Resistance of human cytomegalovirus to antiviral drugs

Clinical Microbiology Reviews

Volumn 12, Issue 2, 1999, Pages 286-297

  Erice, Alejo ^a,b  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; CIDOFOVIR; DNA POLYMERASE; FOSCARNET; GANCICLOVIR;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; BONE MARROW TRANSPLANTATION; CROSS RESISTANCE; CYTOMEGALIC INCLUSION BODY DISEASE; DRUG RESISTANCE; GENE MUTATION; HUMAN CYTOMEGALOVIRUS; IMMUNE DEFICIENCY; LEUKEMIA; NONHUMAN; ORGAN TRANSPLANTATION; REVIEW;

EID: 0032890689     PISSN: 08938512     EISSN: None     Source Type: Journal    
DOI: 10.1128/cmr.12.2.286     Document Type: Review

References (72)

1. Alain, S., P. Honderlick, D. Grenet, M. Stern, C. Vadam, M. Sanson-Le Pors, and M. Mazeron. 1997. Failure of ganciclovir treatment associated with selection of a ganciclovir-resistant cytomegalovirus strain in a lung transplant recipient. Transplantation 63:1533-1536.
2. Baldanti, F., E. Silini, A. Sarasini, C. L. Talarico, S. C. Stanat, K. K. Biron, M. Furione, F. Bono, G. Palú, 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.
3. Baldanti, F., M. R. Underwood, S. C. Stanat, K. K. Biron, S. Chou, A. Sarasini, E. Silini, and G. Gerna. 1996. Single amino acid changes in the DNA polymerase confer foscarnet resistance and slow-growth phenotype. while mutations in the UL97-encoded phosphotransferase confer ganciclovir resistance in three double-resistant human cytomegalovirus strains recovered from patients with AIDS. J. Virol. 70:1390-1395.
4. Baldanti, F., M. R. Underwood, C. L. Talarico, L. Simoncini, A. Sarasini, K. K. Biron, and G. Gerna. 1998. The Cys607Tyr change in the UL97 phosphotransferse confers ganciclovir resistance to two human cytomegalovirus strains recovered from two immunocompromised individuals. Antimicrob. Agents Chemother. 42:444-446.
5. Balfour, H. H., Jr. 1990. Management of cytomegalovirus disease with antiviral drugs. Rev. Infect. Dis. 12(Suppl. 7):S849-S860.
6. Biron, K. K., J. A. Fyfe, S. C. Stanat, L. K. Leslie, J. B. Sorrell, C. U. Lambe, and D. M. Coen. 1986. A human cytomegalovirus mutant resistant to the nucleoside analog 9-{[2-hydroxy-1-(hydroxymethyl)ethoxy]methyl}guanine (BW B759U) induces reduced levels of BW B759U triphosphate. Proc. Natl. Acad. Sci. USA 83:8769-8773.
7. Biron, K. K. 1996. Cytomegalovirus: genetics of drug resistance, p. 135-143. In J. Mills (ed), Antiviral chemotherapy, vol. 4. Plenum Press, New York, N.Y.
8. Boivin, G., A. Erice, D. D. Crane, D. L. Dunn, and H. H. Balfour, Jr. 1993. Ganciclovir susceptibilities of cytomegalovirus (CMV) isolates from solid organ transplant recipients with CMV viremia after antiviral prophylaxis. J. Infect. Dis. 168:332-335.
9. Boivin, G., S. Chou, M. R. Quirk, A. Erice, and M. C. Jordan. 1996. Detection of ganciclovir resistance mutations and quantitation of cytomegalovirus (CMV) DNA in leukocytes of patients with fatal disseminated CMV disease. J. Infect. Dis. 173:523-528.
10. Cherrington, J. M., R. Miner, M. J. M. Hitchcock, J. P. Lalezari, and W. L. Drew. 1996. Susceptibility of human cytomegalovirus to cidofovir is unchanged after limited in vivo exposure to various clinical regimens of drug. J. Infect. Dis. 173:987-992.
11. Cherrington, J. M., M. D. Fuller, P. D. Lamy, R. Miner, J. P. Lalezari, S. Nuessle, and W. L. Drew. 1998. In vitro antiviral susceptibilities of isolates from CMV retinitis patients receiving first or second line cidofovir therapy: relationship to clinical outcome. J. Infect. Dis. 178:1821-1825.
12. 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.
13. 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.
14. Chou, S., G. Marousek, S. Guentzel, S. E. Follansbee, M. E. Poscher, J. P. Lalezari, R. C. Miner, and W. L. Drew. 1997. Evolution of mutations conferring multidrug resistance during prophylaxis and therapy for cytomegalovirus disease. J. Infect. Dis. 176:786-789.
15. Chou, S., G. Marousek, D. M. Parenti, S. M. Gordon, A. G. LaVoy, J. G. Ross, R. C. Miner, and W. L. Drew. 1998. Mutation in region II of the DNA polymerase gene conferring foscarnet resistance in cytomegalovirus isolates from 3 subjects receiving prolonged antiviral therapy. J. Infect. Dis. 178:526-530.
16. Cihlar, T., M. D. Fuller, and J. M. Cherrington. 1998. Characterization of drug resistance-associated mutations in the human cytomegalovirus DNA polymerase gene by using recombinant mutant viruses generated from overlapping DNA fragments. J. Virol. 72:5927-5936.
17. Cole, N. L., and H. H. Balfour, Jr. 1987. In vitro susceptibility of cytomegalovirus isolates from immunocompromised patients to acyclovir and ganciclovir. Diagn. Microbiol. Infect. Dis. 6:255-261.
18. Chrisp, P., and S. P. Clissold. 1991. Foscarnet: a review of its antiviral activity, pharmacokinetic properties, and therapeutic use in immunocompromised patients with CMV retinitis. Drugs 41:104-129.
19. Crumpacker, C. S., F. Baldanti, M. Boeck, S. Chou, S. Danner, W. L. Drew, D. Emanuel, A. Erice, W. D. Hardy, and S. A. Spector. 1996. Drug resistance in cytomegalovirus: current knowledge and implications for patient management. J. Acquired Immune Defic. Syndr. Hum. Retrovirol. 12(Suppl. 1):S1-S22.
20. Crumpacker, C. S. 1996. Ganciclovir. N. Engl. J. Med. 335:721-729.
21. Dankner, W. M., D. Scholl, S. C. Stanat, M. Martin, R. L. Sonke, and S. A. Spector. 1990. Rapid antiviral DNA-DNA hybridization assay for human cytomegalovirus. J. Virol. Methods 28:293-298.
22. De Clercq, E. 1993. Therapeutic potential of HPMPC as an antiviral drug. Rev. Med. Virol. 3:85-96.
23. Drew, W. L., R. C. Miner, D. F. Busch, S. E. Follansbee, J. Gullett, S. G. Mehalko, S. M. Gordon, W. F. Owen, Jr., T. R. Matthews, W. C. Buhles, and B. DeArmond. 1991. Prevalence of resistance in patients receiving ganciclovir for serious cytomegalovirus infections. J. Infect. Dis. 163:716-719.
24. Drew, W. L., R. Miner, and E. Saleh. 1993. Antiviral susceptibility testing of cytomegalovirus: criteria for detecting resistance to antivirals. Clin. Diagn. Virol. 1:179-185.
25. Drew, W. L., R. Anderson, W. Lang, R. C. Miner, G. Davis, and J. Lalezari. 1995. Failure of high-dose oral acyclovir to suppress CMV viruria or induce ganciclovir-resistant CMV in HIV antibody positive patients. J. Acquired Immune Defic. Syndr. Hum. Retrovirol. 8:289-291.
26. Drew, W. L., R. C. Miner, M. Crager, and M. J. Stempien. 1995. Does resistance to ganciclovir develop in patients receiving prophylactic drug? abstr. H135, p. 203. In Program and Abstracts of the 35th Interscience Conference on Antimicrobial Agents and Chemotherapy. American Society for Microbiology, Washington, D.C.
27. Drobyski, W. R., K. K. Knox, D. R. Carrigan, and R. C. Ash. 1991. Foscarnet therapy for ganciclovir-resistant cytomegalovirus in marrow transplantation. Transplantation 52:155-157.
28. Erice, A., M. C. Jordan, B. A. Chace, C. Fletcher, B. J. Chinnok, and H. H. Balfour, Jr. 1987. Ganciclovir treatment of cytomegalovirus disease in transplant recipients and other immunocompromised hosts. JAMA 257:3082-3087.
29. Erice, A., S. Chou, K. K. Biron, S. C. Stanat, H. H. Balfour, Jr., and M. C. Jordan. 1989. Progressive disease due to ganciclovir-resistant cytomegalovirus in immunocompromised patients. N. Engl. J. Med. 320:289-293.
30. Erice, A., C. Gil-Roda, J. Pérez, H. H. Balfour, Jr., K. J. Sannerud, M. N. Hanson, G. Boivin, and S. Chou. 1997. Antiviral susceptibilities and analysis of UL97 and DNA polymerase sequences of clinical cytomegalovirus isolates from immunocompromised patients. J. Infect. Dis. 175:1087-1092.
31. Erice, A., N. Borrell, W. Li, W. J. Miller, and H. H. Balfour, Jr. 1998. Ganciclovir susceptibilities and analysis of UL97 region in cytomegalovirus isolates from bone marrow recipients with CMV disease after antiviral prophylaxis. J. Infect. Dis. 178:531-534.
32. Field, A. K., M. E. Davies, C. DeWitt, H. C. Perry, R. Liou, J. Germershausen, J. D. Karkas, W. T. Ashton, D. B. Johnston, and R. L. Tolman. 1983. 9-[2-Hydroxy-1(hydroxymethyl)ethoxy]methyl guanine: a selective inhibitor of herpes group virus replication. Proc. Natl. Acad. Sci. USA 80: 4139-4143.
33. Gerna, G., F. Baldanti, M. Zavattoni, A. Sarasini, E. Percivalle, and M. G. Revello. 1992. Monitoring of ganciclovir sensitivity of multiple human cytomegalovirus strains coinfecting blood of an AIDS patient by an immediate-early antigen plaque assay. Antiviral Res. 19:333-345.
34. Gerna, G., A. Sarasini, E. Percivalle, M. Zavattoni, F. Baldanti, and M. G. Revello. 1995. Rapid screening for resistance to ganciclovir and foscarnet of primary isolates of human cytomega ovirus from culture-positive blood samples. J. Clin. Microbiol. 33:738-741.
35. Gilbert, C., J. Handfield, E. Toma, R. Lalonde, M. G. Bergeron, and G. Boivin. 1998. Emergence and prevalence of cytomegalovirus mutations associated with ganciclovir resistance in AIDS patients. AIDS 12:125-129.
36. Hanson, M. N., L. C. Preheim, S. Chou, C. L. Talarico, K. 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.
37. Harada, K., Y. Eizuru, Y. Isashiki, S. Ihara, and Y. Minamishima. 1997. Genetic analysis of a clinical isolate of human cytomegalovirus exhibiting resistance against both ganciclovir and cidofovir. Arch. Virol. 142:215-225.
38. He, Z., Y. 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.
39. Jabs, D. A., C. Enger, J. P. Dunn, and M. Forman. 1998. Cytomegalovirus retinitis and viral resistance: ganciclovir resistance. J. Infect. Dis. 177:770-773.
40. Jacobson, M. A., and J. Mills. 1988 Serious cytomegalovirus disease in the acquired immunodeficiency syndrome (AIDS). Ann. Intern. Med. 108:585-594.
41. Jacobson, M. A. 1997. Treatment of cytomegalovirus retinitis in patients with the acquired immunodeficiency syndrome. N. Engl. J. Med. 337:105-114.
42. Kemble, G., G. Duke, R. Winter, and R. Spaete. 1996. Defined large-scale alteration of the human cytomegalovirus genome constructed by cotransfection of overlapping cosmids. J. Virol. 70:2044-2048.
43. Kimberlin, D. W., S. A. Spector, E. L. Hill, K. K. Biron, A. J. Hay, D. L. Mayers, and R. J. Whitley. 1995. Assays for antiviral drug resistance. Antiviral Res. 26:403-413.
44. Lalezari, J. P., W. L. Drew, E. Glutzer, C. James, R. C. Miner, J. Flaherty, and P. E. Fisher. 1995. (S)-1-[3-hydroxy-2-(phosphonyl-methoxy)propyl]cytosine (cidofovir): results of a phase I/II study of a novel nucleotide analogue. J. Infect. Dis. 171:788-796.
45. Lalezari, J. P., R. J. Stagg, B. D. Kuppermann, G. N. Holland, F. Kramer, D. Ives, M. Youle, M. R. Robinson, W. L. Drew, and H. S. Jaffe. 1997. Intravenous cidofovir for peripheral cytomegalovirus retinitis in patients with AIDS. Ann. Intern. Med. 126:257-263.
46. 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.
47. Lurain, N. S., K. D. Thompson, E. W. Holmes, and G. S. Read. 1992. Point mutations in the DNA polymerase gene of human cytomegalovirus that result in resistance to antiviral agents. J. Virol. 66:7146-7152.
48. Lurain, N. S., L. E. Spafford, and K. D. Thompson. 1994. Mutation in the UL97 open reading frame of human cytomegalovirus strains resistant to ganciclovir. J. Virol. 68:4427-4431.
49. Lurain, N. S., H. C. Ammons, K. S. Kapell, V. V. Yeldandi, E. R. Garrity, and J. P. O'Keefe. 1996. Molecular analysis of human cytomegalovirus strains from two lung transplant recipients with the same donor. Transplantation 62:497-502.
50. McSharry, J. M., N. S. Lurain, G. L. Drusano, A. Landay, J. Manischewitz, M. Notka, M. O'Gorman, H. M. Shapiro, A. Weinberg, P. Reichelderfer, and C. Crumpacker. 1998. Flow cytometry determination of ganciclovir susceptibilities of human cytomegalovirus isolates. J. Clin. Microbiol. 36:958-964.
51. Miller, W., P. Flynn, J. McCullough, H. H. Balfour, Jr., A. Goldman, R. Haake, P. McGlave, N. Ramsay, and J. Kersey. 1986. Cytomegalovirus infection after bone marrow transplantation: an association with acute graft-v-host disease. Blood 67:1162-1167.
52. Pepin, J. M., F. Simon, A. Dussault, G. Collin, M. Dazza, and F. Brun-Vezinet. 1992. Rapid determination of human cytomegalovirus susceptibility to ganciclovir directly from clinical specimen primocultures. J. Clin. Microbiol. 30:2917-2920.
53. Peterson, P. K., H. H. Balfour, Jr., S. C. Marker, D. S. Fryd, R. J. Howard, and R. L. Simmons. 1980. Cytomegalovirus disease in renal allograft recipients: a prospective study of the clinical features, risk factors, and impact on renal transplantation. Medicine 59:283-300.
54. Reid, R., E. C. Mar, et al. 1988. Insertion and extension of acyclic, dideoxy, and ara nucleotides by herpesviridae and human polymerases. Antimicrob. Agents Chemother. 25:191-194.
55. Reusser, P., C. Cordonnier, H. Einsele, D. Engelhard, H. Link, A. Locasciulli, and P. Ljungman. 1996. European survey of herpesvirus resistance to antiviral drugs in bone marrow transplant recipients. Bone Marrow Transplant. 17:813-817.
56. Slavin, M. A., R. R. Bindra, C. A. Cleaves, M. B. Pettinger, and R. A. Bowden. 1993. Ganciclovir sensitivity of cytomegalovirus at diagnosis and during treatment of cytomegalovirus pneumonia in marrow transplant recipients. Antimicrob. Agents. Chemother. 37:1360-1363.
57. Smith, I. L., M. Shinkai, W. R. Freeman, and S. A. Spector. 1996. Polyradiculopathy associated with ganciclovir-resistant cytomegalovirus in an AIDS patient: phenotypic and genotypic characterization of sequential virus isolates. J. Infect. Dis. 173:1481-1484.
58. Smith, I. L., J. M. Cherrington, R. E. Jiles, M. D. Fuller, W. R. Freeman, and S. A. Spector. 1997. High-level resistance of cytomegalovirus to ganciclovir is associated with alterations in both the UL97 and DNA polymerase genes. J. Infect. Dis. 176:69-77.
59. Smith, I. L., I. Taskintuna, F. M. Rahhal, H. C. Powell, E. Ai, A. J. Mueller, S. A. Spector, and W. E. Freeman. 1998. Clinical failure of CMV retinitis with intravitreal cidofovir is associated with antiviral resistance. Arch. Ophthalmol. 116:178-185.
60. Smith, I. L., C. Hong, M. L. Pilcher, A. M. Shapiro, R. E. Jiles, and S. A. Spector. 1998. Development of resistant cytomegalovirus genotypes during oral ganciclovir prophylaxis/preemptive therapy, abstr. H120, p. 349. In Program and Abstracts of the 38th Interscience Conference on Antimicrobial Agents and Chemotherapy. American Society for Microbiology, Washington, D.C.
61. Stanat, S. C., J. E. Reardon, A. Erice, M. C. Jordan, W. L. Drew, and K. K. Biron. 1991. Ganciclovir-resistant cytomegalovirus clinical isolates: mode of resistance to ganciclovir. Antimicrob. Agents Chemother. 35:2191-2197.
62. Studies of Ocular Complications of AIDS (SOCA) in collaboration with the AIDS Clinical Trials Group. 1997. Cytomegalovirus (CMV) culture results, drug resistance, and clinical outcome in patients with AIDS and CMV retinitis treated with foscarnet or ganciclovir. J. Infect. Dis. 176:50-58.
63. 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.
64. Sullivan, V., and D. M. Coen. 1991. Isolation of foscarnet-resistant human cytomegalovirus patterns of resistance and sensitivity to other antiviral drugs. J. Infect. Dis. 164:781-784.
65. Sullivan, V., K. K. Biron, C. Talarico, S. C. Stanat, M. Davis, L. M. Pozzi, and D. M. Coen. 1993. A point mutation in the human cytomegalovirus DNA polymerase gene confers resistance to ganciclovir and phosphonylmethoxyalkyl derivatives. Antimicrob. Agents Chemother. 37:19-25.
66. Talarico, C. L., S. C. Stanat, and K. K. Biron. 1994. Evidence that HCMV-encoded UL97 contributes to the phosphorylation of acyclovir in HCMV-infected cells, abstr. H65, p. 206. In Program and Abstracts of the 34th Interscience Conference on Antimicrobial Agents and Chemotherapy. American Society for Microbiology, Washington, D.C.
67. Tatarowicz, W. A., N. S. Lurain, and K. D. Thompson. 1991. In situ ELISA for the evaluation of antiviral compounds effective against human cytomegalovirus. J. Virol. Methods 35:207-215.
68. Telenti, A., and T. F. Smith. 1989. Screening with a shell vial assay for antiviral activity against cytomegalovirus. Diagn. Microbiol. Infect. Dis. 12: 5-8.
69. Weinberg, A., S. A. Schneider, B. J. Bate, and J. C. Clark. 1994. Antigen reduction assay for cytomegalovirus susceptibility to antivirals, abstr. H79, p. 207. In Program and Abstracts of the 34th Interscience Conference on Antimicrobial Agents and Chemotherapy. American Society for Microbiology, Washington, D.C.
70. Wolf, D. G., I. L. Smith, D. J. Lee, W. R. Freeman, M. Flores-Aguilar, and S. A. Spector. 1995. Mutations in human cytomegalovirus UL97 gene confer clinical resistance to ganciclovir and can be detected directly in patient plasma. J. Clin. Investig. 95:257-263.
71. Wolf, D. G., D. J. Lee, and S. A. Spector. 1995. Detection of human cytomegalovirus mutations associated with ganciclovir resistance in cerebrospinal fluid of AIDS patients with central nervous system disease. Antimicrob. Agents Chemother. 39:2552-2554.
72. Wolf, D. G., I. Yaniv, A. Honigman, I. Kassis, T. Schonfeld, and S. Ashkenazi. 1998. Early emergence of ganciclovir-resistant human cytomegalovirus strains in children with primary combined immunodeficiency. J. Infect. Dis. 178:535-538.