Cross-species analysis of the replication complex of old world arenaviruses reveals two nucleoprotein sites involved in L protein function

Journal of Virology

Volumn 85, Issue 23, 2011, Pages 12518-12528

  Kerber, Romy ^a   Rieger, Toni ^a   Busch, Carola ^a   Flatz, Lukas ^b,c   Pinschewer, Daniel D ^b,d   Kümmerer, Beate M ^a,e   Günther, Stephan ^a  

^a BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^b INSTITUTE OF EXPERIMENTAL IMMUNOLOGY   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROLIPOAMIDE DEHYDROGENASE; ISOLEUCINE; VIRUS NUCLEOPROTEIN;

ANIMAL CELL; ARENAVIRUS; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; GENE REPLICATION; GENETIC TRANSCRIPTION; IMMUNOPRECIPITATION; LASSA VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOPEIA VIRUS; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; REPLICON; REPORTER GENE; VERO CELL; VIRUS REPLICATION;

AMINO ACID SEQUENCE; ANIMALS; ARENAVIRIDAE INFECTIONS; ARENAVIRUSES, OLD WORLD; BLOTTING, NORTHERN; BLOTTING, WESTERN; CERCOPITHECUS AETHIOPS; DNA REPLICATION; DNA, VIRAL; IMMUNOPRECIPITATION; MOLECULAR SEQUENCE DATA; NUCLEOPROTEINS; REGULATORY ELEMENTS, TRANSCRIPTIONAL; REPLICON; RNA, VIRAL; SEQUENCE HOMOLOGY, AMINO ACID; SPECIES SPECIFICITY; TRANSCRIPTIONAL ACTIVATION; VERO CELLS; VIRAL PROTEINS;

ARENAVIRUS; LASSA VIRUS; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MOPEIA VIRUS; OLD WORLD ARENAVIRUSES;

EID: 81255184299     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05091-11     Document Type: Article

References (43)

1. Auperin, D. D., V. Romanowski, M. Galinski, and D. H. Bishop. 1984. Sequencing studies of pichinde arenavirus S RNA indicate a novel coding strategy, an ambisense viral S RNA. J. Virol. 52:897-904.
2. Auperin, D. D., D. R. Sasso, and J. B. McCormick. 1986. Nucleotide sequence of the glycoprotein gene and intergenic region of the Lassa virus S genome RNA. Virology 154:155-167.
3. Briese, T., B. Bird, V. Kapoor, S. T. Nichol, and W. I. Lipkin. 2006. Batai and Ngari viruses: M segment reassortment and association with severe febrile disease outbreaks in East Africa. J. Virol. 80:5627-5630.
4. Briese, T., V. Kapoor, and W. I. Lipkin. 2007. Natural M-segment reassortment in Potosi and Main Drain viruses: implications for the evolution of orthobunyaviruses. Arch. Virol. 152:2237-2247.
5. Brunotte, L., et al. 2011. Domain structure of Lassa virus L protein. J. Virol. 85:324-333.
6. Buchholz, U. J., S. Finke, and K. K. Conzelmann. 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.
7. Casabona, J. C., J. M. Levingston Macleod, M. E. Loureiro, G. A. Gomez, and N. Lopez. 2009. The RING domain and the L79 residue of Z protein are involved in both the rescue of nucleocapsids and the incorporation of glycoproteins into infectious chimeric arenavirus-like particles. J. Virol. 83: 7029-7039.
8. Charrel, R. N., X. de Lamballerie, and C. F. Fulhorst. 2001. The Whitewater Arroyo virus: natural evidence for genetic recombination among Tacaribe serocomplex viruses (family Arenaviridae). Virology 283:161-166.
9. Charrel, R. N., X. de Lamballerie, and S. Emonet. 2008. Phylogeny of the genus Arenavirus. Curr. Opin. Microbiol. 11:362-368.
10. Cole, C., J. D. Barber, and G. J. Barton. 2008. The Jpred 3 secondary structure prediction server. Nucleic Acids Res. 36:W197-W201.
11. Ferron, F., et al. 2011. The hexamer structure of the Rift Valley fever virus nucleoprotein suggests a mechanism for its assembly into ribonucleoprotein complexes. PLoS Pathog. 7:e1002030.
12. Flatz, L., A. Bergthaler, J. C. de la Torre, and D. D. Pinschewer. 2006. Recovery of an arenavirus entirely from RNA polymerase I/II-driven cDNA. Proc. Natl. Acad. Sci. U. S. A. 103:4663-4668.
13. Garcin, D., and D. Kolakofsky. 1992. Tacaribe arenavirus RNA synthesis in vitro is primer dependent and suggests an unusual model for the initiation of genome replication. J. Virol. 66:1370-1376.
14. Günther, S., and O. Lenz. 2004. Lassa virus. Crit. Rev. Clin. Lab. Sci. 41:339-390.
15. Hass, M., U. Gölnitz, S. Müller, B. Becker-Ziaja, and S. Günther. 2004. Replicon system for Lassa virus. J. Virol. 78:13793-13803.
16. Hass, M., et al. 2006. Mutational analysis of the Lassa virus promoter. J. Virol. 80:12414-12419.
17. Hass, M., M. Lelke, C. Busch, B. Becker-Ziaja, and S. Günther. 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.
18. Hastie, K. M., C. R. Kimberlin, M. A. Zandonatti, I. J. MacRae, and E. O. Saphire. 2011. Structure of the Lassa virus nucleoprotein reveals a dsRNAspecific 3′ to 5′ exonuclease activity essential for immune suppression. Proc. Natl. Acad. Sci. U. S. A. 108:2396-2401.
19. Jacamo, R., N. Lopez, M. Wilda, and M. T. Franze-Fernandez. 2003. Tacaribe virus Z protein interacts with the L polymerase protein to inhibit viral RNA synthesis. J. Virol. 77:10383-10393.
20. Kranzusch, P. J., et al. 2010. Assembly of a functional Machupo virus polymerase complex. Proc. Natl. Acad. Sci. U. S. A. 107:20069-20074.
21. Lee, K. J., I. S. Novella, M. N. Teng, M. B. Oldstone, and J. C. de La Torre. 2000. NP and L proteins of lymphocytic choriomeningitis virus (LCMV) are sufficient for efficient transcription and replication of LCMV genomic RNA analogs. J. Virol. 74:3470-3477.
22. Lelke, M., L. Brunotte, C. Busch, and S. Günther. 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.
23. Levingston Macleod, J. M., et al. 2011. Identification of two functional domains within the arenavirus nucleoprotein. J. Virol. 85:2012-2023.
24. Lopez, N., R. Jacamo, and M. T. Franze-Fernandez. 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.
25. Lukashevich, I. S. 1992. Generation of reassortants between African arenaviruses. Virology 188:600-605.
26. Lukashevich, I. S., 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. 78:547-551.
27. Martinez-Sobrido, L., E. I. Zuniga, D. Rosario, A. Garcia-Sastre, and J. C. de la Torre. 2006. Inhibition of the type I interferon response by the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 80:9192-9199.
28. Martinez-Sobrido, L., et al. 2009. Identification of amino acid residues critical for the anti-interferon activity of the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 83:11330-11340.
29. Morin, B., et al. 2010. The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog. 6:e1001038.
30. Perez, M., R. C. Craven, and J. C. de la Torre. 2003. The small RING finger protein Z drives arenavirus budding: implications for antiviral strategies. Proc. Natl. Acad. Sci. U. S. A. 100:12978-12983.
31. Pinschewer, D. D., M. Perez, and J. C. de la Torre. 2005. Dual role of the lymphocytic choriomeningitis virus intergenic region in transcription termination and virus propagation. J. Virol. 79:4519-4526.
32. Qi, X., et al. 2010. Cap binding and immune evasion revealed by Lassa nucleoprotein structure. Nature 468:779-783.
33. Raymond, D. D., M. E. Piper, S. R. Gerrard, and J. L. Smith. 2010. Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation. Proc. Natl. Acad. Sci. U. S. A. 107:11769-11774.
34. Sanchez, A. B., and J. C. de la Torre. 2005. Genetic and biochemical evidence for an oligomeric structure of the functional L polymerase of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 79:7262-7268.
35. Shtanko, O., et al. 2010. A role for the C terminus of Mopeia virus nucleoprotein in its incorporation into Z protein-induced virus-like particles. J. Virol. 84:5415-5422.
36. Shtanko, O., S. Watanabe, L. D. Jasenosky, T. Watanabe, and Y. Kawaoka. 2011. ALIX/AIP1 is required for NP incorporation into Mopeia virus Z-induced virus-like particles. J. Virol. 85:3631-3641.
37. Strecker, T., et al. 2003. Lassa virus Z protein is a matrix protein sufficient for the release of virus-like particles. J. Virol. 77:10700-10705.
38. Sutter, G., M. Ohlmann, and V. Erfle. 1995. Non-replicating vaccinia vector efficiently expresses bacteriophage T7 RNA polymerase. FEBS Lett. 371:9-12.
39. Walker, D. H., et al. 1982. Experimental infection of rhesus monkeys with Lassa virus and a closely related arenavirus, Mozambique virus. J. Infect. Dis. 146:360-368.
40. Wilda, M., N. Lopez, J. C. Casabona, and M. T. Franze-Fernandez. 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.
41. Wilson, S. M., and J. C. Clegg. 1991. Sequence analysis of the S RNA of the African arenavirus Mopeia: an unusual secondary structure feature in the intergenic region. Virology 180:543-552.
42. Wunderlich, K., et al. 2009. Identification of a PA-binding peptide with inhibitory activity against influenza A and B virus replication. PLoS One 4:e7517.
43. Yanase, T., et al. 2006. Genetic characterization of Batai virus indicates a genomic reassortment between orthobunyaviruses in nature. Arch. Virol. 151:2253-2260.