Bunyaviridae RNA polymerases (L-protein) have an N-terminal, influenza-like endonuclease domain, essential for viral cap-dependent transcription

PLoS Pathogens

Volumn 6, Issue 9, 2010, Pages

  Reguera, Juan ^a   Weber, Friedemann ^b,c   Cusack, Stephen ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^b UNIVERSITY OF FREIBURG   (Germany)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2,4 DIOXO 4 PHENYLBUTANOIC ACID; 4 PHENYLBUTYRIC ACID; DIHYDROLIPOAMIDE DEHYDROGENASE; ENDONUCLEASE; MANGANESE; RNA POLYMERASE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARENAVIRUS; ARTICLE; CHELATION; CRYSTAL STRUCTURE; INFLUENZA VIRUS; LA CROSSE VIRUS; METAL BINDING; ORTHOBUNYAVIRUS; POINT MUTATION; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; TENUIVIRUS; VIRUS TRANSCRIPTION; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; AMINOBUTYRIC ACIDS; BUNYAVIRIDAE; BUNYAVIRIDAE INFECTIONS; CATALYTIC DOMAIN; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; DNA-DIRECTED RNA POLYMERASES; ENDONUCLEASES; HUMANS; INFLUENZA, HUMAN; MOLECULAR SEQUENCE DATA; ORTHOMYXOVIRIDAE; PROTEIN STRUCTURE, TERTIARY; RNA CAPS; RNA, MESSENGER; RNA, VIRAL; SEQUENCE HOMOLOGY, AMINO ACID; TRANSCRIPTION, GENETIC; VIRAL PROTEINS;

ANIMALIA; BUNYAVIRIDAE; ORTHOBUNYAVIRUS; ORTHOMYXOVIRIDAE; RNA VIRUSES;

EID: 78149353044     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001101     Document Type: Article

References (51)

1. 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.
2. Bishop DH, Gay ME, Matsuoko Y (1983) Nonviral heterogeneous sequences are present at the 59 ends of one species of snowshoe hare bunyavirus S complementary RNA. Nucleic Acids Res 11: 6409-6418.
3. Patterson JL, Holloway B, Kolakofsky D (1984) La Crosse virions contain a primer-stimulated RNA polymerase and a methylated cap-dependent endonu-clease. J Virol 52: 215-222.
4. Garcin D, Lezzi M, Dobbs M, Elliott RM, Schmaljohn C, et al. (1995) The 59 ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis. J Virol 69: 5754-5762.
5. Jin H, Elliott RM (1993) Non-viral sequences at the 59 ends of Dugbe nairovirus S mRNAs. J Gen Virol 74 (Pt 10): 2293-2297.
6. Duijsings D, Kormelink R, Goldbach R (2001) In vivo analysis of the TSWV cap-snatching mechanism: single base complementarity and primer length requirements. Embo J 20: 2545-2552.
7. Raju R, Raju L, Hacker D, Garcin D, Compans R, et al. (1990) Nontemplated bases at the 59 ends of Tacaribe virus mRNAs. Virology 174: 53-59.
8. 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.
9. Vieth S, Torda AE, Asper M, Schmitz H, Gunther S (2004) Sequence analysis of L RNA of Lassa virus. Virology 318: 153-168.
10. Kinsella E, Martin SG, Grolla A, Czub M, Feldmann H, et al. (2004) Sequence determination of the Crimean-Congo hemorrhagic fever virus L segment. Virology 321: 23-28.
11. Ruigrok RW, Crepin T, Hart DJ, Cusack S (2010) Towards an atomic resolution understanding of the influenza virus replication machinery. Curr Opin Struct Biol 20: 104-113.
12. 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.
13. 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.
14. 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.
15. Knizewski L, Kinch LN, Grishin NV, Rychlewski L, Ginalski K (2007) Realm of PD-(D/E)XK nuclease superfamily revisited: detection of novel families with modified transitive meta profile searches. BMC Struct Biol 7: 40.
16. Kukkonen SK, Vaheri A, Plyusnin A (2005) L protein, the RNA-dependent RNA polymerase of hantaviruses. Arch Virol 150: 533-556.
17. Tomassini J, Selnick H, Davies ME, Armstrong ME, Baldwin J, et al. (1994) Inhibition of cap (m7GpppXm)-dependent endonuclease of influenza virus by 4-substituted 2,4-dioxobutanoic acid compounds. Antimicrob Agents Chemother 38: 2827-2837.
18. 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.
19. Ericsson UB, Hallberg BM, Detitta GT, Dekker N, Nordlund P (2006) Thermofluor-based high-throughput stability optimization of proteins for structural studies. Anal Biochem 357: 289-298.
20. Crepin T, Dias A, Cusack S, Ruigrok RW, Palencia A, et al. (2010) Mutational and metal binding analysis of the endonuclease domain of the influenza virus polymerase PA subunit. J Virol 84: 9096-9104.
21. 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.
22. Ventoso I, Barco A, Carrasco L (1998) Mutational analysis of poliovirus 2Apro. Distinct inhibitory functions of 2apro on translation and transcription. J Biol Chem 273: 27960-27967.
23. Falk BW, Tsai JH (1998) Biology and molecular biology of viruses in the genus Tenuivirus. Annu Rev Phytopathol 36: 139-163.
24. Honig JE, Osborne JC, Nichol ST (2004) Crimean-Congo hemorrhagic fever virus genome L RNA segment and encoded protein. Virology 321: 29-35.
25. Makarova KS, Aravind L, Koonin EV (2000) A novel superfamily of predicted cysteine proteases from eukaryotes, viruses and Chlamydia pneumoniae. Trends Biochem Sci 25: 50-52.
26. Zhang HM, Yang J, Sun HR, Xin X, Wang HD, et al. (2007) Genomic analysis of rice stripe virus Zhejiang isolate shows the presence of an OTU-like domain in the RNA1 protein and a novel sequence motif conserved within the intergenic regions of ambisense segments of tenuiviruses. Arch Virol 152: 1917-1923.
27. 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.
28. Lelke M, Brunotte L, Busch C, Gunther S. 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.
29. Mielke N, Muehlbach HP (2007) A novel, multipartite, negative-strand RNA virus is associated with the ringspot disease of European mountain ash (Sorbus aucuparia L.). J Gen Virol 88: 1337-1346.
30. Elbeaino T, Digiaro M, Martelli GP (2009) Complete nucleotide sequence of four RNA segments of fig mosaic virus. Arch Virol 154: 1719-1727.
31. Snow M, Ritchie R, Arnaud O, Villoing S, Aspehaug V, et al. (2003) Isolation and characterisation of segment 1 of the infectious salmon anaemia virus genome. Virus Res 92: 99-105.
32. Presti RM, Zhao G, Beatty WL, Mihindukulasuriya KA, da Rosa AP, et al. (2009) Quaranfil, Johnston Atoll, and Lake Chad viruses are novel members of the family Orthomyxoviridae. J Virol 83: 11599-11606.
33. Mir MA, Duran WA, Hjelle BL, Ye C, Panganiban AT (2008) Storage of cellular 59 mRNA caps in P bodies for viral cap-snatching. Proc Natl Acad Sci U S A 105: 19294-19299.
34. Tomassini JE, Davies ME, Hastings JC, Lingham R, Mojena M, et al. (1996) A novel antiviral agent which inhibits the endonuclease of influenza viruses. Antimicrob Agents Chemother 40: 1189-1193.
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. Nakazawa M, Kadowaki SE, Watanabe I, Kadowaki Y, Takei M, et al. (2008) PA subunit of RNA polymerase as a promising target for anti-influenza virus agents. Antiviral Res 78: 194-201.
37. Kuzuhara T, Iwai Y, Takahashi H, Hatakeyama D, Echigo N (2009) Green tea catechins inhibit the endonuclease activity of influenza A virus RNA polymerase. PLoS Curr Influenza: RRN1052.
38. Grobler JA, Stillmock K, Hu B, Witmer M, Felock P, et al. (2002) Diketo acid inhibitor mechanism and HIV-1 integrase: implications for metal binding in the active site of phosphotransferase enzymes. Proc Natl Acad Sci U S A 99: 6661-6666.
39. Serrao E, Odde S, Ramkumar K, Neamati N (2009) Raltegravir, elvitegravir, and metoogravir: the birth of "me-too" HIV-1 integrase inhibitors. Retrovirol-ogy 6: 25.
40. Hare S, Gupta SS, Valkov E, Engelman A, Cherepanov P. Retroviral intasome assembly and inhibition of DNA strand transfer. Nature 464: 232-236.
41. Kabsch W (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst 26: 795-800.
42. Vonrhein C, Blanc E, Roversi P, Bricogne G (2006) Automated Structure Solution With autoSHARP. Methods Mol Biol 364: 215-230.
43. Perrakis A, Morris R, Lamzin VS (1999) Automated protein model building combined with iterative structure refinement. Nat Struct Biol 6: 458-463.
44. Murshudov GN (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
45. Read RJ (2001) Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallogr D Biol Crystallogr 57: 1373-1382.
46. Kraulis PJ (1991) MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J Appl Cryst 24: 946-950.
47. Esnouf RM (1999) Further additions to Molscript version 1.4, including reading and contouring of electron density maps. Acta Crystallogr 55: 938-940.
48. Merritt EA, Bacon DJ (1997) Raster3D Photorealistic molecular graphics. Methods Enzymol 277: 505-524.
49. 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.
50. Gouet P, Courcelle E, Stuart DI, Metoz F (1999) ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15: 305-308.
51. Toriyama S, Kimishima T, Takahashi M, Shimizu T, Minaka N, et al. (1998) The complete nucleotide sequence of the rice grassy stunt virus genome and genomic comparisons with viruses of the genus Tenuivirus. J Gen Virol 79 (Pt 8): 2051-2058.