Resistant mutations and quasispecies complexity of hepatitis B virus during telbivudine treatment

Journal of General Virology

Volumn 96, Issue 11, 2015, Pages 3302-3312

  Yin, Feifei ^a   Wu, Zeguang ^b   Fang, Wei ^a   Wu, Chunchen ^a   Rayner, Simon ^a   Han, Meifang ^b   Deng, Fei ^a   Du, Ruikun ^a   Liu, Jinliang ^a   Wang, Manli ^a   Wang, Hualin ^a   Ning, Qin ^b   Hu, Zhihong ^a  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATITIS B(E) ANTIGEN; LAMIVUDINE; RNA DIRECTED DNA POLYMERASE; TELBIVUDINE; VIRUS DNA; ANTIVIRUS AGENT; THYMIDINE;

ARTICLE; BLOOD SAMPLING; CHRONIC HEPATITIS B; CLINICAL ARTICLE; CONTROLLED STUDY; GENE MUTATION; GENETIC VARIABILITY; HEPATITIS B VIRUS; HEPATITIS B VIRUS GENOTYPE C; HUMAN; HUMAN CELL; IN VITRO STUDY; MONOTHERAPY; PRIORITY JOURNAL; PYROSEQUENCING; STEADY STATE; TREATMENT DURATION; TREATMENT RESPONSE; ULTRA DEEP PYROSEQUENCING; VIRUS LOAD; VIRUS REPLICATION; ADOLESCENT; ADULT; AGED; ANALOGS AND DERIVATIVES; ANTIVIRAL RESISTANCE; CLASSIFICATION; CLINICAL TRIAL; DRUG EFFECTS; FEMALE; GENETICS; HEPATITIS B, CHRONIC; ISOLATION AND PURIFICATION; MALE; MIDDLE AGED; MUTATION; VIROLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; AGED; ANTIVIRAL AGENTS; DRUG RESISTANCE, VIRAL; FEMALE; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; HUMANS; MALE; MIDDLE AGED; MUTATION; THYMIDINE; YOUNG ADULT;

EID: 84946882154     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000285     Document Type: Article

References (48)

1. Allen, M. I., Deslauriers, M., Andrews, C. W., Tipples, G. A., Walters, K.-A., Tyrrell, D. L., Brown, N., Condreay, L. D. & Lamivudine Clinical Investigation Group (1998). Identification and characterization of mutations in hepatitis B virus resistant to lamivudine. Hepatology 27, 1670-1677.
2. Cao, L., Wu, C., Shi, H., Gong, Z., Zhang, E., Wang, H., Zhao, K., Liu, S., Li, S. & other authors (2014). Coexistence of hepatitis B virus quasispecies enhances viral replication and the ability to induce host antibody and cellular immune responses. J Virol 88, 8656-8666.
3. Chen, L., Zhang, Q., Yu, D. M., Wan, M. B. & Zhang, X. X. (2009). Early changes of hepatitis B virus quasispecies during lamivudine treatment and the correlation with antiviral efficacy. J Hepatol 50, 895-905.
4. Ciftci, S., Keskin, F., Cakiris, A., Akyuz, F., Pinarbasi, B., Abaci, N., Dincer, E., Badur, S., Kaymakoglu, S. & Ustek, D. (2014). Analysis of potential antiviral resistance mutation profiles within the HBV reverse transcriptase in untreated chronic hepatitis B patients using an ultradeep pyrosequencing method. Diagn Microbiol Infect Dis 79, 25-30.
5. Clavel, F. & Hance, A. J. (2004). HIV drug resistance. N Engl J Med 350, 1023-1035.
6. de la Torre, J. C. & Holland, J. J. (1990). RNA virus quasispecies populations can suppress vastly superior mutant progeny. J Virol 64, 6278-6281.
7. Delaney, W. E. IV, Yang, H., Westland, C. E., Das, K., Arnold, E., Gibbs, C. S., Miller, M. D. & Xiong, S. (2003). The hepatitis B virus polymerase mutation rtV173L is selected during lamivudine therapy and enhances viral replication in vitro. J Virol 77, 11833-11841.
8. Dienstag, J. L. (2008). Hepatitis B virus infection. N Engl J Med 359, 1486-1500.
9. Domingo, E. & Gomez, J. (2007). Quasispecies and its impact on viral hepatitis. Virus Res 127, 131-150.
10. Domingo, E., Escarmis, C., Martinez, M. A., Martinez-Salas, E. & Mateu, M. G. (1992). Foot-and-mouth disease virus populations are quasispecies. Curr Top Microbiol Immunol 176, 33-47.
11. Domingo, E., Martín, V., Perales, C., Grande-Pérez, A., García-Arriaza, J. & Arias, A. (2006). Viruses as quasispecies: biological implications. Curr Top Microbiol Immunol 299, 51-82.
12. Eriksson, N., Pachter, L., Mitsuya, Y., Rhee, S. Y., Wang, C., Gharizadeh, B., Ronaghi, M., Shafer, R. W. & Beerenwinkel, N. (2008). Viral population estimation using pyrosequencing. PLOS Comput Biol 4, e1000074.
13. Fishman, S. L. & Branch, A. D. (2009). The quasispecies nature and biological implications of the hepatitis C virus. Infect Genet Evol 9, 1158-1167.
14. Forns, X., Purcell, R. H. & Bukh, J. (1999). Quasispecies in viral persistence and pathogenesis of hepatitis C virus. Trends Microbiol 7, 402-410.
15. Hedskog, C., Mild, M., Jernberg, J., Sherwood, E., Bratt, G., Leitner, T., Lundeberg, J., Andersson, B. & Albert, J. (2010). Dynamics of HIV-1 quasispecies during antiviral treatment dissected using ultradeep pyrosequencing. PLoS One 5, e11345.
16. Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K. & Pease, L. R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
17. Jiang, L., Shi, J., Liu, Y., Liu, W., Si, L., Zhong, Y. & Xu, D. (2010). Efficient replication and expression of a 1.1-ploid genome length HBV recombinant plasmid vector in Huh7 cells. Med J Chinese People’s Liberation Army 35, 635-638.
18. Kwon, H. & Lok, A. S. (2011). Hepatitis B therapy. Nat Rev Gastroenterol Hepatol 8, 275-284.
19. Lai, C. L., Gane, E., Liaw, Y. F., Hsu, C. W., Thongsawat, S., Wang, Y., Chen, Y., Heathcote, E. J., Rasenack, J. & other authors (2007). Telbivudine versus lamivudine in patients with chronic hepatitis B. N Engl J Med 357, 2576-2588.
20. Lavanchy, D. (2004). Hepatitis B virus epidemiology, disease burden, treatment, and current and emerging prevention and control measures. J Viral Hepat 11, 97-107.
21. Le, T., Chiarella, J., Simen, B. B., Hanczaruk, B., Egholm, M., Landry, M. L., Dieckhaus, K., Rosen, M. I. & Kozal, M. J. (2009). Lowabundance HIV drug-resistant viral variants in treatment-experienced persons correlate with historical antiretroviral use. PLoS One 4, e6079.
22. Ling, R. & Harrison, T. J. (1999). Functional analysis of mutations conferring lamivudine resistance on hepatitis B virus. J Gen Virol 80, 601-606.
23. Liu, F., Chen, L., Yu, D. M., Deng, L., Chen, R., Jiang, Y., Chen, L., Huang, S. Y., Yu, J. L. & other authors (2011). Evolutionary patterns of hepatitis B virus quasispecies under different selective pressures: correlation with antiviral efficacy. Gut 60, 1269-1277.
24. Locarnini, S. (2008). Primary resistance, multidrug resistance, and cross-resistance pathways in HBV as a consequence of treatment failure. Hepatol Int 2, 147-151.
25. Lok, A. S., Zoulim, F., Locarnini, S., Bartholomeusz, A., Ghany, M. G., Pawlotsky, J.-M., Liaw, Y.-F., Mizokami, M., Kuiken, C. & Hepatitis B Virus Drug Resistance Working Group (2007). Antiviral drugresistant HBV: standardization of nomenclature and assays and recommendations for management. Hepatology 46, 254-265.
26. Margeridon-Thermet, S., Shulman, N. S., Ahmed, A., Shahriar, R., Liu, T., Wang, C., Holmes, S. P., Babrzadeh, F., Gharizadeh, B. & other authors (2009). Ultra-deep pyrosequencing of hepatitis B virus quasispecies from nucleoside and nucleotide reversetranscriptase inhibitor (NRTI)-treated patients and NRTI-naive patients. J Infect Dis 199, 1275-1285.
27. Matthews, S. J. (2007). Telbivudine for the management of chronic hepatitis B virus infection. Clin Ther 29, 2635-2653.
28. Nash, K. (2009). Telbivudine in the treatment of chronic hepatitis B. Adv Ther 26, 155-169.
29. Ngui, S. L. & Teo, C. G. (1997). Hepatitis B virus genomic heterogeneity: variation between quasispecies may confound molecular epidemiological analyses of transmission incidents. J Viral Hepat 4, 309-315.
30. Nishijima, N., Marusawa, H., Ueda, Y., Takahashi, K., Nasu, A., Osaki, Y., Kou, T., Yazumi, S., Fujiwara, T. & other authors (2012). Dynamics of hepatitis B virus quasispecies in association with nucleos(t)ide analogue treatment determined by ultra-deep sequencing. PLoS One 7, e35052.
31. Ono, S. K., Kato, N., Shiratori, Y., Kato, J., Goto, T., Schinazi, R. F., Carrilho, F. J. & Omata, M. (2001). The polymerase L528M mutation cooperates with nucleotide binding-site mutations, increasing hepatitis B virus replication and drug resistance. J Clin Invest 107, 449-455.
32. Pallier, C., Castéra, L., Soulier, A., Hézode, C., Nordmann, P., Dhumeaux, D. & Pawlotsky, J.-M. (2006). Dynamics of hepatitis B virus resistance to lamivudine. J Virol 80, 643-653.
33. Ramírez, C., Gregori, J., Buti, M., Tabernero, D., Camoús, S., Casillas, R., Quer, J., Esteban, R., Homs, M. & Rodriguez-Frías, F. (2013). A comparative study of ultra-deep pyrosequencing and cloning to quantitatively analyze the viral quasispecies using hepatitis B virus infection as a model. Antiviral Res 98, 273-283.
34. Rhee, S. Y., Margeridon-Thermet, S., Nguyen, M. H., Liu, T. F., Kagan, R. M., Beggel, B., Verheyen, J., Kaiser, R. & Shafer, R. W. (2010). Hepatitis B virus reverse transcriptase sequence variant database for sequence analysis and mutation discovery. Antiviral Res 88, 269-275.
35. Rodriguez, C., Chevaliez, S., Bensadoun, P. & Pawlotsky, J.-M. (2013). Characterization of the dynamics of hepatitis B virus resistance to adefovir by ultra-deep pyrosequencing. Hepatology 58, 890-901.
36. Schmidt-Martin, D., Crosbie, O., Kenny-Walsh, E. & Fanning, L. J. (2012). Hepatitis C quasispecies adaptation in the setting of a variable fidelity polymerase. Virus Adaptation Treatment 4, 43-50.
37. Sheldon, J. & Soriano, V. (2008). Hepatitis B virus escape mutants induced by antiviral therapy. J Antimicrob Chemother 61, 766-768.
38. Sloan, R. D., Ijaz, S., Moore, P. L., Harrison, T. J., Teo, C.-G. & Tedder, R. S. (2008). Antiviral resistance mutations potentiate hepatitis B virus immune evasion through disruption of its surface antigen a determinant. Antivir Ther 13, 439-447.
39. Solmone, M., Vincenti, D., Prosperi, M. C. F., Bruselles, A., Ippolito, G. & Capobianchi, M. R. (2009). Use of massively parallel ultradeep pyrosequencing to characterize the genetic diversity of hepatitis B virus in drug-resistant and drug-naive patients and to detect minor variants in reverse transcriptase and hepatitis B S antigen. J Virol 83, 1718-1726.
40. Standring, D. N., Seifer, M., Patty, A., Chapron, C., Van Doorn, L. J., Chao, G., Brown, N. & Lai, C. L. (2006). 514 HBV resistance determination from the telbivudine globe registration trial. J Hepatol 44 (Suppl. 2), S191.
41. Stein, L. L. & Loomba, R. (2009). Drug targets in hepatitis B virus infection. Infect Disord Drug Targets 9, 105-116.
42. Steinhauer, D. A., de la Torre, J. C., Meier, E. & Holland, J. J. (1989). Extreme heterogeneity in populations of vesicular stomatitis virus. J Virol 63, 2072-2080,.
43. Sun, J., Xie, Q., Tan, D., Ning, Q., Niu, J., Bai, X., Fan, R., Chen, S., Cheng, J. & other authors (2014). The 104-week efficacy and safety of telbivudine-based optimization strategy in chronic hepatitis B patients: a randomized, controlled study. Hepatology 59, 1283-1292.
44. Tenney, D. J., Levine, S. M., Rose, R. E., Walsh, A. W., Weinheimer, S. P., Discotto, L., Plym, M., Pokornowski, K., Yu, C. F. & other authors (2004). Clinical emergence of entecavir-resistant hepatitis B virus requires additional substitutions in virus already resistant to lamivudine. Antimicrob Agents Chemother 48, 3498-3507.
45. Vignuzzi, M., Stone, J. K., Arnold, J. J., Cameron, C. E. & Andino, R. (2006). Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439, 344-348.
46. Wain-Hobson, S. (1992). Human immunodeficiency virus type 1 quasispecies in vivo and ex vivo. Curr Top Microbiol Immunol 176, 181-193.
47. Warner, N., Locarnini, S., Kuiper, M., Bartholomeusz, A., Ayres, A., Yuen, L. & Shaw, T. (2007). The L80I substitution in the reverse transcriptase domain of the hepatitis B virus polymerase is associated with lamivudine resistance and enhanced viral replication in vitro. Antimicrob Agents Chemother 51, 2285-2292.
48. Zoulim, F. & Locarnini, S. (2009). Hepatitis B virus resistance to nucleos(t)ide analogues. Gastroenterology 137, 1593-1608, e1-e2.