Compartmentalisation of Hepatitis B virus X gene evolution in hepatocellular carcinoma microenvironment and the genotype-phenotype correlation of tumorigenicity in HBV-related patients with hepatocellular carcinoma

References

• Zhang S, Wang F, Zhang Z. Current advances in the elimination of hepatitis B in China by 2030. Front Med. 2017;11(4):490–501.
   PubMed Web of Science ®Google Scholar
• Yuen MF, Chen DS, Dusheiko GM, et al. Hepatitis B virus infection. Nature Reviews Disease Primers. 2018;4:18035.
   PubMed Web of Science ®Google Scholar
• Nicolini LA, Orsi A, Tatarelli P, et al. A global view to HBV chronic infection: evolving strategies for diagnosis, treatment and prevention in immunocompetent individuals. Int J Environ Res Public Health. 2019;16(18).
   PubMed Web of Science ®Google Scholar
• Diao J, Garces R, Richardson CD. X protein of hepatitis B virus modulates cytokine and growth factor related signal transduction pathways during the course of viral infections and hepatocarcinogenesis. Cytokine Growth Factor Rev 2001;12(2-3):189–205.
   PubMed Web of Science ®Google Scholar
• Sartorius K, Swadling L, An P, et al. The multiple roles of hepatitis B virus X protein (HBx) dysregulated MicroRNA in hepatitis B virus-associated hepatocellular carcinoma (HBV-HCC) and immune pathways. Viruses. 2020;12(7).
   PubMed Web of Science ®Google Scholar
• Al-Qahtani AA, Al-Anazi MR, Nazir N, et al. Hepatitis B virus (HBV) X gene mutations and their association with liver disease progression in HBV-infected patients. Oncotarget. 2017;8(62):105115–105125.
   PubMedGoogle Scholar
• Ngui SL, Teo CG. Hepatitis B virus genomic heterogeneity: variation between quasispecies may confound molecular epidemiological analyses of transmission incidents. J Viral Hepat. 1997;4(5):309–315.
   PubMed Web of Science ®Google Scholar
• Wagner J, Yuen L, Littlejohn M, et al. Analysis of hepatitis B virus haplotype diversity detects striking sequence conservation across genotypes and chronic disease phase. Hepatology. 2021;73(5):1652–1670.
   PubMed Web of Science ®Google Scholar
• Domingo E, Gomez J. Quasispecies and its impact on viral hepatitis. Virus Res 2007;127(2):131–150.
   PubMed Web of Science ®Google Scholar
• Xue Y, Wang M-J, Huang S-Y, et al. Characteristics of CpG islands and their quasispecies of full-length hepatitis B virus genomes from patients at different phases of infection. SpringerPlus. 2016;5(1).
   Google Scholar
• Yang Z-T, Huang S-Y, Chen L, et al. Characterization of full-length genomes of hepatitis B virus quasispecies in sera of patients at different phases of infection. J Clin Microbiol. 2015;53(7):2203–2214.
   PubMed Web of Science ®Google Scholar
• Chen L, Zhang Q, Yu D-M, et al. Early changes of hepatitis B virus quasispecies during lamivudine treatment and the correlation with antiviral efficacy. J Hepatol. 2009;50(5):895–905.
   PubMed Web of Science ®Google Scholar
• Liu F, Chen L, Yu DM, et al. Evolutionary patterns of hepatitis B virus quasispecies under different selective pressures: correlation with antiviral efficacy. Gut. 2011;60(9):1269–1277.
   PubMed Web of Science ®Google Scholar
• Zhang AY, Lai CL, Poon RT, et al. Hepatitis B virus full-length genomic mutations and quasispecies in hepatocellular carcinoma. J Gastroenterol Hepatol. 2016;31(9):1638–1645.
   PubMed Web of Science ®Google Scholar
• Yin J, Chen X, Li N, et al. Compartmentalized evolution of hepatitis B virus contributes differently to the prognosis of hepatocellular carcinoma. Carcinogenesis. 2021;42(3):461–470.
   PubMed Web of Science ®Google Scholar
• Tian Q, Jia J. Hepatitis B virus genotypes: epidemiological and clinical relevance in Asia. Hepatol Int. 2016;10(6):854–860.
   PubMed Web of Science ®Google Scholar
• Tong S, Revill P. Overview of hepatitis B viral replication and genetic variability. J Hepatol. 2016;64(1 Suppl):S4–S16.
   PubMedGoogle Scholar
• Yu MW, Yeh SH, Chen PJ, et al. Hepatitis B virus genotype and DNA level and hepatocellular carcinoma: a prospective study in men. JNCI: Journal of the National Cancer Institute. 2005;97(4):265–272.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zeng LI, Chen W. HBV x gene point mutations are associated with the risk of hepatocellular carcinoma: A systematic review and meta-analysis. Mol Clin Oncol. 2016;4(6):1045–1051.
   PubMedGoogle Scholar
• Kim H, Lee SA, Kim BJ. X region mutations of hepatitis B virus related to clinical severity. World J Gastroenterol. 2016;22(24):5467–5478.
   PubMed Web of Science ®Google Scholar
• Tu H, Bonura C, Giannini C, et al. Biological impact of natural COOH-terminal deletions of hepatitis B virus X protein in hepatocellular carcinoma tissues. Cancer Res. 2001 Nov 1;61(21):7803–7810.
   PubMed Web of Science ®Google Scholar
• Shi Y, Wang J, Wang Y, et al. A novel mutant 10Ala/Arg together with mutant 144Ser/Arg of hepatitis B virus X protein involved in hepatitis B virus-related hepatocarcinogenesis in HepG2 cell lines. Cancer Lett. 2016;371(2):285–291.
   PubMed Web of Science ®Google Scholar
• Salpini R, Surdo M, Cortese MF, et al. The novel HBx mutation F30V correlates with hepatocellular carcinoma in vivo, reduces hepatitis B virus replicative efficiency and enhances anti-apoptotic activity of HBx N terminus in vitro. Clin Microbiol Infect. 2019;25(7):906.e1–906.e7.
   PubMed Web of Science ®Google Scholar
• Fu Y, Wu S, Hu Y, et al. Mutational characterization of HBV reverse transcriptase gene and the genotype-phenotype correlation of antiviral resistance among Chinese chronic hepatitis B patients. Emerg Microbes Infect. 2020;9(1):2381–2393.
   PubMed Web of Science ®Google Scholar
• Huang JL, Cao SW, Ou QS, et al. The long non-coding RNA PTTG3P promotes cell growth and metastasis via up-regulating PTTG1 and activating PI3K/AKT signaling in hepatocellular carcinoma. Mol Cancer. 2018;17(1):93.
   PubMedGoogle Scholar
• Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics. 2008;9:40.
   PubMed Web of Science ®Google Scholar
• Wu XY, Qian JJ, Lin Y, et al. Hepatitis B virus X protein disrupts DNA interstrand crosslinking agent mitomycin C induced ATR dependent intra-S-phase checkpoint. Eur J Cancer. 2008;44(11):1596–1602.
   PubMed Web of Science ®Google Scholar
• Lin CL, Kao JH. Natural history of acute and chronic hepatitis B: The role of HBV genotypes and mutants. Best Pract Res Clin Gastroenterol. 2017;31(3):249–255.
   PubMed Web of Science ®Google Scholar
• Lee S, Kim W, Ko C, et al. Hepatitis B virus X protein enhances Myc stability by inhibiting SCFSkp2 ubiquitin E3 ligase-mediated Myc ubiquitination and contributes to oncogenesis. Oncogene. 2016;35(14):1857–1867.
   PubMed Web of Science ®Google Scholar
• Wang J, Chen J, Liu Y, et al. Hepatitis B virus induces autophagy to promote its replication by the axis of miR-192-3p-XIAP through NF kappa B signaling. Hepatology. 2019;69(3):974–992.
   PubMed Web of Science ®Google Scholar
• Tsuchiya H, Amisaki M, Takenaga A, et al. HBx and c-MYC cooperate to induce URI1 expression in HBV-related hepatocellular carcinoma. Int J Mol Sci. 2019;20(22).
   Web of Science ®Google Scholar
• Li B, Zhang G, Wang Z, et al. c-Myc-activated USP2-AS1 suppresses senescence and promotes tumor progression via stabilization of E2F1 mRNA. Cell Death Dis. 2021;12(11):1006.
   PubMed Web of Science ®Google Scholar
• Vohhodina J, Goehring LJ, Liu B, et al. BRCA1 binds TERRA RNA and suppresses R-loop-based telomeric DNA damage. Nat Commun. 2021;12(1):3542.
   PubMed Web of Science ®Google Scholar
• Costa L, Corre S, Michel V, et al. USF1 defect drives p53 degradation duringhelicobacter pyloriinfection and accelerates gastric carcinogenesis. Gut. 2020;69(9):15802–11591.
   Web of Science ®Google Scholar
• Dahl ES, Aird KM. Ataxia-Telangiectasia mutated modulation of carbon metabolism in cancer. Front Oncol. 2017;7:291.
   PubMed Web of Science ®Google Scholar
• Zhang H. Regulation of DNA replication licensing and Re-replication by Cdt1. Int J Mol Sci. 2021 May 14;22(10).
   Web of Science ®Google Scholar
• Levrero M, Zucman-Rossi J. Mechanisms of HBV-induced hepatocellular carcinoma. J. Hepatol. 2016;64(1 Suppl):S84–S101.
   PubMedGoogle Scholar
• Malmstrom S, Eilard A, Larsson SB, et al. Genotype impact on long-term virological outcome of chronic hepatitis B virus infection. J Clin Virol. 2012;54(4):321–326.
   PubMed Web of Science ®Google Scholar
• European Association for the Study of the Liver. EASL 2017 clinical practice guidelines on the management of hepatitis B virus infection. J. Hepatol. 2017;67(2):370–398.
   PubMed Web of Science ®Google Scholar
• Kuhnhenn L, Jiang B, Kubesch A, et al. Impact of HBV genotype and mutations on HBV DNA and qHBsAg levels in patients with HBeAg-negative chronic HBV infection. Aliment Pharmacol Ther. 2018;47(11):1523–1535.
   PubMed Web of Science ®Google Scholar
• Sugiyama M, Tanaka Y, Kurbanov F, et al. Direct cytopathic effects of particular hepatitis B virus genotypes in severe combined immunodeficiency transgenic with urokinase-type plasminogen activator mouse with human hepatocytes. Gastroenterology. 2009;136(2):652–662.e3.
   PubMed Web of Science ®Google Scholar
• Elmore LW, Hancock AR, Chang SF, et al. Hepatitis B virus X protein and p53 tumor suppressor interactions in the modulation of apoptosis. Proc Natl Acad Sci U S A. 1997;94(26):14707–14712.
   PubMed Web of Science ®Google Scholar
• Geng X, Harry BL, Zhou Q, et al. Hepatitis B virus X protein targets the Bcl-2 protein CED-9 to induce intracellular Ca2+increase and cell death in caenorhabditis elegans. Proc Natl Acad Sci U S A. 2012;109(45):18465–18470.
   PubMed Web of Science ®Google Scholar
• Ng SA, Lee C. Hepatitis B virus X gene and hepatocarcinogenesis. J Gastroenterol. 2011;46(8):974–990.
   PubMed Web of Science ®Google Scholar