Human herpesvirus 8-encoded thymidine kinase and phoshpotransferase homologues confer sensitivity to ganciclovir

Journal of Virology

Volumn 73, Issue 6, 1999, Pages 4786-4793

  Cannon, Jennifer S ^a   Hamzeh, Fayez ^a   Moore, Stacy ^a   Nicholas, John ^a   Ambinder, Richard F ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; GANCICLOVIR; PHOSPHOTRANSFERASE; THYMIDINE KINASE; TRITIUM;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG SENSITIVITY; ENZYME ACTIVITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN HERPESVIRUS 8; KAPOSI SARCOMA; LYMPHOMA CELL; NONHUMAN; NORTHERN BLOTTING; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; VIRUS GENOME; VIRUS INFECTION;

EID: 0033040349     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.73.6.4786-4793.1999     Document Type: Article

References (60)

1. Alam, J., and J. L. Cook. 1990. Reporter genes: application to the study of mammalian gene transcription. Anal. Biochem. 188:245-254.
2. Alrabiah, F. A., and S. L. Sacks. 1996. New antiherpesvirus agents. Their targets and therapeutic potential. Drugs 52:17-32.
3. Balasubramanian, N. K., V. Veerisetty, and G. A. Gentry. 1990. Herpesviral deoxythymidine kinases contain a site analogous to the phosphoryl-binding arginine-rich region of porcine adenylate kinase; comparison of secondary structure predictions and conservation. J. Gen. Virol. 71:2979-2987.
4. Baldanti, F., E. Silini, A. Sarasini, C. L. Talarico, S. C. Stanat, K. K. Biron, M. Furione, F. Bono, G. Palù, and G. Gerna. 1995. A three-nucleotide deletion in the UL97 open reading frame is responsible for the ganciclovir resistance of a human cytomegalovirus clinical isolate. J. Virol. 69:796-800.
5. Balzarini, J., C. Bohmann, R. Walker, and E. De Clercq. 1994. Comparative cytostatic activity of different antiherpetic drugs against herpes simplex virus thymidine kinase gene-transfected tumor cells. Mol. Pharmacol. 40:1253-1258.
6. Balzarini, J., E. De Clercq, D. Ayusawa, and T. Seno. 1985. Murine mammary FM3A carcinoma cells transformed with the herpes simplex virus type 1 thymidine kinase gene are highly sensitive to the growth-inhibitory properties of (E)-5-(2-bromovinyl)-2′-deoxyuridine and related compounds. FEBS Lett. 185:95-100.
7. Bean, B. 1992. Antiviral therapy: current concepts and practices. Clin. Microbiol. Rev. 5:146-182.
8. Biron, K. K. 1994. Ganciclovir resistance of cytomegalovirus: mechanisms and prospects for rapid detection. Int. Antivir. News 2:117-118.
9. Biron, K. K., S. C. Stanat, J. B. Sorrell, J. A. Fyfe, P. M. Keller, C. U. Lambe, and D. J. Nelson. 1985. Metabolic activation of the nucleoside analog 9-{[2-hydroxy-1-(hydroxymethyl)ethoxy]methyl}guanine in human diploid fibroblasts infected with human cytomegalovirus. Proc. Natl. Acad. Sci. USA 82:2473-2477.
10. Boshoff, C., D. Whitby, T. Hatznoannou, C. Fisher, J. van der Wait, A. Hatzakis, R. Weiss, and T. Schulz. 1995. Kaposi's-sarcoma-associated herpesvirus in HIV-negative Kaposi's sarcoma. Lancet 345:1043-1044.
11. Boyd, M. R., S. Safrin, and E. R. Kern. 1993. Penciclovir: a review of its spectrum of activity, selectivity, and cross-resistance pattern. Antivir. Chem. Chemother. 4:3-11.
12. Campione-Piccardo, J., W. E. Rawls, and S. Bacchetti. 1979. Selective assay for herpes simplex viruses expressing thymidine kinase. J. Virol. 31:281-287.
13. Cannon, J. S., A. C. Hawkins, C. A. Griffin, Q. Tao, M. J. Borowitz, G. S. Hayward, and R. F. Ambinder. 1999. Unpublished data.
14. Cesarman, E., Y. Chang, P. S. Moore, J. W. Said, and D. M. Knowles. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N. Engl. J. Med. 332:1185-1191.
15. Chang, Y., E. Cesarman, M. S. Pessin, F. Lee, J. Culpepper, D. M. Knowles, and P. S. Moore. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266:1865-1869.
16. Chee, M., G. L. Lawrence, and B. G. Barrell. 1989. Alpha-, beta-, and gammaherpesviruses encode a putative phosphotransferase. J. Gen. Virol. 70:1151-1160.
17. Cheng, E. H., J. Nicholas, D. S. Bellows, G. S. Hayward, H. G. Guo, M. S. Reitz, and J. M. Hardwick. 1997. A Bcl-2 homolog encoded by Kaposi sarcoma-associated virus, human herpesvirus 8, inhibits apoptosis but does not heterodimerize with Bax or Bak. Proc. Natl. Acad. Sci. USA 94:690-694.
18. Chomczynskl, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:156-159.
19. Chou, S., A. Erice, M. C. Jordan, G. M. Vercellotti, K. R. Michels, C. L. Talarico, S. C. Stanat, and K. K. Biron. 1995. Analysis of the UL97 phosphotransferase coding sequence in clinical cytomegalovirus isolates and identification of mutations conferring ganciclovir resistance. J. Infect. Dis. 171:576-583.
20. Chou, S., S. Guentzel, K. R. Michels, R. C. Miner, and W. L. Drew. 1995. Frequency of UL97 phosphotransferase mutations related to ganciclovir resistance in clinical cytomegalovirus isolates. J. Infect. Dis. 172:239-242.
21. De Clereq, E. 1984. The antiviral spectrum of (E)-5-(2-bromovinyl)-2′-deoxyuridine. J. Antimicrob. Chemother. 14:85-95.
22. De Clereq, E. 1997. In search of a selective antiviral chemotherapy. Clin. Microbiol. Rev. 10:674-693.
23. Elion, G. B., P. A. Furman, J. A. Fyfe, P. De Miranda, L. Beauchamp, and H. J. Schaeffer. 1977. Selectivity of action of an antiherpetic agent, 9-(2-hydroxyethoxymethyl)guanine. Proc. Natl. Acad. Sci. USA 74:5716-5720.
24. Faulds, D., and R. C. Heel. 1990. Ganciclovir: a review of its antiviral activity, pharmacokinetic properties and therapeutic efficacy in cytomegalovirus infections. Drugs 39:597-638.
25. Glesby, M., D. Hoover, S. Weng, N. Graham, J. Phair, R. Detels, M. Ho, and A. Saah. 1996. Use of antiherpes drugs and the risk of Kaposi's sarcoma: data from the multicenter AIDS cohort study. J. Infect. Dis. 173:1477-1480.
26. Golumbek, P. T., F. M. Hamzeh, P. S. Lietman, and D. M. Pardoll. 1992. Herpes simplex 1 thymidine kinase gene is unable to completely eliminate live, nonimmunogenic tumor cell vaccines. J. Immunother. 12:224-230.
27. Gustafson, E. A., A. C. Chillemi, D. R. Sage, and J. D. Fingeroth. 1998. The Epstein-Barr virus thymidine kinase does not phosphorylate ganciclovir or acyclovir and demonstrates a narrow substrate specificity compared to the herpes simplex virus type 1 thymidine kinase. Antimicrob. Agents Chemother, 42:2923-2931.
28. Hanson, M. N., L. C. Preheim, S. Chou, C. L. Talarico, K. Biron, and A. Erice. 1995. Novel mutation in the UL97 gene of a clinical cytomegalovirus strain conferring resistance to ganciclovir. Antimicrob. Agents Chemother. 39:1204-1205.
29. Harrison, P. T., R. Thompson, and A. J. Davison. 1991. Evolution of herpesvirus thymidine kinases from cellular deoxycytidine kinase. J. Gen. Virol. 72:2583-2586.
30. He, Z., Y. S. He, Y. Kim, L. Chu, C. Ohmstede, K. K. Biron, and D. M. Coen. 1997. The human cytomegalovirus UL97 protein is a protein kinase that autophosphorylates on serines and threonines. J. Virol. 71:405-411.
31. Higgins, D. G., and P. M. Sharp. 1989. Fast and sensitive multiple sequence alignments on a microcomputer. CABIOS 5:151-153.
32. Honess, R. W., M. A. Craxton, L. L. Williams, and U. A. Gompels. 1989. A comparative analysis of the sequence of the thymidine kinase gene of a gammaherpesvirus, herpesvirus saimiri. J. Gen. Virol. 70:3003-3013.
33. Kedes, D. H., and D. Ganem. 1997. Sensitivity of Kaposi's sarcoma-associated herpesvirus replication to antiviral drugs. J. Clin. Investig. 99:2082-2086.
34. Larder, B. A., G. Darby, and D. Richman. 1989. HIV with reduced sensitivity to zidovudine (AZT) isolated during prolonged therapy. Science 243:1731-1734.
35. Leader, D. P. 1993. Viral protein kinases and protein phosphatases. Pharmacol. Ther. 59:343-389.
36. Littler, E., A. D. Stuart, and M. Chee. 1992. Human cytomegalovirus UL97 open reading frame encodes a protein that phosphorylates the antiviral nucleoside analogue ganciclovir. Nature 358:160-162.
37. Littler, E., J. Zeuthen, A. A. McBride, E. Trost Sorensen, K. L. Powell, J. E. Walsh-Arrand, and J. R. Arrand. 1986. Identification of an Epstein-Barr virus-coded thymidine kinase. EMBO J. 5:1959-1966.
38. Lomonte, P., M. Bublot, P.-P. Pastoret, and E. Thiry. 1992. Location and characterization of the bovine herpesvirus type 4 thymidine kinase gene; comparison with thymidine kinase genes of other herpesviruses. Arch. Virol. 127:327-337.
39. Mar, E.-C., J.-F. Chiou, Y.-C. Cheng, and E.-S. Huang. 1985. Inhibition of cellular DNA polymerase α 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.
40. McGuirt, P. V., and P. A. Furman. 1982. Acyclovir inhibition of viral DNA chain elongation in herpes simplex virus infected cells. Am. J. Med. 73:67-71.
41. Medveczky, M., E. Horvath, T. Lund, and P. Medveczky. 1997. In vitro antiviral drug sensitivity of the Kaposi's sarcoma-associated herpesvirus. AIDS 11:1327-1332.
42. Michel, D., P. Schaarschmidt, K. Wunderlich, M. Heuschmid, L. Simoncini, D. Muhlberger, A. Zimmermann, I. Pavic, and T. Mertens. 1998. Functional regions of the human cytomegalovirus protein pUL97 involved in nuclear localization and phosphorylation of ganciclovir and pUL97 itself. J. Gen. Virol. 79:2105-2112.
43. Mocroft, A., M. Youle, B. Gazzard, J. Morinek, R. Halai, and A. Phillips. 1996. Antiherpesvirus treatment and risk of Kaposi's sarcoma in HIV infection. AIDS 10:1101-1105.
44. Moore, P. S., S.-J. Gao, G. Dominguez, E. Cesarman, O. Lungu, D. M. Knowles, R. Garber, P. E. Pellet, D. J. McGeoch, and Y. Chang. 1996. Primary characterization of a herpesvirus agent associated with Kaposi's sarcoma. J. Virol. 70:549-558.
45. Neyts, J., G. Andrei, R. Snoeck, G. Jähne, I. Winkler, M. Helsberg, J. Balzarini, and E. De Clercq. 1994. The N-7-substituted acyclic nucleoside analog 2-amino-7[(1,3-dihydroxy-2-propoxy)methyl]purine is a potent and selective inhibitor of herpesvirus replication. Antimicrob. Agents Chemother. 38:2710-2716.
46. Neyts, J., and E. De Clercq. 1997. Antiviral drug susceptibility of human herpesvirus 8. Antimicrob. Agents Chemother. 41:2754-2756.
47. Ng, T. I., and C. Grose. 1992. Serine protein kinase associated with varicella-zoster virus ORF 47. Virology 191:9-18.
48. Ng, T. I., L. Keenan, P. R. Kinchington, and C. Grose. 1994. Phosphorylation of varicella-zoster virus open reading frame (ORF) 62 regulatory product by viral ORF 47-associated protein kinase. J. Virol. 68:1350-1359.
49. Purves, F. C., W. O. Ogle, and B. Roizman. 1993. Processing of the herpes simplex virus regulatory protein α22 mediated by the UL13 protein kinase determines the accumulation of a subset of alpha and gamma mRNAs and proteins in infected cells. Proc. Natl. Acad. Sci. USA 90:6701-6705.
50. Purves, F. C., and B. Roizman. 1992. The UL13 gene of herpes simplex virus 1 encodes the functions for posttranslational processing associated with phosphorylation of the regulatory protein alpha 22. Proc. Natl. Acad. Sci. USA 89:7310-7314.
51. Robertson, G. R., and J. M. Walley. 1988. Evolution of the herpes thymidine kinase: identification and comparison of the equine herpesvirus I thymidine kinase gene reveals similarity to a cell-encoded thymidylate kinase. Nucleic Acids Res. 16:11303-11317.
52. Russo, J. J., R. A. Bohenzky, M.-C. Chien, J. Chen, M. Yan, D. Maddalena, J. P. Parry, D. Peruzzi, I. S. Edelman, Y. Chang, and P. S. Moore. 1996. Nucleotide sequence of Kaposi's sarcoma-associated herpesvirus (HHV8). Proc. Natl. Acad. Sci. USA 93:14862-14868.
53. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
54. Shiraki, K., H. Mori, Y. Haya, K. Yamanishi, and M. Takahashi. 1989. Regulation of thymidine kinase activity in mouse L cells biochemically transformed by varicella-zoster virus. Microbiol. Immunol. 33:693-698.
55. Slusher, J. T., S. K. Kuwahara, F. M. Hamzeh, L. D. Lewis, D. M. Kornhauser, and P. S. Lietman. 1992. Intracellular zidovudine (ZDV) and ZDV phosphates as measured by a validated combined high-pressure liquid chromatography-radioimmunoassay procedure. Antimicrob. Agents Chemother. 36:2473-2477.
56. Smee, D. F. 1985. Interaction of 9-(1,3-dihydroxy-2-propoxymethyl)guanine with cytosol and mitochondrial deoxyguanosine kinases: possible role in anti-cytomegalovirus activity. Mol. Cell. Biochem. 69:75-81.
57. Smith, R. F., and T. F. Smith. 1989. Identification of new protein kinase-related genes in three herpesviruses, herpes simplex virus, varicella-zoster virus, and Epstein-Barr virus. J. Virol. 63:450-455.
58. Sullivan, V., C. L. Talarico, S. C. Stanat, M. Davis, D. M. Coen, and K. K. Biron. 1992. A protein kinase homologue controls phosphorylation of ganciclovir in human cytomegalovirus-infected cells. Nature 358:162-164.
59. Wolf, D. G., A. Honigman, J. Lazarovits, E. Tavor, and A. Panet. 1998. Characterization of the human cytomegalovirus UL97 gene product as a virion-associated protein kinase. Arch. Virol. 143:1223-1232.
60. Zimmermann, A., D. Michel, I. Pavic, W. Hampl, A. Luske, J. Neyts, E. De Clercq, and T. Mertens. 1997. Phosphorylation of aciclovir, ganciclovir, penciclovir, and S2242 by the cytomegalovirus UL97 protein: a quantitative analysis using recombinant vaccinia viruses. Antivir. Res. 36:35-42.