EID: 78149308100     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001038     Document Type: Article

References (58)

1. Briese T, Paweska JT, McMullan LK, Hutchison SK, Street C, et al. (2009) Genetic detection and characterization of Lujo virus, a new hemorrhagic fever-associated arenavirus from southern Africa. PLoS Pathog 5: e1000455.
2. Charrel RN, de Lamballerie X, Emonet S (2008) Phylogeny of the genus Arenavirus. Curr Opin Microbiol 11: 362-368.
3. Barton LL, Budd SC, Morfitt WS, Peters CJ, Ksiazek TG, et al. (1993) Congenital lymphocytic choriomeningitis virus infection in twins. Pediatr Infect Dis J 12: 942-946.
4. Barton LL, Hyndman NJ (2000) Lymphocytic choriomeningitis virus: reemerg-ing central nervous system pathogen. Pediatrics 105: E35.
5. Fischer SA, Graham MB, Kuehnert MJ, Kotton CN, Srinivasan A, et al. (2006) Transmission of lymphocytic choriomeningitis virus by organ transplantation. N Engl J Med 354: 2235-2249.
6. Palacios G, Druce J, Du L, Tran T, Birch C, et al. (2008) A new arenavirus in a cluster of fatal transplant-associated diseases. N Engl J Med 358: 991-998.
7. Meyer BJ, de la Torre JC, Southern PJ (2002) Arenaviruses: genomic RNAs, transcription, and replication. Curr Top Microbiol Immunol 262: 139-157.
8. Salvato MS, Shimomaye EM (1989) The completed sequence of lymphocytic choriomeningitis virus reveals a unique RNA structure and a gene for a zinc finger protein. Virology 173: 1-10.
9. Meyer BJ, Southern PJ (1993) Concurrent sequence analysis of 5 and 3 RNA termini by intramolecular circularization reveals 5′ nontemplated bases and 3′ terminal heterogeneity for lymphocytic choriomeningitis virus mRNAs. J Virol 67: 2621-2627.
10. Raju R, Raju L, Hacker D, Garcin D, Compans R, et al. (1990) Nontemplated bases at the 5′ ends of Tacaribe virus mRNAs. Virology 174: 53-59.
11. Polyak SJ, Zheng S, Harnish DG (1995) 5′ termini of Pichinde arenavirus S RNAs and mRNAs contain nontemplated nucleotides. J Virol 69: 3211-3215.
12. Plotch SJ, Bouloy M, Krug RM (1979) Transfer of 5′-terminal cap of globin mRNA to influenza viral complementary RNA during transcription in vitro. Proc Natl Acad Sci U S A 76: 1618-1622.
13. Plotch SJ, Bouloy M, Ulmanen I, Krug RM (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.
14. Bishop DH, Gay ME, Matsuoko Y (1983) Nonviral heterogeneous sequences are present at the 5′ ends of one species of snowshoe hare bunyavirus S complementary RNA. Nucleic Acids Res 11: 6409-6418.
15. Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, et al. (2009) The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458: 914-918.
16. Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, et al. (2009) Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458: 909-913.
17. Lopez N, Jacamo R, Franze-Fernandez MT (2001) Transcription and RNA replication of tacaribe virus genome and antigenome analogs require N and L proteins: Z protein is an inhibitor of these processes. J Virol 75: 12241-12251.
18. Muller R, Poch O, Delarue M, Bishop DH, Bouloy M (1994) Rift Valley fever virus L segment: correction of the sequence and possible functional role of newly identified regions conserved in RNA-dependent polymerases. J Gen Virol 75(Pt 6): 1345-1352.
19. Vieth S, Torda AE, Asper M, Schmitz H, Gunther S (2004) Sequence analysis of L RNA of Lassa virus. Virology 318: 153-168.
20. Lukashevich IS, Djavani M, Shapiro K, Sanchez A, Ravkov E, et al. (1997) The Lassa fever virus L gene: nucleotide sequence, comparison, and precipitation of a predicted 250 kDa protein with monospecific antiserum. J Gen Virol 78(Pt 3): 547-551.
21. Wilda M, Lopez N, Casabona JC, Franze-Fernandez MT (2008) Mapping of the tacaribe arenavirus Z-protein binding sites on the L protein identified both amino acids within the putative polymerase domain and a region at the N terminus of L that are critically involved in binding. J Virol 82: 11454-11460.
22. Holm L, Kaariainen S, Rosenstrom P, Schenkel A (2008) Searching protein structure databases with DaliLite v.3. Bioinformatics 24: 2780-2781.
23. Nichol STBBJ, Elliott RM (2005) Virus Taxonomy, VIIIth Report of the ICTV. In: Fauquet CM, Mayo AM, Maniloff J et al eds London: Elsevier Academic Press. pp 695-716.
24. Gro MC, Di Bonito P, Accardi L, Giorgi C (1992) Analysis of 3′ and 5′ ends of N and NSs messenger RNAs of Toscana Phlebovirus. Virology 191: 435-438.
25. Frias-Staheli N, Giannakopoulos NV, Kikkert M, Taylor SL, Bridgen A, et al. (2007) Ovarian tumor domain-containing viral proteases evade ubiquitin- and ISG15-dependent innate immune responses. Cell Host Microbe 2: 404-416.
26. Zhao C, Lou Z, Guo Y, Ma M, Chen 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.
27. Garcin D, Kolakofsky D (1990) A novel mechanism for the initiation of Tacaribe arenavirus genome replication. J Virol 64: 6196-6203.
28. Newman M, Strzelecka T, Dorner LF, Schildkraut I, Aggarwal AK (1994) Structure of restriction endonuclease BamHI and its relationship to EcoRI. Nature 368: 660-664.
29. Pingoud A, Fuxreiter M, Pingoud V, Wende W (2005) Type II restriction endonucleases: structure and mechanism. Cell Mol Life Sci 62: 685-707.
30. Lelke M, Brunotte L, Busch C, Gunther S (2010) An N-terminal region of Lassa virus L protein plays a critical role in transcription but not replication of the virus genome. J Virol 84: 1934-1944.
31. Guilligay D, Tarendeau F, Resa-Infante P, Coloma R, Crepin T, et al. (2008) The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 15: 500-506.
32. Abraham J, Corbett KD, Farzan M, Choe H, Harrison SC. Structural basis for receptor recognition by New World hemorrhagic fever arenaviruses. Nat Struct Mol Biol.
33. De Clercq E, Neyts J (2007) Avian influenza A (H5N1) infection: targets and strategies for chemotherapeutic intervention. Trends Pharmacol Sci 28: 280-285.
34. Hsieh HP, Hsu JT (2007) Strategies of development of antiviral agents directed against influenza virus replication. Curr Pharm Des 13: 3531-3542.
35. Parkes KE, Ermert P, Fassler J, Ives J, Martin JA, et al. (2003) Use of a pharmacophore model to discover a new class of influenza endonuclease inhibitors. J Med Chem 46: 1153-1164.
36. Powell HR (1999) The Rossmann Fourier autoindexing algorithm in MOSFLM. Acta Crystallogr D Biol Crystallogr 55: 1690-1695.
37. (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50: 760-763.
38. Emsley P, Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
39. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
40. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. The Pfam protein families database. Nucleic Acids Res 38: D211-222.
41. Malet H, Coutard B, Jamal S, Dutartre H, Papageorgiou N, et al. (2009) The crystal structures of Chikungunya and Venezuelan equine encephalitis virus nsP3 macro domains define a conserved adenosine binding pocket. J Virol 83: 6534-6545.
42. Hass M, Golnitz U, Muller S, Becker-Ziaja B, Gunther S (2004) Replicon system for Lassa virus. J Virol 78: 13793-13803.
43. Buchholz UJ, Finke S, Conzelmann KK (1999) Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73: 251-259.
44. Hass M, Lelke M, Busch C, Becker-Ziaja B, Gunther S (2008) Mutational evidence for a structural model of the Lassa virus RNA polymerase domain and identification of two residues, Gly1394 and Asp1395, that are critical for transcription but not replication of the genome. J Virol 82: 10207-10217.
45. Sutter G, Ohlmann M, Erfle V (1995) Non-replicating vaccinia vector efficiently expresses bacteriophage T7 RNA polymerase. FEBS Lett 371: 9-12.
46. Kabsch W Xds. Acta Crystallogr D Biol Crystallogr 66: 125-132.
47. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62: 72-82.
48. Vonrhein C, Blanc E, Roversi P, Bricogne G (2007) Automated structure solution with autoSHARP. Methods Mol Biol 364: 215-230.
49. Schneider TR, Sheldrick GM (2002) Substructure solution with SHELXD. Acta Crystallogr D Biol Crystallogr 58: 1772-1779.
50. Bricogne G, Vonrhein C, Flensburg C, Schiltz M, Paciorek W (2003) Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr D Biol Crystallogr 59: 2023-2030.
51. Cowtan K (1994) An automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallog-raphy 31: 34-38.
52. Cowtan K (2006) The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62: 1002-1011.
53. Abrahams JP, Leslie AG (1996) Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallogr D Biol Crystallogr52: 30-42.
54. Emsley P, Lohkamp B, Scott WG, Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501.
55. Bricogne G, Blanc E, Brandl M, Flensburg C, Keller P, et al. (2010) BUSTER version 2.X. Global Phasing Ltd. Cambridge, United Kingdom
56. Leslie AG (1992) MOSFLM - Recent changes and future developments. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography 35: 18-19.
57. Murshudov GN, Vagin AA, Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystal-logr 53: 240-255.
58. Smart O, Brandl M, Flensburg C, Keller P, Paciorek W, et al. (2008) Refinement with Local Structure Similarity Restraints (LSSR) Enables Exploitation of Information from Related Structures and Facilitates use of NCS. Annual Meeting of the American Crystallographic Association.