Heterogeneity and evolution of thymidine kinase and DNA polymerase mutants of herpes simplex virus type 1: Implications for antiviral therapy

Journal of Infectious Diseases

Volumn 207, Issue 8, 2013, Pages 1295-1305

  Andrei, Graciela ^a   Georgala, Aspasia ^b   Topalis, Dimitri ^a   Fiten, Pierre ^a   Aoun, Michel ^b   Opdenakker, Ghislain ^a   Snoeck, Robert ^a  

^a REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^b JULES BORDET INSTITUTE   (Belgium)

Author keywords

DNA polymerase; drug resistance dynamics in HSV; evolution of HSV populations; hematopoietic stem cell transplantation (HSCT); heterogenicity of HSV populations; multiple HSV infections; thymidine kinase

Indexed keywords

ACICLOVIR; AMPHOTERICIN B; AMSACRINE; CIPROFLOXACIN; CORTICOSTEROID; CYCLOSPORIN A; CYTARABINE; DNA POLYMERASE; FLUCONAZOLE; FLUDARABINE; FOSCARNET SODIUM; GANCICLOVIR; IDARUBICIN; MELPHALAN; MOXIFLOXACIN; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PIPERACILLIN; RITUXIMAB; SULFAMETHOXAZOLE; TAZOBACTAM; THYMIDINE KINASE; THYMOCYTE ANTIBODY; TRIMETHOPRIM; VIRUS DNA; VORICONAZOLE;

ADULT; ANTIVIRAL RESISTANCE; ARTICLE; CLINICAL ARTICLE; CLINICAL FEATURE; COMPUTER ASSISTED TOMOGRAPHY; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS RETINITIS; DEATH; DRUG SUBSTITUTION; DRUG WITHDRAWAL; EPSTEIN BARR VIRUS; EPSTEIN BARR VIRUS INFECTION; FEMALE; FEVER; FUNGAL ENDOPHTHALMITIS; GENETIC HETEROGENEITY; GENOTYPE; GRAFT VERSUS HOST REACTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HERPES SIMPLEX VIRUS 1; HERPETIC STOMATITIS; HUMAN; HUMAN CELL; HYPERTHYROIDISM; LUNG ASPERGILLOSIS; MOLECULAR CLONING; MOLECULAR EVOLUTION; MOUTH ULCER; OUTCOME ASSESSMENT; PERICARDIAL EFFUSION; PHENOTYPE; PLEURA EFFUSION; PRIORITY JOURNAL; RESPIRATORY FAILURE; TACHYCARDIA; TREATMENT INDICATION; VIRUS ISOLATION;

ACYCLOVIR; ADULT; DNA, VIRAL; DRUG RESISTANCE, MULTIPLE, VIRAL; EVOLUTION, MOLECULAR; FEMALE; GANCICLOVIR; GENES, POL; GENETIC HETEROGENEITY; GENOTYPE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HERPESVIRUS 1, HUMAN; HUMANS; LEUKEMIA, MYELOID, ACUTE; MUTATION; PHENOTYPE; STOMATITIS, HERPETIC; THYMIDINE KINASE;

EID: 84875605435     PISSN: 00221899     EISSN: None     Source Type: Journal    
DOI: 10.1093/infdis/jit019     Document Type: Article

References (50)

1. Sandherr M, Einsele H, Hebart H, et al. Antiviral prophylaxis in patients with haematological malignancies and solid tumours: Guidelines of the Infectious Diseases Working Party (AGIHO) of the German Society for Hematology and Oncology (DGHO). Ann Oncol 2006; 17:1051-9.
2. Bustamante CI, Wade JC. Herpes simplex virus infection in the immunocompromised cancer patient. J Clin Oncol 1991; 9:1903-15.
3. Danve-Szatanek C, Aymard M, Thouvenot D, et al. Surveillance network for herpes simplex virus resistance to antiviral drugs: 3-year follow-up. J Clin Microbiol 2004; 42:242-9.
4. Frobert E, Cortay JC, Ooka T, et al. Genotypic detection of acyclovirresistant HSV-1: characterization of 67 ACV-sensitive and 14 ACVresistant viruses. Antiviral Res 2008; 79:28-36.
5. Gaudreau A, Hill E, Balfour HH Jr, Erice A, Boivin G. Phenotypic and genotypic characterization of acyclovir-resistant herpes simplex viruses from immunocompromised patients. J Infect Dis 1998; 178:297-303.
6. Morfin F, Souillet G, Bilger K, Ooka T, Aymard M, Thouvenot D. Genetic characterization of thymidine kinase from acyclovir-resistant and -susceptible herpes simplex virus type 1 isolated from bone marrow transplant recipients. J Infect Dis 2000; 182:290-3.
7. Gilbert C, Bestman-Smith J, Boivin G. Resistance of herpesviruses to antiviral drugs: clinical impacts and molecular mechanisms. Drug Resist Updat 2002; 5:88-114.
8. Harris W, Collins P, Fenton RJ, Snowden W, Sowa M, Darby G. Phenotypic and genotypic characterization of clinical isolates of herpes simplex virus resistant to aciclovir. J Gen Virol 2003; 84:1393-401.
9. Piret J, Boivin G. Resistance of herpes simplex viruses to nucleoside analogues: mechanisms, prevalence, and management. Antimicrob Agents Chemother 2011; 55:459-72.
10. Erlich KS, Jacobson MA, Koehler JE, et al. Foscarnet therapy for severe acyclovir-resistant herpes simplex virus type-2 infections in patients with the acquired immunodeficiency syndrome (AIDS). An uncontrolled trial. Ann Intern Med 1989; 110:710-3.
11. Javaly K, Wohlfeiler M, Kalayjian R, et al. Treatment of mucocutaneous herpes simplex virus infections unresponsive to acyclovir with topical foscarnet cream in AIDS patients: a phase I/II study. J Acquir Immune Defic Syndr 1999; 21:301-6.
12. Naik HR, Siddique N, Chandrasekar PH. Foscarnet therapy for acyclovir-resistant herpes simplex virus 1 infection in allogeneic bone marrow transplant recipients. Clin Infect Dis 1995; 21:1514-5.
13. Andrei G, Fiten P, Froeyen M, De Clercq E, Opdenakker G, Snoeck R. DNA polymerase mutations in drug-resistant herpes simplex virus mutants determine in vivo neurovirulence and drug-enzyme interactions. Antivir Ther 2007; 12:719-32.
14. Andrei G, Snoeck R, De Clercq E, Esnouf R, Fiten P, Opdenakker G. Resistance of herpes simplex virus type 1 against different phosphonylmethoxyalkyl derivatives of purines and pyrimidines due to specific mutations in the viral DNA polymerase gene. J Gen Virol 2000; 81:639-48.
15. Saijo M, Suzutani T, Morikawa S, Kurane I. Genotypic characterization of the DNA polymerase and sensitivity to antiviral compounds of foscarnet-resistant herpes simplex virus type 1 (HSV-1) derived from a foscarnet-sensitive HSV-1 strain. Antimicrob Agents Chemother 2005; 49:606-11.
16. Schmit I, Boivin G. Characterization of the DNA polymerase and thymidine kinase genes of herpes simplex virus isolates from AIDS patients in whom acyclovir and foscarnet therapy sequentially failed. J Infect Dis 1999; 180:487-90.
17. Andrei G, Fiten P, Goubau P, et al. Dual infection with polyomavirus BK and acyclovir-resistant herpes simplex virus successfully treated with cidofovir in a bone marrow transplant recipient. Transpl Infect Dis 2007; 9:126-31.
18. Lalezari JP, Drew WL, Glutzer E, et al. Treatment with intravenous (S)-1-[3-hydroxy-2-(phosphonylmethoxy)propyl]-cytosine of acyclovir- resistant mucocutaneous infection with herpes simplex virus in a patient with AIDS. J Infect Dis 1994; 170:570-2.
19. Snoeck R, Andrei G, Gerard M, et al. Successful treatment of progressive mucocutaneous infection due to acyclovir- and foscarnet-resistant herpes simplex virus with (S)-1-(3-hydroxy-2-phosphonylmethoxypropyl) cytosine (HPMPC). Clin Infect Dis 1994; 18:570-8.
20. Chen Y, Scieux C, Garrait V, et al. Resistant herpes simplex virus type 1 infection: an emerging concern after allogeneic stem cell transplantation. Clin Infect Dis 2000; 31:927-35.
21. Chakrabarti S, Pillay D, Ratcliffe D, Cane PA, Collingham KE, Milligan DW. Resistance to antiviral drugs in herpes simplex virus infections among allogeneic stem cell transplant recipients: risk factors and prognostic significance. J Infect Dis 2000; 181:2055-8.
22. Sellar RS, Peggs KS. Management of multidrug-resistant viruses in the immunocompromised host. Br J Haematol 2012; 156:559-72.
23. Andrei G, Balzarini J, Fiten P, De Clercq E, Opdenakker G, Snoeck R. Characterization of herpes simplex virus type 1 thymidine kinase mutants selected under a single round of high-dose brivudin. J Virol 2005; 79:5863-9.
24. Andrei G, Topalis D, Fiten P, et al. In vitro-selected drug-resistant varicella- zoster virus mutants in the thymidine kinase and DNA polymerase genes yield novel phenotype-genotype associations and highlight differences between antiherpesvirus drugs. J Virol 2012; 86:2641-52.
25. Nugier F, Colin JN, Aymard M, Langlois M. Occurrence and characterization of acyclovir-resistant herpes simplex virus isolates: report on a two-year sensitivity screening survey. J Med Virol 1992; 36:1-12.
26. Kussmann-Gerber S, Kuonen O, Folkers G, Pilger BD, Scapozza L. Drug resistance of herpes simplex virus type 1-structural considerations at the molecular level of the thymidine kinase. Eur J Biochem 1998; 255:472-81.
27. Likar Y, Dobrenkov K, Olszewska M, et al. PET imaging of HSV1-tk mutants with acquired specificity toward pyrimidine- and acycloguanosine- based radiotracers. Eur J Nucl Med Mol Imaging 2009; 36:1273-82.
28. Liu S, Knafels JD, Chang JS, et al. Crystal structure of the herpes simplex virus 1 DNA polymerase. J Biol Chem 2006; 281:18193-200.
29. Sarisky RT, Quail MR, Clark PE, et al. Characterization of herpes simplex viruses selected in culture for resistance to penciclovir or acyclovir. J Virol 2001; 75:1761-9.
30. Morfin F, Thouvenot D, Aymard M, Souillet G. Reactivation of acyclovir-resistant thymidine kinase-deficient herpes simplex virus harbouring single base insertion within a 7 Gs homopolymer repeat of the thymidine kinase gene. J Med Virol 2000; 62:247-50.
31. Szpara ML, Tafuri YR, Parsons L, et al. A wide extent of inter-strain diversity in virulent and vaccine strains of alphaherpesviruses. PLoS Pathog 2011; 7:e1002282.
32. Evans KG, Morrissey KA, Goldstein SC, Vittorio CC, Rook AH, Kim EJ. Chronic acyclovir-resistant HSV-2 ulcer in an immunosuppressed patient treated with topical cidofovir. Arch Dermatol 2011; 147: 1462-3.
33. Muluneh B, Dean A, Armistead P, Khan T. Successful clearance of cutaneous acyclovir-resistant, foscarnet-refractory herpes virus lesions with topical cidofovir in an allogeneic hematopoietic stem cell transplant patient. J Oncol Pharm Pract 2012; doi: 10.1177/1078155212448408.
34. Snoeck R, Andrei G, De Clercq E, et al. A new topical treatment for resistant herpes simplex infections. N Engl J Med 1993; 329:968-9.
35. LoPresti AE, Levine JF, Munk GB, Tai CY, Mendel DB. Successful treatment of an acyclovir- and foscarnet-resistant herpes simplex virus type 1 lesion with intravenous cidofovir. Clin Infect Dis 1998; 26: 512-3.
36. Saint-Leger E, Fillet AM, Malvy D, Rabanel B, Caumes E. Efficacy of cidofovir in an HIV infected patient with an acyclovir and foscarnet resistant herpes simplex virus infection. Ann Dermatol Venereol 2001; 128:747-9.
37. Castelo-Soccio L, Bernardin R, Stern J, Goldstein SA, Kovarik C. Successful treatment of acyclovir-resistant herpes simplex virus with intralesional cidofovir. Arch Dermatol 2010; 146:124-6.
38. Lalezari J, Schacker T, Feinberg J, et al. A randomized, double-blind, placebo-controlled trial of cidofovir gel for the treatment of acyclovirunresponsive mucocutaneous herpes simplex virus infection in patients with AIDS. J Infect Dis 1997; 176:892-8.
39. Sims CR, Thompson K, Chemaly RF, Shpall EJ, Champlin RE, Safdar A. Oral topical cidofovir: novel route of drug delivery in a severely immunosuppressed patient with refractory multidrug-resistant herpes simplex virus infection. Transpl Infect Dis 2007; 9:256-9.
40. Hirokawa D, Woldow A, Lee SN, Samie F. Treatment of recalcitrant herpes simplex virus with topical imiquimod. Cutis 2011; 88:276-7.
41. Hostetler KY. Alkoxyalkyl prodrugs of acyclic nucleoside phosphonates enhance oral antiviral activity and reduce toxicity: current state of the art. Antiviral Res 2009; 82:A84-98.
42. Krecmerova M, Holy A, Piskala A, et al. Antiviral activity of triazine analogues of 1-(S)-[3-hydroxy-2-(phosphonomethoxy)propyl]cytosine (cidofovir) and related compounds. J Med Chem 2007; 50:1069-77.
43. Chono K, Katsumata K, Kontani T, et al. ASP2151, a novel helicaseprimase inhibitor, possesses antiviral activity against varicella-zoster virus and herpes simplex virus types 1 and 2. J Antimicrob Chemother 2010; 65:1733-41.
44. Tyring S, Wald A, Zadeikis N, Dhadda S, Takenouchi K, Rorig R. ASP2151 for the treatment of genital herpes: a randomized, doubleblind, placebo- and valacyclovir-controlled, dose-finding study. J Infect Dis 2012; 205:1100-10.
45. Sancho-Shimizu V, Perez dD, Lorenzo L, et al. Herpes simplex encephalitis in children with autosomal recessive and dominant TRIF deficiency. J Clin Invest 2011; 121:4889-902.
46. Liu T, Khanna KM, Chen X, Fink DJ, Hendricks RL. CD8(+) T cells can block herpes simplex virus type 1 (HSV-1) reactivation from latency in sensory neurons. J Exp Med 2000; 191:1459-66.
47. Zaia J, Baden L, Boeckh MJ, et al. Viral disease prevention after hematopoietic cell transplantation. Bone Marrow Transplant 2009; 44:471-82.
48. Stranska R, Schuurman R, Nienhuis E, et al. Survey of acyclovirresistant herpes simplex virus in the Netherlands: prevalence and characterization. J Clin Virol 2005; 32:7-18.
49. Williamson EC, Millar MR, Steward CG, et al. Infections in adults undergoing unrelated donor bone marrow transplantation. Br J Haematol 1999; 104:560-8.
50. Duan R, de Vries RD, van Dun JM, et al. Acyclovir susceptibility and genetic characteristics of sequential herpes simplex virus type 1 corneal isolates from patients with recurrent herpetic keratitis. J Infect Dis 2009; 200:1402-14.