Systems to establish bunyavirus genome replication in the absence of transcription

Journal of Virology

Volumn 87, Issue 14, 2013, Pages 8205-8212

  Klemm, Carolin ^a   Reguera, Juan ^b   Cusack, Stephen ^b   Zielecki, Florian ^a   Kochs, G Georg ^c   Webera, Friedemann ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOCAPSID PROTEIN N; PROTEIN KINASE R; UNCLASSIFIED DRUG; VIRAL POLYMERASE L; VIRUS PROTEIN;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CONTROLLED STUDY; GENOME ANALYSIS; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RIFT VALLEY FEVER BUNYAVIRUS; TRANSCRIPTION INITIATION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS MUTATION; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

AMINO ACID MOTIFS; DNA PRIMERS; DNA-DIRECTED RNA POLYMERASES; GENOME, VIRAL; LA CROSSE VIRUS; LUCIFERASES; MUTATION, MISSENSE; PLASMIDS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE GENETICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBONUCLEASES; RIFT VALLEY FEVER VIRUS; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

EID: 84880255207     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00371-13     Document Type: Article

References (49)

1. Elliott RM, Weber F. 2009. Bunyaviruses and the type I interferon system. Viruses 1:1003-1021.
2. Walter CT, Barr JN. 2011. Recent advances in the molecular and cellular biology of bunyaviruses. J. Gen. Virol. 92:2467-2484.
3. Flick K, Katz A, Overby A, Feldmann H, Pettersson RF, Flick R. 2004. Functional analysis of the noncoding regions of the Uukuniemi virus (Bunyaviridae) RNA segments. J. Virol. 78:11726-11738.
4. Kohl A, Lowen AC, Leonard VH, Elliott RM. 2006. Genetic elements regulating packaging of the Bunyamwera orthobunyavirus genome. J. Gen. Virol. 87:177-187.
5. Terasaki K, Murakami S, Lokugamage KG, Makino S. 2011. Mechanism of tripartite RNA genome packaging in Rift Valley fever virus. Proc. Natl. Acad. Sci. U. S. A. 108:804-809.
6. Albarino CG, Bird BH, Nichol ST. 2007. A shared transcription termination signal on negative and ambisense RNA genome segments of RiftValley fever, sandfly fever Sicilian, and Toscana viruses. J. Virol. 81:5246-5256.
7. Ikegami T, Won S, Peters CJ, Makino S. 2007. Characterization of Rift Valley fever virus transcriptional terminations. J. Virol. 81:8421-8438.
8. Hoenen T, Groseth A, de Kok-Mercado F, Kuhn JH, Wahl-Jensen V. 2011. Minigenomes, transcription and replication competent virus-like particles and beyond: reverse genetics systems for filoviruses and other negative stranded hemorrhagic fever viruses. Antiviral Res. 91:195-208.
9. Habjan M, Penski N, Wagner V, Spiegel M, Overby AK, Kochs G, Huiskonen JT, Weber F. 2009. Efficient production of Rift Valley fever virus-like particles: the antiviral protein MxA can inhibit primary transcription of bunyaviruses. Virology 385:400-408.
10. Overby AK, Popov V, Neve EP, Pettersson RF. 2006. Generation and analysis of infectious virus-like particles of Uukuniemi virus (Bunyaviridae): a useful system for studying bunyaviral packaging and budding. J. Virol. 80:10428-10435.
11. Shi X, Kohl A, Leonard VH, Li P, McLees A, Elliott RM. 2006. Requirement of the N-terminal region of orthobunyavirus nonstructural protein NSm for virus assembly and morphogenesis. J. Virol. 80:8089-8099.
12. Soldan SS, Hollidge BS, Wagner V, Weber F, Gonzalez-Scarano F. 2010. La Crosse virus (LACV) Gc fusion peptide mutants have impaired growth and fusion phenotypes, but remain neurotoxic. Virology 404:139-147.
13. Overby AK, Popov VL, Pettersson RF, Neve EP. 2007. The cytoplasmic tails of Uukuniemi virus (Bunyaviridae) GN and GC glycoproteins are important for intracellular targeting and the budding of virus-like particles. J. Virol. 81:11381-11391.
14. Shi X, Kohl A, Li P, Elliott RM. 2007. Role of the cytoplasmic tail domains of Bunyamwera orthobunyavirus glycoproteins Gn and Gc in virus assembly and morphogenesis. J. Virol. 81:10151-10160.
15. Overby AK, Pettersson RF, Neve EP. 2007. The glycoprotein cytoplasmic tail of Uukuniemi virus (Bunyaviridae) interacts with ribonucleoproteins and is critical for genome packaging. J. Virol. 81:3198-3205.
16. Weber M, Gawanbacht A, Habjan M, Rang A, Borner C, Schmidt AM, Veitinger S, Jacob R, Devignot S, Kochs G, Garcia-Sastre A, Weber F. 2013. Incoming RNA virus nucleocapsids containing a 5=-triphosphorylated genome activate RIG-I and antiviral signaling. Cell Host Microbe 13:336-346.
17. 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.
18. Li S, Koromilas AE. 2001. Dominant negative function by an alternatively spliced form of the interferon-inducible protein kinase PKR. J. Biol. Chem. 276:13881-13890.
19. Blakqori G, Kochs G, Haller O, Weber F. 2003. Functional L polymerase of La Crosse virus allows in vivo reconstitution of recombinant nucleocapsids. J. Gen. Virol. 84:1207-1214.
20. Weber F, Dunn EF, Bridgen A, Elliott RM. 2001. The Bunyamwera virus nonstructural protein NSs inhibits viral RNA synthesis in a minireplicon system. Virology 281:67-74.
21. Reguera J, Weber F, Cusack S. 2010. Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription. PLoS Pathog. 6:e1001101. doi:10.1371/journal.ppat.1001101.
22. Habjan M, Penski N, Spiegel M, Weber F. 2008. T7 RNA polymerasedependent and -independent systems for cDNA-based rescue of Rift Valley fever virus. J. Gen. Virol. 89:2157-2166.
23. Robb NC, Smith M, Vreede FT, Fodor E. 2009. NS2/NEP protein regulates transcription and replication of the influenza virus RNA genome. J. Gen. Virol. 90:1398-1407.
24. +CT method. Methods 25: 402-408.
25. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
26. Beitz E. 2000. TEXshade: shading and labeling of multiple sequence alignments using LATEX2 epsilon. Bioinformatics 16:135-139.
27. Subramaniam S. 1998. The Biology Workbench-a seamless database and analysis environment for the biologist. Proteins 32:1-2.
28. Krissinel E, Henrick K. 2004. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D Biol. Crystallogr. 60:2256-2268.
29. Carlton-Smith C, Elliott RM. 2012. Viperin, MTAP44, and protein kinase R contribute to the interferon-induced inhibition of Bunyamwera orthobunyavirus replication. J. Virol. 86:11548-11557.
30. Habjan M, Pichlmair A, Elliott RM, Overby AK, Glatter T, Gstaiger M, Superti-Furga G, Unger H, Weber F. 2009. NSs protein of Rift Valley fever virus induces the specific degradation of the double-stranded RNAdependent protein kinase. J. Virol. 83:4365-4375.
31. Ikegami T, Narayanan K, Won S, Kamitani W, Peters CJ, Makino S. 2009. Rift Valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2alpha phosphorylation. PLoS Pathog. 5:e1000287. doi:10.1371/journal.ppat.1000287.
32. Streitenfeld H, Boyd A, Fazakerley JK, Bridgen A, Elliott RM, Weber F. 2003. Activation of PKR by Bunyamwera virus is independent of the viral interferon antagonist NSs. J. Virol. 77:5507-5511.
33. Garcia MA, Gil J, Ventoso I, Guerra S, Domingo E, Rivas C, Esteban M. 2006. Impact of protein kinase PKR in cell biology: from antiviral to antiproliferative action. Microbiol. Mol. Biol. Rev. 70:1032-1060.
34. Morin B, Coutard B, Lelke M, Ferron F, Kerber R, Jamal S, Frangeul A, Baronti C, Charrel R, de Lamballerie X, Vonrhein C, Lescar J, Bricogne G, Gunther S, Canard B. 2010. The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog. 6:e1001038. doi:10.1371/journal.ppat.1001038.
35. Boshra H, Lorenzo G, Busquets N, Brun A. 2011. Rift Valley fever: recent insights into pathogenesis and prevention. J. Virol. 85:6098-6105.
36. Dias A, Bouvier D, Crepin T, McCarthy AA, Hart DJ, Baudin F, Cusack S, Ruigrok RW. 2009. The cap-snatching endonuclease of influenza virus polymerase resides in the PA subunit. Nature 458:914-918.
37. Yuan P, Bartlam M, Lou Z, Chen S, Zhou J, He X, Lv Z, Ge R, Li X, Deng T, Fodor E, Rao Z, Liu Y. 2009. Crystal structure of an avian influenza polymerase PA(N) reveals an endonuclease active site. Nature 458:909-913.
38. Barr JN, Rodgers JW, Wertz GW. 2005. The Bunyamwera virus mRNA transcription signal resides within both the 3' and the 5' terminal regions and allows ambisense transcription from a model RNA segment. J. Virol. 79:12602-12607.
39. Barr JN, Wertz GW. 2005. Role of the conserved nucleotide mismatch within 3'-and 5'-terminal regions of Bunyamwera virus in signaling transcription. J. Virol. 79:3586-3594.
40. Eifan SA, Elliott RM. 2009. Mutational analysis of the Bunyamwera orthobunyavirus nucleocapsid protein gene. J. Virol. 83:11307-11317.
41. Walter CT, Bento DF, Alonso AG, Barr JN. 2011. Amino acid changes within the Bunyamwera virus nucleocapsid protein differentially affect the mRNA transcription and RNA replication activities of assembled ribonucleoprotein templates. J. Gen. Virol. 92:80-84.
42. Garcia MA, Meurs EF, Esteban M. 2007. The dsRNA protein kinase PKR: virus and cell control. Biochimie 89:799-811.
43. Nallagatla SR, Hwang J, Toroney R, Zheng X, Cameron CE, Bevilacqua PC. 2007. 5'-triphosphate-dependent activation of PKR by RNAs with short stem-loops. Science 318:1455-1458.
44. Jorba N, Coloma R, Ortin J. 2009. Genetic trans-complementation establishes a new model for influenza virus RNA transcription and replication. PLoS Pathog. 5:e1000462. doi:10.1371/journal.ppat.1000462.
45. Randall RE, Goodbourn S. 2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1-47.
46. Baum A, Garcia-Sastre A. 2011. Differential recognition of viral RNA by RIG-I. Virulence 2:166-169.
47. Bowzard JB, Davis WG, Jeisy-Scott V, Ranjan P, Gangappa S, Fujita T, Sambhara S. 2011. PAMPer and tRIGer: ligand-induced activation of RIG-I. Trends Biochem. Sci. 36:314-319.
48. Jensen S, Thomsen AR. 2012. Sensing of RNA viruses: a review of innate immune receptors involved in recognizing RNA virus invasion. J. Virol. 86:2900-2910.
49. Kato H, Takahasi K, Fujita T. 2011. RIG-I-like receptors: cytoplasmic sensors for non-self RNA. Immunol. Rev. 243:91-98.