Cross-resistance testing of antihepadnaviral compounds using novel recombinant baculoviruses which encode drug-resistant strains of hepatitis B virus

Antimicrobial Agents and Chemotherapy

Volumn 45, Issue 6, 2001, Pages 1705-1713

  Delaney IV, William E ^a,d   Edwards, Ros ^a   Colledge, Danni ^a   Shaw, Tim ^a   Torresi, Joseph ^a   Miller, Thomas G ^b   Isom, Harriet C ^b   Bock, C Thomas ^c   Manns, Michael P ^c   Trautwein, Christian ^c   Locarnini, Stephen ^a  

^a VICTORIAN INFECTIOUS DISEASES REFERENCE LABORATORY   (Australia)

^b PENN STATE COLLEGE OF MEDICINE   (United States)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d GILEAD SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADEFOVIR; ANTIVIRUS AGENT; FAMCICLOVIR; LAMIVUDINE; PENCICLOVIR;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; BACULOVIRUS; BIOAVAILABILITY; CROSS RESISTANCE; DRUG EFFECT; ENZYME PHOSPHORYLATION; HEPATITIS B VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STRAIN DIFFERENCE; VIRUS INFECTION; VIRUS PARTICLE; VIRUS REPLICATION; VIRUS RESISTANCE; VIRUS STRAIN;

2-AMINOPURINE; ANTIVIRAL AGENTS; BACULOVIRIDAE; CELLS, CULTURED; DNA, VIRAL; DRUG RESISTANCE, MICROBIAL; GENOME, VIRAL; HEPADNAVIRIDAE; HEPATITIS B VIRUS; LAMIVUDINE; MICROBIAL SENSITIVITY TESTS; MUTAGENESIS;

EID: 0035018490     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.45.6.1705-1713.2001     Document Type: Article

References (74)

1. Allen, I. M., M. Deslauriers, C. W. Andrews, G. A. Tipples, K. A. Walters, D. L. Tyrrell, N. Brown, and L. D. Condreay. 1998. Identification and characterization of mutations in hepatitis B virus resistant to lamivudine. Hepatology 27:1670-1677.
2. Aye, T. T., A. Bartholomeusz, T. Shaw, S. Bowden, A. Breschkin, J. McMillan, P. Angus, and S. Locarnini. 1997. Hepatitis B virus polymerase mutations during antiviral therapy in a patient following liver transplantation. J. Hepatol. 26:1148-1153.
3. Bartholomeusz, A., L. C. Groenen, and S. A. Locarnini. 1997. Clinical experience with famciclovir against hepatitis B virus. Intervirology 40:337-342.
4. Bartholomew, M. M., R. W. Jansen, L. J. Jeffers, K. R. Reddy, L. C. Johnson, H. Bunzendahl, L. D. Condreay, A. G. Tzakis, E. R. Schiff, and N. A. Brown. 1997. Hepatitis-B-virus resistance to lamivudine given for recurrent infection after orthotopic liver transplantation. Lancet 349:20-22.
5. Beasley, R. P., L. Y. Hwang, C. C. Lin, and C. S. Chien. 1981. Hepatocellular carcinoma and hepatitis B virus. A prospective study of 22,707 men in Taiwan. Lancet ii:1129-1133.
6. Bock, C., N. P. Malek, H. L. Tillmann, M. P. Manns, and C. Trautwein. 2000. The enhancer I core region contributes to the replication level of hepatitis B virus in vivo and in vitro. J. Virol. 74:2193-2202.
7. Boyce, F. M., and N. L. Bucher. 1996. Baculovirus-mediated gene transfer into mammalian cells. Proc. Natl. Acad. Sci. USA 93:2348-2352.
8. Coates, J. A., N. Cammack, H. J. Jenkinson, A. J. Jowett, M. I. Jowett, B. A. Pearson, C. R. Penn, P. L. Rouse, K. C. Viner, and J. M. Cameron. 1992. (-)-2′-deoxy-3′-thiacytidine is a potent, highly selective inhibitor of human immunodeficiency virus type 1 and type 2 replication in vitro. Antimicrob. Agents Chemother. 36:733-739.
9. Colacino, J. M., and K. A. Staschke. 1998. The identification and development of antiviral agents for the treatment of chronic hepatitis B virus infection. Prog. Drug Res. 50:259-322.
10. Colledge, D., G. Civitico, S. Locarnini, and T. Shaw. 2000. In vitro antihepadnaviral activities of combinations of penciclovir, lamivudine, and adefovir. Antimicrob. Agents Chemother. 44:551-560.
11. Colledge, D., S. Locarnini, and T. Shaw. 1997. Synergistic inhibition of hepadnaviral replication by lamivudine in combination with penciclovir in vitro. Hepatology 26:216-225.
12. De Clercq, E., A. Holy, I. Rosenberg, T. Sakuma, J. Balzarini, and P. C. Maudgal. 1986. A novel selective broad-spectrum anti-DNA virus agent. Nature 323:464-467.
13. Deeks, S. G., A. Collier, J. Lalezari, A. Pavia, D. Rodrigue, W. L. Drew, J. Toole, H. S. Jaffe, A. S. Mulato, P. D. Lamy, W. Li, J. M. Cherrington, N. Hellmann, and J. Kahn. 1997. The safety and efficacy of adefovir dipivoxil, a novel anti-human immunodeficiency virus (HIV) therapy, in HIV-infected adults: a randomized, double-blind, placebo-controlled trial. J. Infect. Dis. 176:1517-1523.
14. Delaney, W. E., IV, and H. C. Isom. 1998. Hepatitis B virus replication in human HepG2 cells mediated by hepatitis B virus recombinant baculovirus. Hepatology 28:1134-1146.
15. Delaney, W. E., IV, T. G. Miller, and H. C. Isom. 1999. Use of the hepatitis B virus recombinant baculovirus-HepG2 system to study the effects of (-)-β-2′,3′-dideoxy-3′-thiacytidine on replication of hepatitis B virus and accumulation of covalently closed circular DNA. Antimicrob. Agents Chemother. 43:2017-2026.
16. 15a. de Man, R. A., P. Marcellin, F. Habal, P. Desmond, T. Wright, T. Rose, R. Jurewicz, and C. Young. 2000. A randomized, placebo-controlled study to evaluate the efficacy of 12-month famciclovir treatment in patients with chronic hepatitis B e antigen-positive hepatitis B. Hepatology 32:413-417.
17. Dienstag, J. L., E. R. Schiff, T. L. Wright, R. P. Perrillo, H. W. Hann, Z. Goodman, L. Crowther, L. D. Condreay, M. Woessner, M. Rubin, and N. A. Brown. 1999. Lamivudine as initial treatment for chronic hepatitis B in the United States. N. Engl. J. Med. 341:1256-1263.
18. Doong, S. L., C. H. Tsai, R. F. Schinazi, D. C. Liotta, and Y. C. Cheng. 1991. Inhibition of the replication of hepatitis B virus in vitro by 2′,3′-dideoxy-3′-thiacytidine and related analogues. Proc. Natl. Acad. Sci. USA 88:8495-8499.
19. Fu, L., S. H. Liu, and Y. C. Cheng. 1999. Sensitivity of L-(-)2,3-dideoxythiacytidine resistant hepatitis B virus to other antiviral nucleoside analogues. Biochem. Pharmacol. 57:1351-1359.
20. Gilson, R. J., K. B. Chopra, A. M. Newell, I. M. Murray-Lyon, M. R. Nelson, S. J. Rice, R. S. Tedder, J. Toole, H. S. Jaffe, and I. V. Weller. 1999. A placebo-controlled phase I/II study of adefovir dipivoxil in patients with chronic hepatitis B virus infection. J. Viral Hepatitis 6:387-395.
21. Guidotti, L. G., B. Matzke, H. Schaller, and F. V. Chisari. 1995. High-level hepatitis B virus replication in transgenic mice. J. Virol. 69:6158-6169.
22. Heijtink, R. A., G. A. De Wilde, J. Kruining, L. Berk, J. Balzarini, E. De Clercq, A. Holy, and S. W. Schalm. 1993. Inhibitory effect of 9-(2-phosphonylmethoxyethyl)-adenine (PMEA) on human and duck hepatitis B virus infection. Antivir. Res. 21:141-153.
23. Hirsch, R., R. Colgrove, and D. Ganem. 1988. Replication of duck hepatitis B virus in two differentiated human hepatoma cell lines after transfection with cloned viral DNA. Virology 167:136-142.
24. Honkoop, P., H. G. Niesters, R. A. de Man, A. D. Osterhaus, and S. W. Schalm. 1997. Lamivudine resistance in immunocompetent chronic hepatitis B. Incidence and patterns. J. Hepatol. 26:1393-1395.
25. Hussain, M., and A. S. Lok. 1999. Mutations in the hepatitis B virus polymerase gene associated with antiviral treatment for hepatitis B. J. Viral Hepatitis 6:183-194.
26. Jarvis, B., and D. Faulds. 1999. Lamivudine. A review of its therapeutic potential in chronic hepatitis B. Drugs 58:101-141.
27. Kahn, J., S. Lagakos, M. Wulfsohn, D. Cherng, M. Miller, J. Cherrington, D. Hardy, G. Beall, R. Cooper, R. Murphy, N. Basgoz, E. Ng, S. Deeks, D. Winslow, J. J. Toole, and D. Coakley. 1999. Efficacy and safety of adefovir dipivoxil with antiretroviral therapy: a randomized controlled trial. JAMA 282:2305-2312.
28. Korba, B. E., and M. R. Boyd. 1996. Penciclovir is a selective inhibitor of hepatitis B virus replication in cultured human hepatoblastoma cells. Antimicrob. Agents Chemother. 40:1282-1284.
29. Korba, B. E., P. Cote, W. Hornbuckle, R. Schinazi, J. L. Gerin, and B. C. Tennant. 2000. Enhanced antiviral benefit of combination therapy with lamivudine and famciclovir against WHV replication in chronic WHV carrier woodchucks. Antivir. Res. 45:19-32.
30. Ladner, S. K., T. J. Miller, and R. W. King. 1998. The M539V polymerase variant of human hepatitis B virus demonstrates resistance to 2′-deoxy-3′-thiacytidine and a reduced ability to synthesize viral DNA. Antimicrob. Agents Chemother. 42:2128-2131.
31. Ladner, S. K., T. J. Miller, M. J. Otto, and R. W. King. 1998. The hepatitis B virus M539V polymerase variation responsible for 3TC resistance also confers cross-resistance to other nucleoside analogues. Antivir. Chem. Chemother. 9:65-72.
32. Lai, C. L., R. N. Chien, N. W. Leung, T. T. Chang, R. Guan, D. I. Tai, K. Y. Ng, P. C. Wu, J. C. Dent, J. Barber, S. L. Stephenson, and D. F. Gray. 1998. A one-year trial of lamivudine for chronic hepatitis B. N. Engl. J. Med. 339:61-68.
33. Liaw, Y. F., R. N. Chien, C. T. Yeh, S. L. Tsai, and C. M. Chu. 1999. Acute exacerbation and hepatitis B virus clearance after emergence of YMDD motif mutation during lamivudine therapy. Hepatology 30:567-572.
34. Ling, R., D. Mutimer, M. Ahmed, E. H. Boxall, E. Elias, G. M. Dusheiko, and T. J. Harrison. 1996. Selection of mutations in the hepatitis B virus polymerase during therapy of transplant recipients with lamivudine. Hepatology 24:711-713.
35. Locarnini, S. A. 1998. Hepatitis B virus surface antigen and polymerase gene variants: potential virological and clinical significance. Hepatology 27:294-297.
36. Lok, A. S. 2000. Hepatitis B infection: pathogenesis and management. J. Hepatol. 32:89-97.
37. Main, J., J. L. Brown, C. Howells, R. Galassini, M. Crossey, P. Karayiannis, F. Georgiou, G. Atkinson, and H. C. Thomas. 1996. A double blind, placebo-controlled study to assess the effect of famciclovir on virus replication in patients with chronic hepatitis B virus infection. J. Viral Hepatitis 3:211-215.
38. Mason, W. S., J. Cullen, G. Moraleda, J. Saputelli, C. E. Aldrich, D. S. Miller, B. Tennant, L. Frick, D. Averett, L. D. Condreay, and A. R. Jilbert. 1998. Lamivudine therapy of WHV-infected woodchucks. Virology 245:18-32.
39. Melegari, M., P. P. Scaglioni, and J. R. Wands. 1998. Hepatitis B virus mutants associated with 3TC and famciclovir administration are replication defective. Hepatology 27:628-633.
40. Miller, M. D., K. E. Anton, A. S. Mulato, P. D. Lamy, and J. M. Cherrington. 1999. Human immunodeficiency virus type 1 expressing the lamivudine-associated M184V mutation in reverse transcriptase shows increased susceptibility to adefovir and decreased replication capability in vitro. J. Infect. Dis. 179:92-100.
41. Moraleda, G., J. Saputelli, C. E. Aldrich, D. Averett, L. Condreay, and W. S. Mason. 1997. Lack of effect of antiviral therapy in nondividing hepatocyte cultures on the closed circular DNA of woodchuck hepatitis virus. J. Virol. 71:9392-9399.
42. Mutimer, D., D. Pillay, P. Cook, D. Ratcliffe, K. O'Donnell, D. Dowling, J. Shaw, E. Elias, and P. A. Cane. 2000. Selection of multiresistant hepatitis B virus during sequential nucleoside-analogue therapy. J. Infect. Dis. 181:713-716.
43. Nassal, M., and H. Schaller. 1996. Hepatitis B virus replication - an update. J. Viral Hepatitis 3:217-226.
44. Nevens, F., J. Main, P. Honkoop, D. L. Tyrrell, J. Barber, M. T. Sullivan, J. Fevery, R. A. De Man, and H. C. Thomas. 1997. Lamivudine therapy for chronic hepatitis B: a six-month randomized dose-ranging study. Gastroenterology 113:1258-1263.
45. Newbold, J. E., H. Xin, M. Tencza, G. Sherman, J. Dean, S. Bowden, and S. Locarnini. 1995. The covalently closed duplex form of the hepadnavirus genome exists in situ as a heterogeneous population of viral minichromosomes. J. Virol. 69:3350-3357.
46. Nicoll, A. J., D. L. Colledge, J. J. Toole, P. W. Angus, R. A. Smallwood, and S. A. Locarnini. 1998. Inhibition of duck hepatitis B virus replication by 9-(2-phosphonylmethoxyethyl)adenine, an acyclic phosphonate nucleoside analogue. Antimicrob. Agents Chemother. 42:3130-3135.
47. Niederau, C., T. Heintges, S. Lange, G. Goldmann, C. M. Niederau, L. Mohr, and D. Haussinger. 1996. Long-term follow-up of HBeAg-positive patients treated with interferon alfa for chronic hepatitis B. N. Engl. J. Med. 334: 1422-1427.
48. Omata, M., K. Hirota, and O. Yokosuka. 1986. In vivo study of the mechanism of action of antiviral agents against hepadna virus replication in the liver. Resistance of supercoiled viral DNA. J. Hepatol. 3(Suppl. 2):S49-S55.
49. Ono-Nita, S. K., N. Kato, Y. Shiratori, K. H. Lan, H. Yoshida, F. J. Carrilho, and M. Omata. 1999. Susceptibility of lamivudine-resistant hepatitis B virus to other reverse transcriptase inhibitors. J. Clin. Investig. 103:1635-1640.
50. Ono-Nita, S. K., N. Kato, Y. Shiratori, T. Masaki, K. H. Lan, F. J. Carrilho, and M. Omata. 1999. YMDD motif in hepatitis B virus DNA polymerase influences on replication and lamivudine resistance: a study by in vitro full-length viral DNA transfection. Hepatology 29:939-945.
51. O'Reilly, D. R. 1997. Use of baculovirus expression vectors. Methods Mol. Biol. 62:235-246.
52. Perrillo, R., E. Schiff, E. Yoshida, A. Statler, K. Hirsch, T. Wright, K. Gutfreund, P. Lamy, and A. Murray. 2000. Adefovir dipivoxil for the treatment of lamivudine-resistant hepatitis B mutants. Hepatology 32:129-134.
53. Peters, G. M., G. Singer, T. Howard, S. Jacobsmeyer, X. Xiong, C. S. Gibbs, P. Lamy, and A. Murray. 1999. Fulminant hepatic failure resulting from lamivudine-resistant hepatitis B virus in a renal transplant recipient: durable response after orthotopic liver transplantation on adefovir dipivoxil and hepatitis B immune globulin. Transplantation 68:1912-1914.
54. Pichoud, C., B. Seigneres, Z. Wang, C. Trepo, and F. Zoulim. 1999. Transient selection of a hepatitis B virus polymerase gene mutant associated with a decreased replication capacity and famciclovir resistance. Hepatology 29: 230-237.
55. Rayes, N., D. Seehofer, W. O. Bechstein, A. R. Muller, T. Berg, R. Neuhaus, and P. Neuhaus. 1999. Long-term results of famciclovir for recurrent or de novo hepatitis B virus infection after liver transplantation. Clin. Transplant. 13:447-452.
56. Santantonio, T., M. Mazzola, T. Iacovazzi, A. Miglietta, A. Guastadisegni, and G. Pastore. 2000. Long-term follow-up of patients with anti-HBe/HBV DNA-positive chronic hepatitis B treated for 12 months with lamivudine. J. Hepatol. 32:300-306.
57. Seigneres, B., C. Pichoud, S. S. Ahmed, O. Hantz, C. Trepo, and F. Zoulim. 2000. Evolution of hepatitis B virus polymerase gene sequence during famciclovir therapy for chronic hepatitis B. J. Infect. Dis. 181:1221-1233.
58. Severini, A., X. Y. Liu, J. S. Wilson, and D. L. Tyrrell. 1995. Mechanism of inhibition of duck hepatitis B virus polymerase by (-)-β-L-2′,3′-dideoxy-3′-thiacytidine. Antimicrob. Agents Chemother. 39:1430-1435.
59. Shaw, T., P. Amor, G. Civitico, M. Boyd, and S. Locarnini. 1994. In vitro antiviral activity of penciclovir, a novel purine nucleoside, against duck hepatitis B virus. Antimicrob. Agents Chemother. 38:719-723.
60. Shaw, T., and S. A. Locarnini. 1999. Preclinical aspects of lamivudine and famciclovir against hepatitis B virus. J. Viral Hepatitis 6:89-106.
61. Shaw, T., and S. Locarnini. 2000. Combination chemotherapy for HBV: the path forward? Drugs 60:517-531.
62. Tassopoulos, N. C., R. Volpes, G. Pastore, J. Heathcote, M. Buti, R. D. Goldin, S. Hawley, J. Barber, L. Condreay, and D. F. Gray. 1999. Efficacy of lamivudine in patients with hepatitis B e antigen-negative/hepatitis B virus DNA-positive (precore mutant) chronic hepatitis B. Hepatology 29:889-896.
63. Tillmann, H. L., C. Trautwein, T. Bock, K. H. Boker, E. Jackel, M. Glowienka, K. Oldhafer, I. Bruns, J. Gauthier, L. D. Condreay, H. R. Raab, and M. P. Manns. 1999. Mutational pattern of hepatitis B virus on sequential therapy with famciclovir and lamivudine in patients with hepatitis B virus reinfection occurring under HBIg immunoglobulin after liver transplantation. Hepatology 30:244-256.
64. Tipples, G. A., M. M. Ma, K. P. Fischer, V. G. Bain, N. M. Kneteman, and D. L. Tyrrell. 1996. Mutation in HBV RNA-dependent DNA polymerase confers resistance to lamivudine in vivo. Hepatology 24:714-717.
65. Tuttleman, J. S., C. Pourcel, and J. Summers. 1986. Formation of the pool of covalently closed circular viral DNA in hepadnavirus-infected cells. Cell 47:451-460.
66. Vere Hodge, R. A., D. Sutton, M. R. Boyd, M. R. Harnden, and R. L. Jarvest. 1989. Selection of an oral prodrug (BRL 42810; famciclovir) for the antiherpesvirus agent BRL 39123 [9-(4-hydroxy-3-hydroxymethylbut-l-yl)guanine; penciclovir]. Antimicrob. Agents Chemother. 33:1765-1773.
67. Weinberger, K. M., T. Bauer, S. Bohm, and W. Jilg. 2000. High genetic variability of the group-specific a-determinant of hepatitis B virus surface antigen (HBsAg) and the corresponding fragment of the viral polymerase in chronic virus carriers lacking detectable HBsAg in serum. J. Gen. Virol. 81:1165-1174.
68. Wolters, L. M., P. Honkoop, H. G. Niesters, and R. A. de Man. 1998. Efficacy of famciclovir treatment in chronic hepatitis B patients with different mutations at position 552 of the DNA polymerase gene. J. Hepatol. 28:909-910.
69. Wong, D. K., A. M. Cheung, K. O'Rourke, C. D. Naylor, A. S. Detsky, and J. Heathcote. 1993. Effect of alpha-interferon treatment in patients with hepatitis B e antigen-positive chronic hepatitis B. A meta-analysis. Ann. Intern. Med. 119:312-323.
70. Xiong, X., C. Flores, H. Yang, J. J. Toole, and C. S. Gibbs. 1998. Mutations in hepatitis B DNA polymerase associated with resistance to lamivudine do not confer resistance to adefovir in vitro. Hepatology 28:1669-1673.
71. Xiong, X., H. Yang, C. E. Westland, R. Zou, and C. S. Gibbs. 2000. In vitro evaluation of hepatitis B virus polymerase mutations associated with famciclovir resistance. Hepatology 31:219-224.
72. Yeh, C. T., R. N. Chien, C. M. Chu, and Y. F. Liaw. 2000. Clearance of the original hepatitis B virus YMDD-motif mutants with emergence of distinct lamivudine-resistant mutants during prolonged lamivudine therapy. Hepatology 31:1318-1326.
73. Ying, C., E. De Clercq, W. Nicholson, P. Furman, and J. Neyts. 2000. Inhibition of the replication of the DNA polymerase M550V mutation variant of human hepatitis B virus by adefovir, tenofovir, L-FMAU, DAPD, penciclovir and lobucavir. J. Viral Hepatitis 7:161-165.
74. Yokota, T., S. Mochizuki, K. Konno, S. Mori, S. Shigeta, and E. De Clercq. 1990. Phosphonylmethoxyalkyl derivatives of purine as inhibitors of human hepatitis B virus DNA synthesis. Nucleic Acids Symp. Ser. 22:17-18.