Low-resolution structure of vaccinia virus DNA replication machinery

Journal of Virology

Volumn 87, Issue 3, 2013, Pages 1679-1689

  Sèle, Céleste ^a   Gabel, Frank ^b   Gutsche, Irina ^a   Ivanov, Ivan ^a   Burmeister, Wim P ^a   Iseni, Frédéric ^c   Tarbouriech, Nicolas ^a  

^a UNIV GRENOBLE ALPES   (France)

^b INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^c INSTITUT DE RECHERCHE BIOMÉDICALE DES ARMÉES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

A20D4 POLYMERASE COFACTOR; DNA POLYMERASE; DNA POLYMERASE E9; HELICASE; HELICASE PRIMASE D5; HOLOENZYME; HOLOENZYME A20D4E9; PROTEIN A20; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; URACIL DNA GLYCOSIDASE; URACIL DNA GLYCOSYLASE D4; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; DNA BINDING; DNA REPLICATION; ELECTRON MICROSCOPY; ENZYME ACTIVE SITE; ENZYME BINDING; GENE REPLICATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; VACCINIA VIRUS; VIRUS GENOME; X RAY CRYSTALLOGRAPHY;

DNA REPLICATION; MACROMOLECULAR SUBSTANCES; MICROSCOPY, ELECTRON; PROTEIN INTERACTION MAPPING; SCATTERING, SMALL ANGLE; VACCINIA VIRUS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84873029046     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01533-12     Document Type: Article

References (91)

1. Lewis-Jones S. 2004. Zoonotic poxvirus infections in humans. Curr. Opin. Infect. Dis. 17:81-89.
2. Ninove L, Domart Y, Vervel C, Voinot C, Salez N, Raoult D, Meyer H, Capek I, Zandotti C, Charrel RN. 2009. Cowpox virus transmission from pet rats to humans, France. Emerg. Infect. Dis. 15:781-784.
3. WHO. 1980. The global eradication of smallpox: final report of the Global Commission for the Certification of Smallpox Eradication. World Health Organization, Geneva, Switzerland.
4. Massung RF, Liu LI, Qi J, Knight JC, Yuran TE, Kerlavage AR, Parsons JM, Venter JC, Esposito JJ. 1994. Analysis of the complete genome of smallpox variola major virus strain Bangladesh 1975. Virology 201:215-240.
5. Berche P. 2001. The threat of smallpox and bioterrorism. Trends Microbiol. 9:15-18.
6. Pennington H. 2003. Smallpox and bioterrorism. Bull. World Health Organ. 81:762-767.
7. Bray M. 2003. Pathogenesis and potential antiviral therapy of complications of smallpox vaccination. Antiviral Res. 58:101-114.
8. Lederman E, Miramontes R, Openshaw J, Olson VA, Karem KL, Marcinak J, Panares R, Staggs W, Allen D, Weber SG, Vora S, Gerber SI, Hughes CM, Regnery R, Collins L, Diaz PS, Reynolds MG, Damon I. 2009. Eczema vaccinatum resulting from the transmission of vaccinia virus from a smallpox vaccinee: an investigation of potential fomites in the home environment. Vaccine 27:375-377.
9. Baker RO, Bray M, Huggins JW. 2003. Potential antiviral therapeutics for smallpox, monkeypox and other orthopoxvirus infections. Antiviral Res. 57:13-23.
10. De Clercq E. 2002. Cidofovir in the treatment of poxvirus infections. Antiviral Res. 55:1-13.
11. Quenelle DC, Kern ER. 2010. Treatment of vaccinia and cowpox virus infections in mice with CMX001 and ST-246. Viruses 2:2681-2695.
12. Yang G, Pevear DC, Davies MH, Collett MS, Bailey T, Rippen S, Barone L, Burns C, Rhodes G, Tohan S, Huggins JW, Baker RO, Buller RL, Touchette E, Waller K, Schriewer J, Neyts J, DeClercq E, Jones K, Hruby D, Jordan R. 2005. An orally bioavailable antipoxvirus compound (ST-246) inhibits extracellular virus formation and protects mice from lethal orthopoxvirus challenge. J. Virol. 79:13139-13149.
13. Pennington T, Folett E. 1974. Vaccinia virus replication in enucleated BSC-1 cells: particle production and synthesis of viral DNA and proteins. J. Virol. 13:488-493.
14. Prescott DM, Kates J, Kirkpatrick JB. 1971. Replication of vaccinia virus DNA in enucleated L-cells. J. Mol. Biol. 59:505-508.
15. Moss B, De Silva FS. 2006. DNA replication & human disease; poxvirus DNA replication and human disease. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
16. Baroudy BM, Venkatesan S, Moss B. 1982. Incompletely base-paired flip-flop terminal loops link the two DNA strands of the vaccinia virus genome into one uninterrupted polynucleotide chain. Cell 28:315-324.
17. Baroudy BM, Venkatesan S, Moss B. 1983. Structure and replication of vaccinia virus telomeres. Cold Spring Harb. Symp. Quant. Biol. 47:723-729.
18. Moyer RW, Graves RL. 1981. The mechanism of cytoplasmic orthopoxvirus DNA replication. Cell 27:391-401.
19. DeLange AM. 1989. Identification of temperature-sensitive mutants of vaccinia that are defective in conversion of concatemeric replicative intermediates to the mature linear DNA genome. J. Virol. 63:2437-2444.
20. Merchlinsky M. 1990. Mutational analysis of the resolution sequence of vaccinia virus DNA: essential sequence consists of two separate AT-rich regions highly conserved among poxviruses. J. Virol. 64:5029-5035.
21. Esteban M, Flores L, Holowczak JA. 1977. Model for vaccinia virus DNA replication. Virology 83:467-473.
22. Pogo BG, O'Shea M, Freimuth P. 1981. Initiation and termination of vaccinia virus DNA replication. Virology 108:241-248.
23. Garcia AD, Aravind L, Koonin EV, Moss B. 2000. Bacterial-type DNA Holliday junction resolvases in eukaryotic viruses. Proc. Natl. Acad. Sci. U. S. A. 97:8926-8931.
24. Garcia AD, Moss B. 2001. Repression of vaccinia virus Holliday junction resolvase inhibits processing of viral DNA into unit-length genomes. J. Virol. 75:6460-6471.
25. Esteban M, Holowczak JA. 1977. Replication of vaccinia DNA in mouse L cells. I. In vivo DNA synthesis. Virology 78:57-75.
26. De Silva FS, Lewis W, Berglund P, Koonin EV, Moss B. 2007. Poxvirus DNA primase. Proc. Natl. Acad. Sci. U. S. A. 104:18724-18729.
27. Frick DN, Richardson CC. 2001. DNA primases. Annu. Rev. Biochem. 70:39-80.
28. Du S, Traktman P. 1996. Vaccinia virus DNA replication: two hundred base pairs of telomeric sequence confer optimal replication efficiency on minichromosome templates. Proc. Natl. Acad. Sci. U. S. A. 93:9693-9698.
29. De Silva FS, Moss B. 2005. Origin-independent plasmid replication occurs in vaccinia virus cytoplasmic factories and requires all five known poxvirus replication factors. Virol. J. 2:23. doi:10.1186/1743-422X-2-23.
30. DeLange AM, McFadden G. 1986. Sequence-nonspecific replication of transfected plasmid DNA in poxvirus-infected cells. Proc. Natl. Acad. Sci. U. S. A. 83:614-618.
31. Kato SE, Moussatche N, D'Costa SM, Bainbridge TW, Prins C, Strahl AL, Shatzer AN, Brinker AJ, Kay NE, Condit RC. 2008. Marker rescue mapping of the combined Condit/Dales collection of temperaturesensitive vaccinia virus mutants. Virology 375:213-222.
32. McCraith S, Holtzman T, Moss B, Fields S. 2000. Genome-wide analysis of vaccinia virus protein-protein interactions. Proc. Natl. Acad. Sci. U. S. A. 97:4879-4884.
33. Zhang L, Villa NY, Rahman MM, Smallwood S, Shattuck D, Neff C, Dufford M, Lanchbury JS, Labaer J, McFadden G. 2009. Analysis of vaccinia virus-host protein-protein interactions: validations of yeast twohybrid screenings. J. Proteome Res. 8:4311-4318.
34. Traktman P, Anderson MK, Rempel RE. 1989. Vaccinia virus encodes an essential gene with strong homology to protein kinases. J. Biol. Chem. 264:21458-21461.
35. Stuart DT, Upton C, Higman MA, Niles EG, McFadden G. 1993. A poxvirus-encoded uracil DNA glycosylase is essential for virus viability. J. Virol. 67:2503-2512.
36. McDonald WF, Klemperer N, Traktman P. 1997. Characterization of a processive form of the vaccinia virusDNApolymerase. Virology 234:168-175.
37. McDonald WF, Traktman P. 1994. Vaccinia virus DNA polymerase. In vitro analysis of parameters affecting processivity. J. Biol. Chem. 269: 31190-31197.
38. Hamilton MD, Evans DH. 2005. Enzymatic processing of replication and recombination intermediates by the vaccinia virus DNA polymerase. Nucleic Acids Res. 33:2259-2268.
39. Willer DO, Mann MJ, Zhang W, Evans DH. 1999. Vaccinia virus DNA polymerase promotes DNA pairing and strand-transfer reactions. Virology 257:511-523.
40. Willer DO, Yao XD, Mann MJ, Evans DH. 2000. In vitro concatemer formation catalyzed by vaccinia virus DNA polymerase. Virology 278: 562-569.
41. Ishii K, Moss B. 2002. Mapping interaction sites of the A20R protein component of the vaccinia virus DNA replication complex. Virology 303: 232-239.
42. Klemperer N, McDonald W, Boyle K, Unger B, Traktman P. 2001. The A20R protein is a stoichiometric component of the processive form of vaccinia virus DNA polymerase. J. Virol. 75:12298-12307.
43. Stanitsa ES, Arps L, Traktman P. 2006. Vaccinia virus uracil DNA glycosylase interacts with the A20 protein to form a heterodimeric processivity factor for the viral DNA polymerase. J. Biol. Chem. 281:3439-3451.
44. Schormann N, Grigorian A, Samal A, Krishnan R, DeLucas L, Chattopadhyay D. 2007. Crystal structure of vaccinia virus uracil-DNA glycosylase reveals dimeric assembly. BMC Struct. Biol. 7:45. doi:10.1186/1741 -6807-7-45.
45. Holzer GW, Falkner FG. 1997. Construction of a vaccinia virus deficient in the essential DNA repair enzyme uracil DNA glycosylase by a complementing cell line. J. Virol. 71:4997-5002.
46. Millns AK, Carpenter MS, DeLange AM. 1994. The vaccinia virusencoded uracil DNA glycosylase has an essential role in viral DNA replication. Virology 198:504-513.
47. De Silva FS, Moss B. 2008. Effects of vaccinia virus uracil DNA glycosylase catalytic site and deoxyuridine triphosphatase deletion mutations individually and together on replication in active and quiescent cells and pathogenesis in mice. Virol. J. 5:145. doi:10.1186/1743-422X-5-145.
48. Boyle KA, Stanitsa ES, Greseth MD, Lindgren JK, Traktman P. 2011. Evaluation of the role of the vaccinia virus uracilDNAglycosylase and A20 proteins as intrinsic components of the DNA polymerase holoenzyme. J. Biol. Chem. 286:24702-24713.
49. Evans E, Klemperer N, Ghosh R, Traktman P. 1995. The vaccinia virus D5 protein, which is required for DNA replication, is a nucleic acidindependent nucleoside triphosphatase. J. Virol. 69:5353-5361.
50. Iyer LM, Koonin EV, Leipe DD, Aravind L. 2005. Origin and evolution of the archaeo-eukaryotic primase superfamily and related palm-domain proteins: structural insights and new members. Nucleic Acids Res. 33: 3875-3896.
51. Gorbalenya AE, Koonin EV. 1989. Viral proteins containing the purine NTP-binding sequence pattern. Nucleic Acids Res. 17:8413-8440.
52. Iyer LM, Aravind L, Koonin EV. 2001. Common origin of four diverse families of large eukaryotic DNA viruses. J. Virol. 75:11720-11734.
53. Boyle KA, Arps L, Traktman P. 2007. Biochemical and genetic analysis of the vaccinia virus D5 protein: multimerization-dependent ATPase activity is required to support viral DNA replication. J. Virol. 81:844-859.
54. De Silva FS, Paran N, Moss B. 2009. Products and substrate/template usage of vaccinia virus DNA primase. Virology 383:136-141.
55. Delelis O, Carayon K, Guiot E, Leh H, Tauc P, Brochon JC, Mouscadet JF, Deprez E. 2008. Insight into the integrase-DNA recognition mechanism. A specific DNA-binding mode revealed by an enzymatically labeled integrase. J. Biol. Chem. 283:27838-27849.
56. Berger I, Fitzgerald DJ, Richmond TJ. 2004. Baculovirus expression system for heterologous multiprotein complexes. Nat. Biotechnol. 22: 1583-1587.
57. Trowitzsch S, Bieniossek C, Nie Y, Garzoni F, Berger I. 2010. New baculovirus expression tools for recombinant protein complex production. J. Struct. Biol. 172:45-54.
58. Ludtke SJ, Baldwin PR, Chiu W. 1999. EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol. 128:82-97.
59. Mindell JA, Grigorieff N. 2003. Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol. 142:334-347.
60. Heymann JB, Cardone G, Winkler DC, Steven AC. 2008. Computational resources for cryo-electron tomography in Bsoft. J. Struct. Biol. 161:232-242.
61. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M. 1996. A new generation of the IMAGIC image processing system. J. Struct. Biol. 116: 17-24.
62. Pernot P, Theveneau P, Giraud T, Nogueira Fernandes R, Nurizzo D, Spruce D, Surr J, McSweeney S, Round A, Felisaz F, Foedinger L, Gobbo A, Huet J, Villard C, Cipriani F. 2010. New beamline dedicated to solution scattering from biological macromolecules at the ESRF. J. Phys. Conf. Ser., vol 247. doi:10.1088/1742-6596/247/1/012009.
63. Konarev PV, Volkov A, Sokolova AV, Koch MHJ, Svergun DI. 2003. PRIMUS: a Windows-PC based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36:1277-1282.
64. Konarev PV, Petoukhov MV, Volkov VV, Svergun DI. 2006. ATSAS 2.1, a program package for small-angle scattering data analysis. J. Appl. Crystallogr. 39:277-286.
65. Svergun DI. 1992. Determination of the regularization parameter in indirect- transform methods using perceptual criteria. J. Appl. Crystallogr. 25:495-503.
66. Franke D, Svergun DI. 2009. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42: 342-346.
67. Volkov VV, Svergun DI. 2003. Uniqueness of ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr. 36:860-864.
68. Wriggers W. 2010. Using Situs for the integration of multi-resolution structures. Biophys. Rev. 2:21-27.
69. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
70. Lassmann T, Sonnhammer EL. 2005. Kalign: an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 6:298. doi:10 .1186/1741-2105-6-298.
71. Gille C, Frommel C. 2001. STRAP: editor for STRuctural Alignments of Proteins. Bioinformatics 17:377-378.
72. Deleage G, Blanchet C, Geourjon C. 1997. Protein structure prediction. Implications for the biologist. Biochimie 79:681-686.
73. Svergun DI, Barberato C, Koch MHJ. 1995. CRYSOL: a program to evalate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28:768-773.
74. Kozin M, Svergun DI. 2000. Automated matching of high- and lowresolution structural models. J. Appl. Crystallogr. 34:33-41.
75. Garcia De La Torre J, Huertas ML, Carrasco B. 2000. Calculation of hydrodynamic properties of globular proteins from their atomic-level structure. Biophys. J. 78:719-730.
76. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671-675.
77. Gorbalenya AE, Koonin EV, Wolf YI. 1990. A new superfamily of putative NTP-binding domains encoded by genomes of small DNA and RNA viruses. FEBS Lett. 262:145-148.
78. Singleton MR, Dillingham MS, Wigley DB. 2007. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 76:23-50.
79. James JA, Escalante CR, Yoon-Robarts M, Edwards TA, Linden RM, Aggarwal AK. 2003. Crystal structure of the SF3 helicase from adenoassociated virus type 2. Structure 11:1025-1035.
80. Enemark EJ, Joshua-Tor L. 2006. Mechanism of DNA translocation in a replicative hexameric helicase. Nature 442:270-275.
81. Ziegelin G, Scherzinger E, Lurz R, Lanka E. 1993. Phage P4 alpha protein is multifunctional with origin recognition, helicase and primase activities. EMBO J. 12:3703-3708.
82. Digard P, Bebrin WR, Weisshart K, Coen DM. 1993. The extreme C terminus of herpes simplex virusDNApolymerase is crucial for functional interaction with processivity factor UL42 and for viral replication. J. Virol. 67:398-406.
83. Zuccola HJ, Filman DJ, Coen DM, Hogle JM. 2000. The crystal structure of an unusual processivity factor, herpes simplex virus UL42, bound to the C terminus of its cognate polymerase. Mol. Cell 5:267-278.
84. Parikh SS, Mol CD, Slupphaug G, Bharati S, Krokan HE, Tainer JA. 1998. Base excision repair initiation revealed by crystal structures and binding kinetics of human uracil-DNA glycosylase with DNA. EMBO J. 17:5214-5226.
85. Franklin MC, Wang J, Steitz TA. 2001. Structure of the replicating complex of a pol alpha family DNA polymerase. Cell 105:657-667.
86. Firbank SJ, Wardle J, Heslop P, Lewis RJ, Connolly BA. 2008. Uracil recognition in archaeal DNA polymerases captured by X-ray crystallography. J. Mol. Biol. 381:529-539.
87. Swan MK, Johnson RE, Prakash L, Prakash S, Aggarwal AK. 2009. Structural basis of high-fidelity DNA synthesis by yeast DNA polymerase delta. Nat. Struct. Mol. Biol. 16:979-986.
88. Mueser TC, Hinerman JM, Devos JM, Boyer RA, Williams KJ. 2010. Structural analysis of bacteriophage T4 DNA replication: a review in the Virology Journal series on bacteriophage T4 and its relatives. Virol. J. 7:359. doi:10.1186/1743-422X-7-359.
89. Scaramozzino N, Sanz G, Crance JM, Saparbaev M, Drillien R, Laval J, Kavli B, Garin D. 2003. Characterisation of the substrate specificity of homogeneous vaccinia virus uracil-DNA glycosylase. Nucleic Acids Res. 31:4950-4957.
90. Gai D, Zhao R, Li D, Finkielstein CV, Chen XS. 2004. Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 119:47-60.
91. Lipps G, Weinzierl AO, von Scheven G, Buchen C, Cramer P. 2004. Structure of a bifunctional DNA primase-polymerase. Nat. Struct. Mol. Biol. 11:157-162.