Novel natural mutations in the Hepatitis B Virus reverse transcriptase domain associated with hepatocellular carcinoma

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Wu, Yan ^a   Gan, Yu ^a   Gao, Fumin ^a,b   Zhao, Zhimei ^a   Jin, Yan ^a   Zhu, Yu ^a   Sun, Zhihan ^b   Wu, Hao ^b   Chen, Taoyang ^c   Wang, Jinbing ^c   Sun, Yan ^c   Fan, Chunsun ^c   Xiang, Yongbing ^a   Qian, Gengsun ^a   Groopman, John D ^d   Gu, Jianren ^a   Tu, Hong ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b FUDAN UNIVERSITY   (China)

^c QIDONG LIVER CANCER INSTITUTE   (China)

^d JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA DIRECTED DNA POLYMERASE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CANCER RISK; CONTROLLED STUDY; FEMALE; GENE MUTATION; GENETIC ASSOCIATION; HEPATITIS B VIRUS; HUMAN; LIVER CELL CARCINOMA; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN DOMAIN; RISK ASSESSMENT; RISK FACTOR; UNINDEXED SEQUENCE; ADULT; ALLELE; CARCINOMA, HEPATOCELLULAR; CASE CONTROL STUDY; COMPLICATION; GENETICS; HEPATITIS B; LIVER NEOPLASMS; MIDDLE AGED; MUTATION RATE; REPRODUCIBILITY; RISK; VIROLOGY; VIRUS LOAD;

ADULT; ALLELES; AMINO ACID SUBSTITUTION; CARCINOMA, HEPATOCELLULAR; CASE-CONTROL STUDIES; FEMALE; HEPATITIS B; HEPATITIS B VIRUS; HUMANS; LIVER NEOPLASMS; MALE; MIDDLE AGED; MUTATION RATE; ODDS RATIO; REPRODUCIBILITY OF RESULTS; RISK FACTORS; RNA-DIRECTED DNA POLYMERASE; VIRAL LOAD;

EID: 84900426494     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0094864     Document Type: Article

References (54)

1. (2009) Hepatitis B vaccines. Wkly Epidemiol Rec 84: 405-419.
2. Locarnini S (2004) Molecular virology of hepatitis B virus. Semin Liver Dis 24 Suppl 1: 3-10.
3. Nowak MA, Bonhoeffer S, Hill AM, Boehme R, Thomas HC, et al. (1996) Viral dynamics in hepatitis B virus infection. Proc Natl Acad Sci U S A 93: 4398-4402. (Pubitemid 26144299)
4. Liu S, Zhang H, Gu C, Yin J, He Y, et al. (2009) Associations between hepatitis B virus mutations and the risk of hepatocellular carcinoma: a meta-analysis. J Natl Cancer Inst 101: 1066-1082.
5. Zhu Y, Jin Y, Guo X, Bai X, Chen TY, et al. (2010) Comparison Study on the Complete Sequence of Hepatitis B Virus Identifies New Mutations in Core Gene Associated with Hepatocellular Carcinoma. Cancer Epidemiol Biomarkers Prev 19: 2623-2630.
6. Tong MJ, Blatt LM, Kao JH, Cheng JT, Corey WG (2007) Basal core promoter T1762/A1764 and precore A1896 gene mutations in hepatitis B surface antigen-positive hepatocellular carcinoma: a comparison with chronic carriers. Liver Int 27: 1356-1363. (Pubitemid 350142249)
7. Chen CH, Changchien CS, Lee CM, Hung CH, Hu TH, et al. (2008) Combined mutations in pre-s/surface and core promoter/precore regions of hepatitis B virus increase the risk of hepatocellular carcinoma: a case-control study. J Infect Dis 198: 1634-1642.
8. Chen BF, Liu CJ, Jow GM, Chen PJ, Kao JH, et al. (2006) High prevalence and mapping of pre-S deletion in hepatitis B virus carriers with progressive liver diseases. Gastroenterology 130: 1153-1168.
9. Qu L, Kuai X, Liu T, Chen T, Ni Z, et al. (2013) Pre-S deletion and complex mutations of hepatitis B virus related to young age hepatocellular carcinoma in Qidong, China. PLoS One 8: e59583.
10. Kohlstaedt LA, Wang J, Friedman JM, Rice PA, Steitz TA (1992) Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256: 1783-1790.
11. Ghany M, Liang TJ (2007) Drug targets and molecular mechanisms of drug resistance in chronic hepatitis B. Gastroenterology 132: 1574-1585. (Pubitemid 46627588)
12. Lok AS, Zoulim F, Locarnini S, Bartholomeusz A, Ghany MG, et al. (2007) Antiviral drug-resistant HBV: standardization of nomenclature and assays and recommendations for management. Hepatology 46: 254-265. (Pubitemid 47171942)
13. Zoulim F, Locarnini S (2009) Hepatitis B virus resistance to nucleos(t)ide analogues. Gastroenterology 137: 1593-1608 e1591-1592.
14. Liaw YF (2013) Impact of therapy on the outcome of chronic hepatitis B. Liver Int 33 Suppl 1: 111-115.
15. Hosaka T, Suzuki F, Kobayashi M, Seko Y, Kawamura Y, et al. (2013) Long-term entecavir treatment reduces hepatocellular carcinoma incidence in patients with hepatitis B virus infection. Hepatology 58: 98-107.
16. Chen JG, Zhang SW (2011) Liver cancer epidemic in China: past, present and future. Semin Cancer Biol 21: 59-69.
17. Chen JG, Lu JH, Zhu YR, Zhu J, Zhang YH (2010) [A thirty-one year prospective follow-up program on the HBsAg carrier state and primary liver cancer in Qidong, China]. Zhonghua Liu Xing Bing Xue Za Zhi 31: 721-726.
18. Jin Y, Zhu Y, Chen TY, Guo X, Zhang J, et al. (2010) The association of hepatitis B virus genotype and the basal core promoter mutation in Qidong, China. Zhonghua Gan Zang Bing Za Zhi 18: 511-515.
19. Cao ZG, Bai X, Guo X, Jin Y, Qian GS, et al. (2008) High prevalence of hepatitis B virus pre-S mutation and its association with hepatocellular carcinoma in Qidong, China. Arch Virol 153: 1807-1812.
20. Bai X, Zhu Y, Jin Y, Guo X, Qian G, et al. (2011) Temporal acquisition of sequential mutations in the enhancer II and basal core promoter of HBV in individuals at high risk for hepatocellular carcinoma. Carcinogenesis 32: 63-68.
21. Guo X, Jin Y, Qian GS, Tu H (2008) Sequential accumulation of the mutations in core promoter of hepatitis B virus is associated with the development of hepatocellular carcinoma in Qidong, China. J Hepatol 49: 718-725.
22. Sun Y, Chen TY, Lu PX, Wang JB, Wu Y, et al. (2011) A seventeen-year prospective cohort study on association of hepatitis B virus e antigen with the risk of hepatocellular carcinoma. Tumor 31: 841-845.
23. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599. (Pubitemid 47236692)
24. Keeffe EB, Dieterich DT, Pawlotsky JM, Benhamou Y (2008) Chronic hepatitis B: preventing, detecting, and managing viral resistance. Clin Gastroenterol Hepatol 6: 268-274. (Pubitemid 351324881)
25. Kramvis A, Arakawa K, Yu MC, Nogueira R, Stram DO, et al. (2008) Relationship of serological subtype, basic core promoter and precore mutations to genotypes/subgenotypes of hepatitis B virus. J Med Virol 80: 27-46. (Pubitemid 350220086)
26. Wang YX, Xu X, Luo C, Ma ZM, Jiang HL, et al. (2007) A putative new domain target for anti-hepatitis B virus: residues flanking hepatitis B virus reverse transcriptase residue 306 (rtP306). J Med Virol 79: 676-682. (Pubitemid 46709361)
27. Kuang SY, Jackson PE, Wang JB, Lu PX, Munoz A, et al. (2004) Specific mutations of hepatitis B virus in plasma predict liver cancer development. Pro Nat Acad Sci U S A 101: 3575-3580. (Pubitemid 38338237)
28. Chen CH, Hung CH, Lee CM, Hu TH, Wang JH, et al. (2007) Pre-S deletion and complex mutations of hepatitis B virus related to advanced liver disease in HBeAg-Negative patients. Gastroenterology 133: 1466-1474. (Pubitemid 350029756)
29. Arbuthnot P, Kew M (2001) Hepatitis B virus and hepatocellular carcinoma. Int J Exp Pathol 82: 77-100. (Pubitemid 32681936)
30. Yuan JM, Ambinder A, Fan Y, Gao YT, Yu MC, et al. (2009) Prospective evaluation of hepatitis B 1762(T)/1764(A) mutations on hepatocellular carcinoma development in Shanghai, China. Cancer Epidemiol Biomarkers Prev 18: 590-594.
31. Fang ZL, Sabin CA, Dong BQ, Ge LY, Wei SC, et al. (2008) HBV A1762T, G1764A mutations are a valuable biomarker for identifying a subset of male HBsAg carriers at extremely high risk of hepatocellular carcinoma: a prospective study. Am J Gastroenterol 103: 2254-2262.
32. Tsai WL, Chung RT (2010) Viral hepatocarcinogenesis. Oncogene 29: 2309-2324.
33. McMahon BJ (2009) The natural history of chronic hepatitis B virus infection. Hepatology 49: S45-55.
34. Yuen MF, Tanaka Y, Shinkai N, Poon RT, But DY, et al. (2008) Risk for hepatocellular carcinoma with respect to hepatitis B virus genotypes B/C, specific mutations of enhancer II/core promoter/precore regions and HBV DNA levels. Gut 57: 98-102.
35. Akarsu M, Sengonul A, Tankurt E, Sayiner AA, Topalak O, et al. (2006) YMDD motif variants in inactive hepatitis B carriers detected by Inno-Lipa HBV DR assay. J Gastroenterol Hepatol 21: 1783-1788. (Pubitemid 44656997)
36. Ramezani A, Velayati AA, Roshan MR, Gachkar L, Banifazl M, et al. (2008) Rate of YMDD motif mutants in lamivudine-untreated Iranian patients with chronic hepatitis B virus infection. Int J Infect Dis 12: 252-255. (Pubitemid 351539097)
37. Tan Y, Ding K, Su J, Trinh X, Peng Z, et al. (2012) The naturally occurring YMDD mutation among patients chronically infected HBV and untreated with lamivudine: a systematic review and meta-analysis. PLoS One 7: 1-9.
38. Tauseef I, Iqbal F, Rehman W, Ali M, Qureshi JA, et al. (2012) A PCR-RFLP based protocol for the detection of hepatitis B virus variants in some lamivudine-untreated chronic hepatitis B virus carriers in Pakistan. Pak J Pharm Sci 25: 349-352.
39. Lin X, Ma ZM, Yao X, He LF, Yuan ZH, et al. (2005) Substitution of proline 306 in the reverse transcriptase domain of hepatitis B virus regulates replication. J Gen Virol 86: 85-90. (Pubitemid 40081153)
40. Lin X, Yuan ZH, Wu L, Ding JP, Wen YM (2001) A single amino acid in the reverse transcriptase domain of hepatitis B virus affects virus replication efficiency. J Virol 75: 11827-11833. (Pubitemid 33063274)
41. Wang YX, Xu X, Luo C, Ma ZM, Jiang HL, et al. (2007) Mutational analysis revealed that conservation of hepatitis B virus reverse transcriptase residue 306 (rtP306) is crucial for encapsidation of pregenomic RNA. FEBS Lett 581: 558-564. (Pubitemid 46157229)
42. Jang ES, Jeong SH, Lee SH, Hwang SH, Ahn SY, et al. (2013) The effect of coffee consumption on the development of hepatocellular carcinoma in hepatitis B virus endemic area. Liver Int 33: 1092-1099.
43. Chen CJ, Yang HI, Su J, Jen CL, You SL, et al. (2006) Risk of hepatocellular carcinoma across a biological gradient of serum hepatitis B virus DNA level. JAMA 295: 65-73. (Pubitemid 43042691)
44. Chan HL, Tse CH, Mo F, Koh J, Wong VW, et al. (2008) High viral load and hepatitis B virus subgenotype ce are associated with increased risk of hepatocellular carcinoma. J Clin Oncol 26: 177-182.
45. Xu J, Lin Y, Wang YP, Chen YX, Shi B, et al. (2009) Hepatitis B virus DNA in patients with hepatitis B-related liver cirrhosis with or without hepatocellular carcinomas: a matched case-control study. J Dig Dis 10: 138-144.
46. Zhou JY, Zhang L, Li L, Gu GY, Zhou YH, et al. (2012) High hepatitis B virus load is associated with hepatocellular carcinomas development in Chinese chronic hepatitis B patients: a case control study. Virol J 9: 16.
47. Liu TT, Fang Y, Xiong H, Chen TY, Ni ZP, et al. (2008) A case-control study of the relationship between hepatitis B virus DNA level and risk of hepatocellular carcinoma in Qidong, China. World J Gastroenterol 14: 3059-3063.
48. Sun Y, Chen TY, Lu PX, Wang JB, Wu Y, et al. (2012) [Relationship between serum hepatitis B virus DNA load and hepatocellular carcinoma in Qidong, China: a cohort follow-up study of 14 years]. Zhonghua Yi Xue Za Zhi 92: 1874-1877.
49. Yu MW, Yeh SH, Chen PJ, Liaw YF, Lin CL, et al. (2005) Hepatitis B virus genotype and DNA level and hepatocellular carcinoma: a prospective study in men. J Natl Cancer Inst 97: 265-272.
50. Moolla N, Kew M, Arbuthnot P (2002) Regulatory elements of hepatitis B virus transcription. J Viral Hepat 9: 323-331.
51. Guo WT, Bell KD, Ou JH (1991) Characterization of the hepatitis B virus EnhI enhancer and X promoter complex. J Virol 65: 6686-6692.
52. Fukai K, Takada S, Yokosuka O, Saisho H, Omata M, et al. (1997) Characterization of a specific region in the hepatitis B virus enhancer I for the efficient expression of X gene in the hepatic cell. Virology 236: 279-287. (Pubitemid 27423770)
53. Motavaf M, Safari S, Saffari Jourshari M, Alavian SM (2013) Hepatitis B virus-induced hepatocellular carcinoma: the role of the virus x protein. Acta Virol 57: 389-396.
54. Liaw YF, Tai DI, Chen TJ, Chu CM, Huang MJ (1986) Alpha-fetoprotein changes in the course of chronic hepatitis: relation to bridging hepatic necrosis and hepatocellular carcinoma. Liver 6: 133-137. (Pubitemid 17184758)