Comparative Structural and Functional Analysis of Bunyavirus and Arenavirus Cap-Snatching Endonucleases

PLoS Pathogens

Volumn 12, Issue 6, 2016, Pages

  Reguera, Juan ^a,c   Gerlach, Piotr ^a,d   Rosenthal, Maria ^b   Gaudon, Stephanie ^a   Coscia, Francesca ^a,e   Günther, Stephan ^b   Cusack, Stephen ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

^b BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^c Centre National de la Recherche Scientifique   (France)

^d MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^e UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAP SNATCHING ENDONUCLEASE; ENDONUCLEASE; MANGANESE; MESSENGER RNA; UNCLASSIFIED DRUG; VIRUS ENZYME; CAPPED RNA; VIRAL PROTEIN;

AMINO TERMINAL SEQUENCE; ARENAVIRUS; ARTICLE; BUNYAVIRIDAE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME STABILITY; ENZYME STRUCTURE, FUNCTION AND VARIABILITY; ESCHERICHIA COLI; HANTAAN VIRUS; INFLUENZA VIRUS; ISOTHERMAL TITRATION CALORIMETRY; LA CROSSE VIRUS; NONHUMAN; PROTEIN EXPRESSION; REPLICON; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY; CALORIMETRY; CHEMISTRY; ENZYMOLOGY; HANTAVIRUS; LASSA VIRUS; METABOLISM; ORTHOBUNYAVIRUS; PROTEIN CONFORMATION; STRUCTURE ACTIVITY RELATION;

ARENAVIRUS; CALORIMETRY; CRYSTALLOGRAPHY, X-RAY; ENDONUCLEASES; HANTAVIRUS; LASSA VIRUS; ORTHOBUNYAVIRUS; PROTEIN CONFORMATION; RNA CAPS; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL PROTEINS;

EID: 84978864743     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005636     Document Type: Article

References (40)

1. Rosenberg R, (2015) Detecting the emergence of novel, zoonotic viruses pathogenic to humans. Cell Mol Life Sci72: 1115–1125. doi: 10.1007/s00018-014-1785-y25416679
2. Compans RW, Bishop DH, (1983) Segmented Negative Strand Virus. Orlando, Florida 32887: Academic Press, INC. 412 p.
3. Clegg JC, (2009) Influence of climate change on the incidence and impact of arenavirus diseases: a speculative assessment. Clin Microbiol Infect15: 504–509. doi: 10.1111/j.1469-0691.2009.02847.x19604274
4. Elliott RM, (2009) Bunyaviruses and climate change. Clin Microbiol Infect15: 510–517. doi: 10.1111/j.1469-0691.2009.02849.x19604275
5. 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. Cell23: 847–858. 6261960
6. Garcin D, Lezzi M, Dobbs M, Elliott RM, Schmaljohn C, et al. (1995) The 5' ends of Hantaan virus (Bunyaviridae) RNAs suggest a prime-and-realign mechanism for the initiation of RNA synthesis. J Virol69: 5754–5762. 7637020
7. Jin H, Elliott RM, (1993) Non-viral sequences at the 5' ends of Dugbe nairovirus S mRNAs. J Gen Virol74 (Pt 10): 2293–2297. 8409954
8. Duijsings D, Kormelink R, Goldbach R, (2001) In vivo analysis of the TSWV cap-snatching mechanism: single base complementarity and primer length requirements. EMBO J20: 2545–2552. 11350944
9. Reich S, Guilligay D, Pflug A, Malet H, Berger I, et al. (2014) Structural insight into cap-snatching and RNA synthesis by influenza polymerase. Nature516: 361–366. doi: 10.1038/nature1400925409151
10. 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. Nature458: 914–918. doi: 10.1038/nature0774519194459
11. 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 Biol15: 500–506. doi: 10.1038/nsmb.142118454157
12. Pflug A, Guilligay D, Reich S, Cusack S, (2014) Structure of influenza A polymerase bound to the viral RNA promoter. Nature516: 355–360. doi: 10.1038/nature1400825409142
13. Morin B, Coutard B, Lelke M, Ferron F, Kerber R, et al. (2010) The N-terminal domain of the arenavirus L protein is an RNA endonuclease essential in mRNA transcription. PLoS Pathog6: e1001038. doi: 10.1371/journal.ppat.100103820862324
14. 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 Pathog6: e1001101. doi: 10.1371/journal.ppat.100110120862319
15. Klemm C, Reguera J, Cusack S, Zielecki F, Kochs G, et al. (2013) Systems to establish bunyavirus genome replication in the absence of transcription. J Virol87: 8205–8212. doi: 10.1128/JVI.00371-1323698297
16. Wallat GD, Huang Q, Wang W, Dong H, Ly H, et al. (2014) High-resolution structure of the N-terminal endonuclease domain of the Lassa virus L polymerase in complex with magnesium ions. PLoS One9: e87577. doi: 10.1371/journal.pone.008757724516554
17. 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 Virol84: 1934–1944. doi: 10.1128/JVI.01657-0920007273
18. Devignot S, Bergeron E, Nichol S, Mirazimi A, Weber F, (2015) A virus-like particle system identifies the endonuclease domain of crimean-congo hemorrhagic Fever virus. J Virol89: 5957–5967. doi: 10.1128/JVI.03691-1425810550
19. Lecompte E, Fichet-Calvet E, Daffis S, Koulemou K, Sylla O, et al. (2006) Mastomys natalensis and Lassa fever, West Africa. Emerg Infect Dis12: 1971–1974. 17326956
20. Zeier M, Handermann M, Bahr U, Rensch B, Muller S, et al. (2005) New ecological aspects of hantavirus infection: a change of a paradigm and a challenge of prevention—a review. Virus Genes30: 157–180. 15744574
21. Hasegawa H, Holm L, (2009) Advances and pitfalls of protein structural alignment. Curr Opin Struct Biol19: 341–348. doi: 10.1016/j.sbi.2009.04.00319481444
22. Fernández-García Y, Reguera J, Busch C, Witte G, Sánchez-Ramos O, et al. (2016) Atomic Structure and Biochemical Characterization of an RNA Endonuclease in the N terminus of Andes Virus L Protein. co-submission to Plos Path.
23. Krissinel E, Henrick K, (2004) Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr60: 2256–2268. 15572779
24. Crepin T, Dias A, Palencia A, Swale C, Cusack S, et al. (2010) Mutational and metal binding analysis of the endonuclease domain of the influenza virus polymerase PA subunit. J Virol84: 9096–9104. doi: 10.1128/JVI.00995-1020592097
25. 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 Chemother38: 2827–2837. 7695269
26. Kowalinski E, Zubieta C, Wolkerstorfer A, Szolar OH, Ruigrok RW, et al. (2012) Structural analysis of specific metal chelating inhibitor binding to the endonuclease domain of influenza pH1N1 (2009) polymerase. PLoS Pathog8: e1002831. doi: 10.1371/journal.ppat.100283122876177
27. Gerlach P, Malet H, Cusack S, Reguera J, (2015) Structural Insights into Bunyavirus Replication and Its Regulation by the vRNA Promoter. Cell161: 1267–1279. doi: 10.1016/j.cell.2015.05.00626004069
28. Hengrung N, El Omari K, Serna Martin I, Vreede FT, Cusack S, et al. (2015) Crystal structure of the RNA-dependent RNA polymerase from influenza C virus. Nature527: 114–117. doi: 10.1038/nature1552526503046
29. Ortin J, Martin-Benito J, (2015) The RNA synthesis machinery of negative-stranded RNA viruses. Virology479–480: 532–544. doi: 10.1016/j.virol.2015.03.01825824479
30. Thierry E, Guilligay D, Kosinski J, Bock T, Gaudon S, et al. (2015) Influenza Polymerase Can Adopt an Alternative Configuration Involving a Radical Repacking of PB2 Domains. Mol Cell.
31. Ericsson UB, Hallberg BM, Detitta GT, Dekker N, Nordlund P, (2006) Thermofluor-based high-throughput stability optimization of proteins for structural studies. Anal Biochem357: 289–298. 16962548
32. Dimasi N, Flot D, Dupeux F, Marquez JA, (2007) Expression, crystallization and X-ray data collection from microcrystals of the extracellular domain of the human inhibitory receptor expressed on myeloid cells IREM-1. Acta Crystallogr Sect F Struct Biol Cryst Commun63: 204–208. 17329815
33. Ness SR, de Graaff RA, Abrahams JP, Pannu NS, (2004) CRANK: new methods for automated macromolecular crystal structure solution. Structure12: 1753–1761. 15458625
34. Kabsch W, (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Cryst26: 795–800.
35. Perrakis A, Morris R, Lamzin VS, (1999) Automated protein model building combined with iterative structure refinement. Nat Struct Biol6: 458–463. 10331874
36. Murshudov GN, Vagin AA, Dodson EJ, (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr53: 240–255. 15299926
37. Hass M, Golnitz U, Muller S, Becker-Ziaja B, Gunther S, (2004) Replicon system for Lassa virus. J Virol78: 13793–13803. 15564487
38. 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 Virol82: 10207–10217. doi: 10.1128/JVI.00220-0818667512
39. 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 Virol73: 251–259. 9847328
40. Sutter G, Ohlmann M, Erfle V, (1995) Non-replicating vaccinia vector efficiently expresses bacteriophage T7 RNA polymerase. FEBS Lett371: 9–12. 7664891