Discovery of an essential nucleotidylating activity associated with a newly delineated conserved domain in the RNA polymerase-containing protein of all nidoviruses

Nucleic Acids Research

Volumn 43, Issue 17, 2015, Pages 8416-8434

  Lehmann, Kathleen C ^a   Gulyaeva, Anastasia ^a   Zevenhoven Dobbe, Jessika C ^a   Janssen, George M C ^a   Ruben, Mark ^b   Overkleeft, Hermen S ^b   Van Veelen, Peter A ^a   Samborskiy, Dmitry V ^c   Kravchenko, Alexander A ^c   Leontovich, Andrey M ^c   Sidorov, Igor A ^a   Snijder, Eric J ^a   Posthuma, Clara C ^a   Gorbalenya, Alexander E ^a,c  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE; GUANOSINE; GUANOSINE TRIPHOSPHATE; HISTIDINE; LYSINE; MANGANESE; MESSENGER RNA; NIDOVIRUS RDRP ASSOCIATED NUCLEOTIDYLTRANSFERASE; NIDOVIRUS RNA DEPENDENT RNA POLYMERASE ASSOCIATED NUCLEOTIDYLTRANSFERASE; NUCLEOTIDYLTRANSFERASE; PROTEIN VARIANT; RECOMBINANT NONSTRUCTURAL PROTEIN 9; RECOMBINANT PROTEIN; RNA DIRECTED RNA POLYMERASE; UNCLASSIFIED DRUG; URIDINE PHOSPHATE; VIRUS ENZYME; NUCLEOTIDE; PHOSPHATE; POLYPROTEIN; URIDINE; URIDINE TRIPHOSPHATE; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ARTERIVIRUS EQUINE ARTERITIS VIRUS; ARTICLE; CELL CULTURE; CONTROLLED STUDY; COVALENT BOND; GENETIC CONSERVATION; NIDOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN RNA BINDING; PROTEOMICS; RNA CAPPING; RNA SYNTHESIS; RNA VIRUS; SARS CORONAVIRUS; VIRUS MUTATION; VIRUS REPLICATION; BINDING SITE; CHEMISTRY; ENZYMOLOGY; EQUINE ARTERITIS VIRUS; GENETICS; METABOLISM; NIDOVIRALES; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

ARTERITIS VIRUS, EQUINE; BINDING SITES; CONSERVED SEQUENCE; GUANOSINE; GUANOSINE TRIPHOSPHATE; MANGANESE; NIDOVIRALES; NUCLEOTIDES; NUCLEOTIDYLTRANSFERASES; PHOSPHATES; POLYPROTEINS; PROTEIN STRUCTURE, TERTIARY; RNA REPLICASE; SARS VIRUS; URIDINE; URIDINE TRIPHOSPHATE; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84945261819     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv838     Document Type: Article

References (112)

1. de Groot, R.J., Cowley, J.A., Enjuanes, L., Faaberg, K.S., Perlman, S., Rottier, P.J., Snijder, E.J., Ziebuhr, J. and Gorbalenya, A.E. (2012) Order Nidovirales. In: King, AMQ, Adams, MJ, Carstens, EB and Lefkowitz, EJ (eds). Virus Taxonomy. Ninth Report of the International Committee on Taxonomy of Viruses. Elsevier Academic Press, Amsterdam, pp. 785-795.
2. Lauber, C., Ziebuhr, J., Junglen, S., Drosten, C., Zirkel, F., Nga, P.T., Morita, K., Snijder, E.J. and Gorbalenya, A.E. (2012) Mesoniviridae: a proposed new family in the order Nidovirales formed by a single species of mosquito-borne viruses. Arch. Virol., 157, 1623-1628.
3. Neumann, E.J., Kliebenstein, J.B., Johnson, C.D., Mabry, J.W., Bush, E.J., Seitzinger, A.H., Green, A.L. and Zimmerman, J.J. (2005) Assessment of the economic impact of porcine reproductive and respiratory syndrome on swine production in the United States. J. Am. Vet. Med. Assoc., 227, 385-392.
4. Coleman, C.M. and Frieman, M.B. (2014) Coronaviruses: important emerging human pathogens. J. Virol., 88, 5209-5212.
5. Hilgenfeld, R. and Peiris, M. (2013) From SARS to MERS: 10 years of research on highly pathogenic human coronaviruses. Antiviral Res., 100, 286-295.
6. Zaki, A.M., van Boheemen, S., Bestebroer, T.M., Osterhaus, A.D.M.E. and Fouchier, R.A.M. (2012) Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N Engl J Med., 367, 1814-1820.
7. Lauber, C., Goeman, J.J., Parquet, M.C., Nga, P.T., Snijder, E.J., Morita, K. and Gorbalenya, A.E. (2013) The footprint of genome architecture in the largest genome expansion in RNA viruses. PLoS Pathog., 9, e1003500.
8. Snijder, E.J., Siddell, S.G. and Gorbalenya, A.E. (2005) The order Nidovirales. In: Mahy, BW and ter Meulen, V (eds). Topley and Wilson's Microbiology and Microbial Infections: Virology Volume. Hodder Arnold, London, pp. 390-404.
9. Pasternak, A.O., Spaan, W.J. and Snijder, E.J. (2006) Nidovirus transcription: how to make sense. . . ? J. Gen. Virol., 87, 1403-1421.
10. Sawicki, S. G., Sawicki, D. L. and Siddell, S. G. (2007) A contemporary view of coronavirus transcription. J. Virol., 81, 20-29.
11. Brian, D. A. and Baric, R. S. (2005) Coronavirus genome structure and replication. Curr. Top. Microbiol. Immunol., 287, 1-30.
12. Masters, P.S. (2006) The molecular biology of coronaviruses. Adv. Virus Res., 66, 193-292.
13. Gorbalenya, A.E., Enjuanes, L., Ziebuhr, J. and Snijder, E.J. (2006) Nidovirales: evolving the largest RNA virus genome. Virus Res., 117, 17-37.
14. Ziebuhr, J., Snijder, E.J. and Gorbalenya, A.E. (2000) Virus-encoded proteinases and proteolytic processing in the Nidovirales. J. Gen. Virol., 81, 853-879.
15. Weiss, S.R. and Leibowitz, J.L. (2011) Coronavirus pathogenesis. Adv Virus Res., 81, 85-164.
16. Perlman, S. and Netland, J. (2009) Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol., 7, 439-450.
17. Subissi, L., Imbert, I., Ferron, F., Collet, A., Coutard, B., Decroly, E. and Canard, B. (2014) SARS-CoV ORF1b-encoded nonstructural proteins 12-16: replicative enzymes as antiviral targets. Antiviral Res., 101, 122-130.
18. Neuman, B.W., Angelini, M.M. and Buchmeier, M.J. (2014) Does form meet function in the coronavirus replicative organelle? Trends Microbiol., 22, 642-647.
19. Denison, M.R., Graham, R.L., Donaldson, E.F., Eckerle, L.D. and Baric, R.S. (2011) Coronaviruses: an RNA proofreading machine regulates replication fidelity and diversity. RNA Biol., 8, 270-279.
20. Lehmann, K.C., Snijder, E.J., Posthuma, C.C. and Gorbalenya, A.E. (2014) What we know but do not understand about nidovirus helicases. Virus Res., 202, 12-32.
21. Bouvet, M., Imbert, I., Subissi, L., Gluais, L., Canard, B. and Decroly, E. (2012) RNA 3'-end mismatch excision by the severe acute respiratory syndrome coronavirus nonstructural protein nsp10/nsp14 exoribonuclease complex. Proc. Natl. Acad. Sci. U.S.A., 109, 9372-9377.
22. Minskaia, E., Hertzig, T., Gorbalenya, A.E., Campanacci, V., Cambillau, C., Canard, B. and Ziebuhr, J. (2006) Discovery of an RNA virus 3'->5' exoribonuclease that is critically involved in coronavirus RNA synthesis. Proc. Natl. Acad. Sci. U.S.A., 103, 5108-5113.
23. Bouvet, M., Debarnot, C., Imbert, I., Selisko, B., Snijder, E.J., Canard, B. and Decroly, E. (2010) In vitro reconstitution of SARS-coronavirus mRNA cap methylation. PLoS Pathog., 6, e1000863.
24. Chen, Y., Cai, H., Pan, J., Xiang, N., Tien, P., Ahola, T. and Guo, D. (2009) Functional screen reveals SARS coronavirus nonstructural protein nsp14 as a novel cap N7 methyltransferase. Proc. Natl. Acad. Sci. U.S.A., 106, 3484-3489.
25. Ivanov, K.A., Hertzig, T., Rozanov, M., Bayer, S., Thiel, V., Gorbalenya, A.E. and Ziebuhr, J. (2004) Major genetic marker of nidoviruses encodes a replicative endoribonuclease. Proc. Natl. Acad. Sci. U.S.A., 101, 12694-12699.
26. Nedialkova, D.D., Ulferts, R., van den Born, E., Lauber, C., Gorbalenya, A.E., Ziebuhr, J. and Snijder, E.J. (2009) Biochemical characterization of arterivirus nonstructural protein 11 reveals the nidovirus-wide conservation of a replicative endoribonuclease. J. Virol., 83, 5671-5682.
27. Chen, Y., Su, C., Ke, M., Jin, X., Xu, L., Zhang, Z., Wu, A., Sun, Y., Yang, Z., Tien, P. et al. (2011) Biochemical and structural insights into the mechanisms of SARS coronavirus RNA ribose 2'-O-methylation by nsp16/nsp10 protein complex. PLoS Pathog., 7, e1002294.
28. Daffis, S., Szretter, K.J., Schriewer, J., Li, J., Youn, S., Errett, J., Lin, T.Y., Schneller, S., Zust, R., Dong, H. et al. (2010) 2'-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature, 468, 452-456.
29. Decroly, E., Imbert, I., Coutard, B., Bouvet, M., Selisko, B., Alvarez, K., Gorbalenya, A.E., Snijder, E.J. and Canard, B. (2008) Coronavirus nonstructural protein 16 is a cap-0 binding enzyme possessing (nucleoside-2'O)-methyltransferase activity. J. Virol., 82, 8071-8084.
30. Nga, P.T., Parquet, M.C., Lauber, C., Parida, M., Nabeshima, T., Yu, F., Thuy, N.T., Inoue, S., Ito, T., Okamoto, K. et al. (2011) Discovery of the first insect nidovirus, a missing evolutionary link in the emergence of the largest RNA virus genomes. PLoS Pathog., 7, e1002215.
31. Gorbalenya, A.E. (2001) Big nidovirus genome. When count and order of domains matter. Adv. Exp. Med. Biol., 494, 1-17.
32. Lehmann, K.C., Hooghiemstra, L., Gulyaeva, A., Samborskiy, D., Zevenhoven-Dobbe, J., Snijder, E., Gorbalenya, A.E. and Posthuma, C.C. (2015) Arterivirus nsp12 versus the coronavirus nsp16 2'-O-methyltransferase: comparison of the C-terminal cleavage products of two nidovirus pp1ab polyproteins. J. Gen. Virol., doi:10.1099/vir.0.000209.
33. Lang, D.M., Zemla, A.T. and Zhou, C.L. (2013) Highly similar structural frames link the template tunnel and NTP entry tunnel to the exterior surface in RNA-dependent RNA polymerases. Nucleic Acids Res., 41, 1464-1482.
34. Ng, K.K., Arnold, J.J. and Cameron, C.E. (2008) Structure-function relationships among RNA-dependent RNA polymerases. Curr. Top. Microbiol. Immunol., 320, 137-156.
35. Gorbalenya, A.E., Pringle, F.M., Zeddam, J.L., Luke, B.T., Cameron, C.E., Kalmakoff, J., Hanzlik, T.N., Gordon, K.H. and Ward, V.K. (2002) The palm subdomain-based active site is internally permuted in viral RNA-dependent RNA polymerases of an ancient lineage. J. Mol. Biol., 324, 47-62.
36. Gorbalenya, A.E., Koonin, E.V., Donchenko, A.P. and Blinov, V.M. (1989) Coronavirus genome: prediction of putative functional domains in the non-structural polyprotein by comparative amino acid sequence analysis. Nucleic Acids Res., 17, 4847-4861.
37. Azzi, A. and Lin, S.X. (2004) Human SARS-coronavirus RNA-dependent RNA polymerase: activity determinants and nucleoside analogue inhibitors. Proteins, 57, 12-14.
38. Xu, X., Liu, Y., Weiss, S., Arnold, E., Sarafianos, S.G. and Ding, J. (2003) Molecular model of SARS coronavirus polymerase: implications for biochemical functions and drug design. Nucleic Acids Res., 31, 7117-7130.
39. Snijder, E.J., Bredenbeek, P.J., Dobbe, J.C., Thiel, V., Ziebuhr, J., Poon, L.L., Guan, Y., Rozanov, M., Spaan, W.J. and Gorbalenya, A.E. (2003) Unique and conserved features of genome and proteome of SARS-coronavirus, an early split-off from the coronavirus group 2 lineage. J. Mol. Biol., 331, 991-1004.
40. Ahn, D.G., Choi, J.K., Taylor, D.R. and Oh, J.W. (2012) Biochemical characterization of a recombinant SARS coronavirus nsp12 RNA-dependent RNA polymerase capable of copying viral RNA templates. Arch. Virol., 157, 2095-2104.
41. Bautista, E.M., Faaberg, K.S., Mickelson, D. and McGruder, E.D. (2002) Functional properties of the predicted helicase of porcine reproductive and respiratory syndrome virus. Virology, 298, 258-270.
42. Beerens, N., Selisko, B., Ricagno, S., Imbert, I., van der Zanden, L., Snijder, E.J. and Canard, B. (2007) De novo initiation of RNA synthesis by the arterivirus RNA-dependent RNA polymerase. J. Virol., 81, 8384-8395.
43. Ivanov, K.A., Thiel, V., Dobbe, J.C., van der Meer, Y., Snijder, E.J. and Ziebuhr, J. (2004) Multiple enzymatic activities associated with severe acute respiratory syndrome coronavirus helicase. J. Virol., 78, 5619-5632.
44. Ivanov, K.A. and Ziebuhr, J. (2004) Human coronavirus 229E nonstructural protein 13: characterization of duplex-unwinding, nucleoside triphosphatase, and RNA 5'-triphosphatase activities. J. Virol., 78, 7833-7838.
45. Seybert, A., van Dinten, L.C., Snijder, E.J. and Ziebuhr, J. (2000) Biochemical characterization of the equine arteritis virus helicase suggests a close functional relationship between arterivirus and coronavirus helicases. J. Virol., 74, 9586-9593.
46. Seybert, A., Posthuma, C.C., van Dinten, L.C., Snijder, E.J., Gorbalenya, A.E. and Ziebuhr, J. (2005) A complex zinc finger controls the enzymatic activities of nidovirus helicases. J. Virol., 79, 696-704.
47. te Velthuis, A.J., van den Worm, S.H., Sims, A.C., Baric, R.S., Snijder, E.J. and van Hemert, M.J. (2010) Zn(2+) inhibits coronavirus and arterivirus RNA polymerase activity in vitro and zinc ionophores block the replication of these viruses in cell culture. PLoS Pathog., 6, e1001176.
48. van Dinten, L.C., van Tol, H., Gorbalenya, A.E. and Snijder, E.J. (2000) The predicted metal-binding region of the arterivirus helicase protein is involved in subgenomic mRNA synthesis, genome replication, and virion biogenesis. J. Virol., 74, 5213-5223.
49. Eckerle, L.D., Lu, X., Sperry, S.M., Choi, L. and Denison, M.R. (2007) High fidelity of murine hepatitis virus replication is decreased in nsp14 exoribonuclease mutants. J. Virol., 81, 12135-12144.
50. Posthuma, C.C., Nedialkova, D.D., Zevenhoven-Dobbe, J.C., Blokhuis, J.H., Gorbalenya, A.E. and Snijder, E.J. (2006) Site-directed mutagenesis of the Nidovirus replicative endoribonuclease NendoU exerts pleiotropic effects on the arterivirus life cycle. J. Virol., 80, 1653-1661.
51. Zust, R., Cervantes-Barragan, L., Habjan, M., Maier, R., Neuman, B.W., Ziebuhr, J., Szretter, K.J., Baker, S.C., Barchet, W., Diamond, M.S. et al. (2011) Ribose 2'-O-methylation provides a molecular signature for the distinction of self and non-self mRNA dependent on the RNA sensor Mda5. Nat. Immunol., 12, 137-143.
52. Benson, D.A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J. and Sayers, E.W. (2013) GenBank. Nucleic Acids Res., 41, D36-D42.
53. Pruitt, K.D., Brown, G.R., Hiatt, S.M., Thibaud-Nissen, F., Astashyn, A., Ermolaeva, O., Farrell, C.M., Hart, J., Landrum, M.J., McGarvey, K.M. et al. (2014) RefSeq: an update on mammalian reference sequences. Nucleic Acids Res., 42, D756-D763.
54. Lauber, C. and Gorbalenya, A.E. (2012) Partitioning the genetic diversity of a virus family: approach and evaluation through a case study of picornaviruses. J. Virol., 86, 3890-3904.
55. Sidorov, I.A., Reshetov, D.A. and Gorbalenya, A.E. (2009) SNAD: sequence name annotation-based designer. BMC Bioinformatics., 10, 251.
56. Gorbalenya, A.E., Lieutaud, P., Harris, M.R., Coutard, B., Canard, B., Kleywegt, G.J., Kravchenko, A.A., Samborskiy, D.V., Sidorov, I.A., Leontovich, A.M. et al. (2010) Practical application of bioinformatics by the multidisciplinary VIZIER consortium. Antiviral Res., 87, 95-110.
57. Finn, R.D., Clements, J. and Eddy, S.R. (2011) HMMER web server: interactive sequence similarity searching. Nucleic Acids Res., 39, W29-W37.
58. Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32, 1792-1797.
59. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics., 23, 2947-2948.
60. Ziebuhr, J., Bayer, S., Cowley, J.A. and Gorbalenya, A.E. (2003) The 3C-like proteinase of an invertebrate nidovirus links coronavirus and potyvirus homologs. J. Virol., 77, 1415-1426.
61. Blanck, S., Stinn, A., Tsiklauri, L., Zirkel, F., Junglen, S. and Ziebuhr, J. (2014) Characterization of an alphamesonivirus 3C-like protease defines a special group of nidovirus main proteases. J. Virol., 88, 13747-13758.
62. Soding, J. (2005) Protein homology detection by HMM-HMM comparison. Bioinformatics., 21, 951-960.
63. Remmert, M., Biegert, A., Hauser, A. and Soding, J. (2012) HHblits: lightning-fast iterative protein sequence searching by HMM-HMM alignment. Nat. Methods, 9, 173-175.
64. Cole, C., Barber, J.D. and Barton, G.J. (2008) The Jpred 3 secondary structure prediction server. Nucleic Acids Res., 36, W197-W201.
65. Jones, D.T. (1999) Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol., 292, 195-202.
66. Robert, X. and Gouet, P. (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res., 42, W320-W324.
67. NCBI Resource Coordinators (2015) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res., 43, D6-D17.
68. Finn, R.D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R.Y., Eddy, S.R., Heger, A., Hetherington, K., Holm, L., Mistry, J. et al. (2014) Pfam: the protein families database. Nucleic Acids Res., 42, D222-D230.
69. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N. and Bourne, P.E. (2000) The Protein Data Bank. Nucleic Acids Res., 28, 235-242.
70. Jones, D.T. (1999) GenTHREADER: an efficient and reliable protein fold recognition method for genomic sequences. J. Mol. Biol., 287, 797-815.
71. McGuffin, L.J. and Jones, D.T. (2003) Improvement of the GenTHREADER method for genomic fold recognition. Bioinformatics., 19, 874-881.
72. Lobley, A., Sadowski, M.I. and Jones, D.T. (2009) pGenTHREADER and pDomTHREADER: new methods for improved protein fold recognition and superfamily discrimination. Bioinformatics., 25, 1761-1767.
73. Grant, B.J., Rodrigues, A.P., ElSawy, K.M., McCammon, J.A. and Caves, L.S. (2006) Bio3d: an R package for the comparative analysis of protein structures. Bioinformatics., 22, 2695-2696.
74. Henikoff, S. and Henikoff, J.G. (1992) Amino acid substitution matrices from protein blocks. Proc. Natl. Acad. Sci. U.S.A, 89, 10915-10919.
75. Guindon, S., Dufayard, J.F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol., 59, 307-321.
76. Paradis, E., Claude, J. and Strimmer, K. (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics., 20, 289-290.
77. R Development Core Team. (2011) R: a Language and Environment for Statistical Computing. R Foundation for statistical computing, Vienna
78. Hanoulle, X., Van, D.J., Staes, A., Martens, L., Goethals, M., Vandekerckhove, J. and Gevaert, K. (2006) A new functional, chemical proteomics technology to identify purine nucleotide binding sites in complex proteomes. J. Proteome. Res., 5, 3438-3445.
79. van den Born, E., Gultyaev, A.P. and Snijder, E.J. (2004) Secondary structure and function of the 5'-proximal region of the equine arteritis virus RNA genome. RNA, 10, 424-437.
80. Nedialkova, D.D., Gorbalenya, A.E. and Snijder, E.J. (2010) Arterivirus Nsp1 modulates the accumulation of minus-strand templates to control the relative abundance of viral mRNAs. PLoS Pathog., 6, e1000772.
81. van der Meer, Y., van, T.H., Locker, J.K. and Snijder, E.J. (1998) ORF1a-encoded replicase subunits are involved in the membrane association of the arterivirus replication complex. J. Virol., 72, 6689-6698.
82. Pfefferle, S., Krahling, V., Ditt, V., Grywna, K., Muhlberger, E. and Drosten, C. (2009) Reverse genetic characterization of the natural genomic deletion in SARS-Coronavirus strain Frankfurt-1 open reading frame 7b reveals an attenuating function of the 7b protein in-vitro and in-vivo. Virol. J., 6, 131.
83. Tischer, B.K., Smith, G.A. and Osterrieder, N. (2010) En passant mutagenesis: a two step markerless red recombination system. Methods Mol. Biol., 634, 421-430.
84. Subissi, L., Posthuma, C.C., Collet, A., Zevenhoven-Dobbe, J.C., Gorbalenya, A.E., Decroly, E., Snijder, E.J., Canard, B. and Imbert, I. (2014) One severe acute respiratory syndrome coronavirus protein complex integrates processive RNA polymerase and exonuclease activities. Proc. Natl. Acad. Sci. U.S.A., 111, e3900.
85. Bartlett, G.J., Porter, C.T., Borkakoti, N. and Thornton, J.M. (2002) Analysis of catalytic residues in enzyme active sites. J. Mol. Biol., 324, 105-121.
86. Henderson, B.R., Saeedi, B.J., Campagnola, G. and Geiss, B.J. (2011) Analysis of RNA binding by the dengue virus NS5 RNA capping enzyme. PLoS One, 6, e25795.
87. Shuman, S. and Schwer, B. (1995) RNA capping enzyme and DNA ligase: a superfamily of covalent nucleotidyl transferases. Mol. Microbiol., 17, 405-410.
88. Shuman, S. and Lima, C.D. (2004) The polynucleotide ligase and RNA capping enzyme superfamily of covalent nucleotidyltransferases. Curr. Opin. Struct. Biol., 14, 757-764.
89. Traut, T.W. (1994) Physiological concentrations of purines and pyrimidines. Mol. Cell Biochem., 140, 1-22.
90. Chakravarty, A.K., Subbotin, R., Chait, B.T. and Shuman, S. (2012) RNA ligase RtcB splices 3'-phosphate and 5'-OH ends via covalent RtcB-(histidinyl)-GMP and polynucleotide-(3')pp(5')G intermediates. Proc. Natl. Acad. Sci. U.S.A., 109, 6072-6077.
91. Duclos, B., Marcandier, S. and Cozzone, A.J. (1991) Chemical properties and separation of phosphoamino acids by thin-layer chromatography and/or electrophoresis. Methods Enzymol., 201, 10-21.
92. Kang, H., Bhardwaj, K., Li, Y., Palaninathan, S., Sacchettini, J., Guarino, L., Leibowitz, J.L. and Kao, C.C. (2007) Biochemical and genetic analyses of murine hepatitis virus Nsp15 endoribonuclease. J. Virol., 81, 13587-13597.
93. te Velthuis, A.J., Arnold, J.J., Cameron, C.E., van den Worm, S.H. and Snijder, E.J. (2010) The RNA polymerase activity of SARS-coronavirus nsp12 is primer dependent. Nucleic Acids Res., 38, 203-214.
94. Kumar, N.V. and Govil, G. (1984) Theoretical studies on protein-nucleic acid interactions. III. Stacking of aromatic amino acids with bases and base pairs of nucleic acids. Biopolymers, 23, 2009-2024.
95. Bartlett, G.J., Borkakoti, N. and Thornton, J.M. (2003) Catalysing new reactions during evolution: economy of residues and mechanism. J. Mol. Biol., 331, 829-860.
96. Schmelz, S. and Naismith, J.H. (2009) Adenylate-forming enzymes. Curr. Opin. Struct. Biol., 19, 666-671.
97. Ahola, T., Laakkonen, P., Vihinen, H. and Kaariainen, L. (1997) Critical residues of Semliki Forest virus RNA capping enzyme involved in methyltransferase and guanylyltransferase-like activities. J. Virol., 71, 392-397.
98. Nandakumar, J., Shuman, S. and Lima, C.D. (2006) RNA ligase structures reveal the basis for RNA specificity and conformational changes that drive ligation forward. Cell, 127, 71-84.
99. Decroly, E., Ferron, F., Lescar, J. and Canard, B. (2012) Conventional and unconventional mechanisms for capping viral mRNA. Nat. Rev. Microbiol., 10, 51-65.
100. Bouvet, M., Debarnot, C., Imbert, I., Selisko, B., Snijder, E.J., Canard, B. and Decroly, E. (2010) In vitro reconstitution of SARS-coronavirus mRNA cap methylation. PLoS Pathog., 6, e1000863.
101. Lai, M.M., Patton, C.D. and Stohlman, S.A. (1982) Further characterization of mRNA's of mouse hepatitis virus: presence of common 5'-end nucleotides. J. Virol., 41, 557-565.
102. van Vliet, A.L., Smits, S.L., Rottier, P.J. and de Groot, R.J. (2002) Discontinuous and non-discontinuous subgenomic RNA transcription in a nidovirus. EMBO J., 21, 6571-6580.
103. Sagripanti, J.L., Zandomeni, R.O. and Weinmann, R. (1986) The cap structure of simian hemorrhagic fever virion RNA. Virology, 151, 146-150.
104. Issur, M., Geiss, B.J., Bougie, I., Picard-Jean, F., Despins, S., Mayette, J., Hobdey, S.E. and Bisaillon, M. (2009) The flavivirus NS5 protein is a true RNA guanylyltransferase that catalyzes a two-step reaction to form the RNA cap structure. RNA, 15, 2340-2350.
105. Ahola, T. and Ahlquist, P. (1999) Putative RNA capping activities encoded by brome mosaic virus: methylation and covalent binding of guanylate by replicase protein 1a. J. Virol., 73, 10061-10069.
106. Paul, A.V., Rieder, E., Kim, D.W., van Boom, J.H. and Wimmer, E. (2000) Identification of an RNA hairpin in poliovirus RNA that serves as the primary template in the in vitro uridylylation of VPg. J. Virol., 74, 10359-10370.
107. Ambros, V. and Baltimore, D. (1978) Protein is linked to the 5' end of poliovirus RNA by a phosphodiester linkage to tyrosine. J. Biol. Chem., 253, 5263-5266.
108. Pan, J., Lin, L. and Tao, Y.J. (2009) Self-guanylylation of birnavirus VP1 does not require an intact polymerase activity site. Virology, 395, 87-96.
109. Mitra, T., Sosnovtsev, S.V. and Green, K.Y. (2004) Mutagenesis of tyrosine 24 in the VPg protein is lethal for feline calicivirus. J. Virol., 78, 4931-4935.
110. Jiang, J. and Laliberte, J.F. (2011) The genome-linked protein VPg of plant viruses-a protein with many partners. Curr. Opin. Virol., 1, 347-354.
111. Zeddam, J.L., Gordon, K.H., Lauber, C., Alves, C.A., Luke, B.T., Hanzlik, T.N., Ward, V.K. and Gorbalenya, A.E. (2010) Euprosterna elaeasa virus genome sequence and evolution of the Tetraviridae family: emergence of bipartite genomes and conservation of the VPg signal with the dsRNA Birnaviridae family. Virology, 397, 145-154.
112. Imbert, I., Guillemot, J.C., Bourhis, J.M., Bussetta, C., Coutard, B., Egloff, M.P., Ferron, F., Gorbalenya, A.E. and Canard, B. (2006) A second, non-canonical RNA-dependent RNA polymerase in SARS coronavirus. EMBO J., 25, 4933-4942.