Impact of 2-bromo-5,6-dichloro-1-β-D-ribofuranosyl benzimidazole riboside and inhibitors of DNA, RNA, and protein synthesis on human cytomegalovirus genome maturation

Journal of Virology

Volumn 79, Issue 17, 2005, Pages 11115-11127

  McVoy, Michael A ^a   Nixon, Daniel E ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 BROMO 5,6 DICHLORO 1 BETA DEXTRO RIBOFURANOSYLBENZIMIDAZOLE RIBOSIDE; BENZIMIDAZOLE DERIVATIVE; DNA POLYMERASE; MONOMER; RADIOISOTOPE; UNCLASSIFIED DRUG; VIRUS DNA;

ARTICLE; CONTROLLED STUDY; DNA CLEAVAGE; DNA DAMAGE; DNA PACKAGING; DNA RECOMBINATION; DNA REPAIR; DNA SYNTHESIS; GUINEA PIG; HERPES VIRUS; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; LONG TERMINAL REPEAT; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA SYNTHESIS; RNA TRANSCRIPTION; VIRUS CAPSID; VIRUS GENOME;

BENZIMIDAZOLES; CYTOMEGALOVIRUS; DNA, VIRAL; ENZYME INHIBITORS; GENOME, VIRAL; HUMANS; NUCLEIC ACID SYNTHESIS INHIBITORS; PROTEIN SYNTHESIS INHIBITORS; RIBONUCLEOSIDES; VIRUS REPLICATION;

GUINEA PIG CYTOMEGALOVIRUS; HERPESVIRIDAE; HUMAN HERPESVIRUS 5; MIRIDAE;

EID: 23844490714     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.17.11115-11127.2005     Document Type: Article

References (66)

1. Abbotts, A. P., V. G. Preston, M. Hughes, A. H. Patel, and N. D. Stow. 2000. Interaction of the herpes simplex virus type 1 packaging protein UL15 with full-length and deleted forms of the UL28 protein. J. Gen. Virol. 81:2999-3009.
2. Abe, A., T. Takeo, N. Emi, M. Tanimoto, R. Ueda, J. K. Yee, T. Friedmann, and H. Saito. 1993. Transduction of a drug-sensitive toxic gene into human leukemia cell lines with a novel retroviral vector. Proc. Soc. Exp. Biol. Med. 203:354-359.
3. Adelman, K., B. Salmon, and J. D. Baines. 2001. Herpes simplex virus DNA packaging sequences adopt novel structures that are specifically recognized by a component of the cleavage and packaging machinery. Proc. Natl. Acad. Sci. USA 98:3086-3091.
4. Adler, S. P. 1986. Molecular epidemiology of cytomegalovirus: evidence for viral transmission to parents from children infected at a day care center. Pediatr. Infect. Dis. 5:315-318.
5. Bartel, P. L., J. A. Roecklein, D. SenGupta, and S. Fields. 1996. A protein linkage map of Escherichia coli bacteriophage T7. Nat. Genet. 12:72-77.
6. Bataille, D., and A. Epstein. 1994. Herpes simplex virus replicative concatemers contain L components in inverted orientation. Virology 203:384-388.
7. Beard, P. M., N. S. Taus, and J. D. Baines. 2002. DNA cleavage and packaging proteins encoded by genes U(L)28, U(L)15, and U(L)33 of herpes simplex virus type 1 form a complex in infected cells. J. Virol. 76:4785-4791.
8. Ben-Porat, T. 1983. Replication of herpesvirus DNA, p. 81-106. In B. Roizman (ed.), The herpesviruses. Plenum Press, New York, N.Y.
9. Berger, N. A., and E. S. Johnson. 1976. DNA synthesis in permeabilized mouse L cells. Biochim. Biophys. Acta 425:1-17.
10. Bhattacharyya, S. P., and V. B. Rao. 1993. A novel terminase activity associated with the DNA packaging protein gp17 of bacteriophage T4. Virology 196:34-44.
11. Biron, K. K., R. J. Harvey, S. C. Chamberlain, S. S. Good, A. A. Smith III, M. G. Davis, C. L. Talarico, W. H. Miller, R. Ferris, R. E. Dornsife, S. C. Stanat, J. C. Drach, L. B. Townsend, and G. W. Koszalka. 2002. Potent and selective inhibition of human cytomegalovirus replication by 1263W94, a benzimidazole L-riboside with a unique mode of action. Antimicrob. Agents Chemother. 46:2365-2372.
12. Black, L. W. 1989. DNA packaging in dsDNA bacteriophages. Annu. Rev. Microbiol. 43:267-292.
13. Bogner, E., K. Radsak, and M. F. Stinski. 1998. The gene product of human cytomegalovirus open reading frame UL56 binds the pac motif and has specific nuclease activity. J. Virol. 72:2259-2264.
14. Brown, J. C., M. A. McVoy, and F. L. Homa. 2002. Packaging DNA into herpesvirus capsids. In E. Bogner and A. Holzenburg (ed.), Structure-function relationships of human pathogenic viruses. Kluwer Academic/Plenum Publishers, London, United Kingdom.
15. Buerger, I., J. Reefschlaeger, W. Bender, P. Eckenberg, A. Popp, O. Weber, S. Graeper, H. D. Klenk, H. Ruebsamen-Waigmann, and S. Hallenberger. 2001. A novel nonnucleoside inhibitor specifically targets cytomegalovirus DNA maturation via the UL89 and UL56 gene products. J. Virol. 75:9077-9086.
16. Chung, Y. B., and D. C. Hinkle. 1990. Bacteriophage T7 DNA packaging. II. Analysis of the DNA sequences required for packaging using a plasmid transduction assay. J. Mol. Biol. 216:927-938.
17. Church, G. A., A. Dasgupta, and D. W. Wilson. 1998. Herpes simplex virus DNA packaging without measurable DNA synthesis. J. Virol. 72:2745-2751.
18. Church, G. A., and D. W. Wilson. 1997. Study of herpes simplex virus maturation during a synchronous wave of assembly. J. Virol. 71:3603-3612.
19. Deiss, L. P., and N. Frenkel. 1986. Herpes simplex virus amplicon: cleavage of concatemeric DNA is linked to packaging and involves amplification of the terminally reiterated a sequence. J. Virol. 57:933-941.
20. Dunn, J. J., and F. W. Studier. 1983. Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J. Mol. Biol. 166:477-535.
21. Fujisawa, H., and K. Sugimoto. 1983. On the terminally redundant sequences of bacteriophage T3 DNA. Virology 124:251-258.
22. Garber, D. A., S. M. Beverley, and D. M. Coen. 1993. Demonstration of circularization of herpes simplex virus DNA following infection using pulsed field gel electrophoresis. Virology 197:459-462.
23. Gerlach, V. L., W. J. Feaver, P. L. Fischhaber, and E. C. Friedberg. 2001. Purification and characterization of pol kappa, a DNA polymerase encoded by the human DINB1 gene. J. Biol. Chem. 276:92-98.
24. Greaves, R. F., J. M. Brown, J. Vieira, and E. S. Mocarski. 1995. Selectable insertion and deletion mutagenesis of the human cytomegalovirus genome using the Escherichia coli guanosine phosphoribosyl transferase (gpt) gene. J. Gen. Virol. 76:2151-2160.
25. Hwang, J. S., and E. Bogner. 2002. ATPase activity of the terminase subunit pUL56 of human cytomegalovirus. J. Biol. Chem. 277:6943-6948.
26. Isom, H. C., M. Gao, and B. Wigdahl. 1984. Characterization of guinea pig cytomegalovirus DNA. J. Virol. 49:426-436.
27. Jacob, R. J., L. S. Morse, and B. Roizman. 1979. Anatomy of herpes simplex virus DNA. XII. Accumulation of head-to-tail concatemers in nuclei of infected cells and their role in the generation of the four isomeric arrangements of viral DNA. J. Virol. 29:448-457.
28. Koslowski, K. M., P. R. Shaver, J. T. Casey II, T. Wilson, G. Yamanaka, A. K. Sheaffer, D. J. Tenney, and N. E. Pederson. 1999. Physical and functional interactions between the herpes simplex virus UL15 and UL28 DNA cleavage and packaging proteins. J. Virol. 73:1704-1707.
29. Koslowski, K. M., P. R. Shaver, X. Y. Wang, D. J. Tenney, and N. E. Pederson. 1997. The pseudorabies virus UL28 protein enters the nucleus after coexpression with the herpes simplex virus UL15 protein. J. Virol. 71:9118-9123.
30. Kramata, P., K. M. Downey, and L. R. Paborsky. 1998. Incorporation and excision of 9-(2-phosphonylmethoxyethyl)guanine (PMEG) by DNA polymerase delta and epsilon in vitro. J. Biol. Chem. 273:21966-21971.
31. Krosky, P. M., M. R. Underwood, S. R. Turk, K. W. Feng, R. K. Jain, R. G. Ptak, A. C. Westerman, K. K. Biron, L. B. Townsend, and J. C. Drach. 1998. Resistance of human cytomegalovirus to benzimidazole ribonucleosides maps to two open reading frames: UL89 and UL56. J. Virol. 72:4721-4728.
32. Langman, L., V. Paetkau, D. Scraba, R. C. Miller, Jr., G. S. Roeder, and P. D. Sadowski. 1978. The structure and maturation of intermediates in bacteriophage T7 DNA replication. Can. J. Biochem. 56:508-516.
33. Littler, E., A. D. Stuart, and M. S. Chee. 1992. Human cytomegalovirus UL97 open reading frame encodes a protein that phosphorylates the antiviral nucleoside analogue ganciclovir. Nature 358:160-162.
34. Maga, G., I. Shevelev, K. Ramadan, S. Spadari, and U. Hubscher. 2002. DNA polymerase theta purified from human cells is a high-fidelity enzyme. J. Mol. Biol. 319:359-369.
35. Mar, E. C., J. F. Chiou, Y. C. Cheng, and E. S. Huang. 1985. Inhibition of cellular DNA polymerase alpha and human cytomegalovirus-induced DNA polymerase by the triphosphates of 9-(2-hydroxyethoxymethyl)guanine and 9-(1,3-dihydroxy-2-propoxymethyl)guanine. J. Virol. 53:776-780.
36. Martinez, R., R. T. Sarisky, P. C. Weber, and S. K. Weller. 1996. Herpes simplex virus type 1 alkaline nuclease is required for efficient processing of viral DNA replication intermediates. J. Virol. 70:2075-2085.
37. Masutani, C., M. Araki, A. Yamada, R. Kusumoto, T. Nogimori, T. Maekawa, S. Iwai, and F. Hanaoka. 1999. Xeroderma pigmentosum variant (XP-V) correcting protein from HeLa cells has a thymine dimer bypass DNA polymerase activity. EMBO J. 18:3491-3501.
38. McVoy, M. A., and S. P. Adler. 1994. Human cytomegalovirus DNA replicates after early circularization by concatemer formation, and inversion occurs within the concatemer. J. Virol. 68:1040-1051.
39. McVoy, M. A., D. E. Nixon, and S. P. Adler. 1997. Circularization and cleavage of guinea pig cytomegalovirus genomes. J. Virol. 71:4209-4217.
40. McVoy, M. A., D. E. Nixon, J. K. Hur, and S. P. Adler. 2000. The ends on herpesvirus DNA replicative concatemers contain pac2 cis cleavage/packaging elements and their formation is controlled by terminal cis sequences. J. Virol. 74:1587-1592.
41. Mocarski, E. S., A. C. Liu, and R. R. Spaete. 1987. Structure and variability of the a sequence in the genome of human cytomegalovirus (Towne strain). J. Gen. Virol. 68:2223-2230.
42. Morita, M., M. Tasaka, and H. Fujisawa. 1993. DNA packaging ATPase of bacteriophage T3. Virology 193:748-752.
43. Nixon, D. E., and M. A. McVoy. 2004. Dramatic effects of 2-bromo-5,6-dichloro-1-beta-D-ribofuranosyl benzimidazole riboside on the genome structure, packaging, and egress of guinea pig cytomegalovirus. J. Virol. 78:1623-1635.
44. Nixon, D. E., and M. A. McVoy. 2002. Terminally repeated sequences on a herpesvirus genome are deleted following circularization but are reconstituted by duplication during cleavage and packaging of concatemeric DNA. J. Virol. 76:2009-2013.
45. Pisarev, V. M., S. H. Lee, M. C. Connelly, and A. Fridland. 1997. Intracellular metabolism and action of acyclic nucleoside phosphonates on DNA replication. Mol. Pharmacol. 52:63-68.
46. Ramadan, K., I. V. Shevelev, G. Maga, and U. Hubscher. 2002. DNA polymerase lambda from calf thymus preferentially replicates damaged DNA. J. Biol. Chem. 277:18454-18458.
47. Reuven, N. B., S. Willcox, J. D. Griffith, and S. K. Weller. 2004. Catalysis of strand exchange by the HSV-1 UL12 and ICP8 proteins: potent ICP8 recombinase activity is revealed upon resection of dsDNA substrate by nuclease. J. Mol. Biol. 342:57-71.
48. Roizman, B., and P. E. Pellett. 2001. The family of Herpesviridae: a brief introduction, p. 2381-2397. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed. Lippincott Williams and Wilkins, Philadelphia, Pa.
49. Roizman, B., and A. E. Sears. 1996. Herpes simplex viruses and their replication, p. 1048-1066. In B. N. Fields, D. M. Knipe, P. M. Howley, R. M. Chanock, J. L. Melnick, T. P. Monath, and B. Roizman (ed.), Fundamental virology. Raven Press, New York, N.Y.
50. Scheffczik, H., C. G. Savva, A. Holzenburg, L. Kolesnikova, and E. Bogner. 2002. The terminase subunits pUL56 and pUL89 of human cytomegalovirus are DNA-metabolizing proteins with toroidal structure. Nucleic Acids Res. 30:1695-1703.
51. Scholz, B., S. Rechter, J. C. Drach, L. B. Townsend, and E. Bogner. 2003. Identification of the ATP-binding site in the terminase subunit pUL56 of human cytomegalovirus. Nucleic Acids Res. 31:1426-1433.
52. Severini, A., A. R. Morgan, D. R. Tovell, and D. L. Tyrrell. 1994. Study of the structure of replicative intermediates of HSV-1 DNA by pulsed-field gel electrophoresis. Virology 200:428-435.
53. Shao, L., L. M. Rapp, and S. K. Weller. 1993. Herpes simplex virus 1 alkaline nuclease is required for efficient egress of capsids from the nucleus. Virology 196:146-162.
54. Shcherbakova, P. V., K. Bebenek, and T. A. Kunkel. 2003. Functions of eukaryotic DNA polymerases. Sci. Aging Knowledge Environ. 2003:RE3.
55. Shimizu, K., Y. Kawasaki, S. Hiraga, M. Tawaramoto, N. Nakashima, and A. Sugino. 2002. The fifth essential DNA polymerase phi in Saccharomyces cerevisiae is localized to the nucleolus and plays an important role in synthesis of rRNA. Proc. Natl. Acad. Sci. USA 99:9133-9138.
56. Stinski, M. F. 1991. Cytomegalovirus and its replication, p. 929-950. In B. N. Fields and D. M. Knipe (ed.). Fundamental virology, 2nd ed. Raven Press, New York, N.Y.
57. Takeuchi, R., M. Oshige, M. Uchida, G. Ishikawa, K. Takata, K. Shimanouchi, Y. Kanai, T. Ruike, H. Morioka, and K. Sakaguchi. 2004. Purification of Drosophila DNA polymerase zeta by REV1 protein-affinity chromatography. Biochem. J. 382:535-543.
58. Tamashiro, J. C., and D. H. Spector. 1986. Terminal structure and heterogeneity in human cytomegalovirus strain AD169. J. Virol. 59:591-604.
59. Tissier, A., J. P. McDonald, E. G. Frank, and R. Woodgate. 2000. poliota, a remarkably error-prone human DNA polymerase. Genes Dev. 14:1642-1650.
60. Underwood, M. R., R. G. Ferris, D. W. Selleseth, M. G. Davis, J. C. Drach, L. B. Townsend, K. K. Biron, and F. L. Boyd. 2004. Mechanism of action of the ribopyranoside benzimidazole GW275175X against human cytomegalovirus. Antimicrob. Agents Chemother. 48:1647-1651.
61. Underwood, M. R., R. J. Harvey, S. C. Stanat, M. L. Hemphill, T. Miller, J. C. Drach, L. B. Townsend, and K. K. Biron. 1998. Inhibition of human cytomegalovirus DNA maturation by a benzimidazole ribonucleoside is mediated through the UL89 gene product. J. Virol. 72:717-725.
62. Varmuza, S. L., and J. R. Smiley. 1985. Signals for site-specific cleavage of HSV DNA: maturation involves two separate cleavage events at sites distal to the recognition sequences. Cell 41:793-802.
63. White, J. H., and C. C. Richardson. 1987. Processing of concatemers of bacteriophage T7 DNA in vitro. J. Biol. Chem. 262:8851-8860.
64. Wist, E., and H. Prydz. 1979. The effect of aphidicolin on DNA synthesis in isolated HeLa cell nuclei. Nucleic Acids Res. 6:1583-1590.
65. Wright, G. E., and N. C. Brown. 1990. Deoxyribonucleotide analogs as inhibitors and substrates of DNA polymerases. Pharmacol. Ther. 47:447-497.
66. Zhang, X., S. Efstathiou, and A. Simmons. 1994. Identification of novel herpes simplex virus replicative intermediates by field inversion gel electrophoresis: implications for viral DNA amplification strategies. Virology 202:530-539.