Evolutionary characteristics and immune mutation of hepatitis C virus genotype 1b among intravenous drug users in mainland, China
Sheng Wu
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorHuangbo Yuan
State Key Laboratory of Genetic Engineering, Human Phenome Institute, Fudan University, Shanghai, China
School of Life Sciences, Fudan University, Shanghai, China
Search for more papers by this authorHong Fan
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorYiyun Xu
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorZhenqiu Liu
State Key Laboratory of Genetic Engineering, Human Phenome Institute, Fudan University, Shanghai, China
School of Life Sciences, Fudan University, Shanghai, China
Search for more papers by this authorXuefu Wu
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorMingshan Wu
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorXin Zhang
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorTingting Shi
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorCorresponding Author
Tiejun Zhang
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Shanghai Institute of Infectious Diseases and Biosafety, Shanghai, China
Yiwu Research Institute, Fudan University, Yiwu, China
Correspondence
Tiejun Zhang, Department of Epidemiology, School of Public Health, Fudan University, Shanghai 200237, China.
Email: [email protected]
Search for more papers by this authorSheng Wu
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorHuangbo Yuan
State Key Laboratory of Genetic Engineering, Human Phenome Institute, Fudan University, Shanghai, China
School of Life Sciences, Fudan University, Shanghai, China
Search for more papers by this authorHong Fan
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorYiyun Xu
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorZhenqiu Liu
State Key Laboratory of Genetic Engineering, Human Phenome Institute, Fudan University, Shanghai, China
School of Life Sciences, Fudan University, Shanghai, China
Search for more papers by this authorXuefu Wu
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorMingshan Wu
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorXin Zhang
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorTingting Shi
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Search for more papers by this authorCorresponding Author
Tiejun Zhang
Department of Epidemiology, School of Public Health, Fudan University, Shanghai, China
Shanghai Institute of Infectious Diseases and Biosafety, Shanghai, China
Yiwu Research Institute, Fudan University, Yiwu, China
Correspondence
Tiejun Zhang, Department of Epidemiology, School of Public Health, Fudan University, Shanghai 200237, China.
Email: [email protected]
Search for more papers by this authorFunding information
This study was supported by the Special Foundation for Science and Technology Basic Research Program (2019FY101103), the Natural Science Foundation of China (81772170) and by the National Key Research and Development Program of China (No. 2017YFC0211704).
Abstract
China is one of the countries with the heaviest burden of hepatitis C virus (HCV) worldwide, especially subtype 1b. To better control hepatitis C, insights into the characteristics of dynamic spread and genomic mutations are urgently needed. We retrieved sequences of HCV-1b NS5B among intravenous drug users (IDUs) and general people (Non-IDUs) in China from 2000 to 2011 in NCBI. Bayesian phylogenetic and phylogeographic analyses were used to evaluate the transmission dynamics of HCV-1b. Non-synonymous substitutions were detected to illustrate immune adaptation. Evolutionary history demonstrated that HCV-1b effective population size experienced a sharp increase in 1990. HCV-1b sequences among IDUs had a higher estimated evolutionary rate (5.7185 × 10−3 substitutions/site/year) than overall (7.7332 × 10−4). 105/136 (77.2%) of HCV-1b sequences clustered into 38 networks. The average non-synonymous HCV-1b immune epitopes among IDUs were 0.211, higher than non-IDUs, especially in the HLA-A*02 molecular recognition region. All of these posed significant challenges for the prevention and treatment of HCV. Heterogeneity and genetic linkages of HCV-1b suggest that evolutionary surveillance of HCV in cities in east-central China and among IDUs could not be neglected.
CONFLICT OF INTERESTS
The authors declare that they have no competing interests.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
Filename | Description |
---|---|
jvh13647-sup-0001-Supinfo.docxWord 2007 document , 13.2 MB | Supplementary Material |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- 1Thrift AP, El-Serag HB, Kanwal F. Global epidemiology and burden of HCV infection and HCV-related disease. Nat Rev Gastroenterol Hepatol. 2017; 14(2): 122-132.
- 2Lauer GM, Walker BD. Hepatitis C virus infection. N Engl J Med. 2001; 345(1): 41-52.
- 3McHutchison JG, Bacon BR. Chronic hepatitis C: an age wave of disease burden. Am J Manag Care. 2005; 11(10 Suppl): S286-S295; quiz S307-S311.
- 4Keyvani H, Fazlalipour M, Monavari SH, Mollaie HR. Hepatitis C virus–proteins, diagnosis, treatment and new approaches for vaccine development. Asian Pac J Cancer Prev. 2012; 13(12): 5931-5949.
- 5Degenhardt L, Peacock A, Colledge S, et al. Global prevalence of injecting drug use and sociodemographic characteristics and prevalence of HIV, HBV, and HCV in people who inject drugs: a multistage systematic review. Lancet Global Health. 2017; 5(12): e1192-e1207.
- 6Lanièce Delaunay C, Godin A, Kronfli N, et al. Can hepatitis C elimination targets be sustained among people who inject drugs post-2030? Int J Drug Policy. 2021; 96:103343.
- 7Blach S, Zeuzem S, Manns M, et al. Global prevalence and genotype distribution of hepatitis C virus infection in 2015: a modelling study. Lancet Gastroenterol Hepatol. 2017; 2(3): 161-176.
- 8Liu C-R, Li XI, Chan P-L, et al. Prevalence of hepatitis C virus infection among key populations in China: a systematic review. Int J Infect Dis. 2019; 80: 16-27.
- 9Sarpel D, Wasserman I, Trochtenberg AL, et al. Non-adherence is the most important risk factor for ledipasvir/sofosbuvir HCV treatment failure in the real world. Hepatology. 2016; 64: 811-1050.
- 10Geddawy A, Ibrahim YF, Elbahie NM, Ibrahim MA. Direct acting anti-hepatitis C virus drugs: clinical pharmacology and future direction. J Transl Int Med. 2017; 5(1): 8-17.
- 11Persico M, Coppola N, Rosato V, Abenavoli L, Masarone M, De Luna A. HCV antiviral therapy in injection drug users: difficult to treat or easy to cure? Ann Hepatol. 2015; 14(3): 325-332.
- 12Ashfaq UA, Javed T, Rehman S, Nawaz Z, Riazuddin S. An overview of HCV molecular biology, replication and immune responses. Virol J. 2011; 8(1): 161.
- 13Behrens SE, Tomei L, De Francesco R. Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus. EMBO J. 1996; 15(1): 12-22.
- 14De Francesco R, Tomei L, Altamura S, Summa V, Migliaccio G. Approaching a new era for hepatitis C virus therapy: inhibitors of the NS3-4A serine protease and the NS5B RNA-dependent RNA polymerase. Antiviral Res. 2003; 58(1): 1-16.
- 15Shoukry NH, Hepatitis C. Vaccines, antibodies, and T cells. Front Immunol. 2018; 9: 1480.
- 16Di Maio VC, Cento V, Mirabelli C, et al. Hepatitis C virus genetic variability and the presence of NS5B resistance-associated mutations as natural polymorphisms in selected genotypes could affect the response to NS5B inhibitors. Antimicrob Agents Chemother. 2014; 58(5): 2781.
- 17Lutchman G, Danehower S, Song B, et al. Mutation rate of the hepatitis C virus NS5B in patients undergoing treatment with ribavirin monotherapy. Gastroenterology. 2007; 132(5): 1757-1766.
- 18Costantino A, Spada E, Equestre M, et al. Naturally occurring mutations associated with resistance to HCV NS5B polymerase and NS3 protease inhibitors in treatment-naïve patients with chronic hepatitis C. Virol J. 2015; 12(1): 186.
- 19Li M, Zhuang H, Wei L. How would China achieve WHO's target of eliminating HCV by 2030? Expert Rev Anti Infect Ther. 2019; 17(10): 763-773.
- 20Wei L, Hou JL. The guideline of prevention and treatment for hepatitis C: a 2015 update. Zhonghua Gan Zang Bing Za Zhi. 2015; 23(12): 906-923.
- 21Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013; 30(4): 772-780.
- 22Kumar S, Stecher G, Li M, Knyaz C, Tamura K. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018; 35(6): 1547-1549.
- 23Martin DP, Murrell B, Golden M, Khoosal A, Muhire B. RDP4: detection and analysis of recombination patterns in virus genomes. Virus Evol. 2015; 1:vev003.
- 24Drummond AJ, Rambaut A, Shapiro B, Pybus OG. Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol. 2005; 22(5): 1185-1192.
- 25Bouckaert R, Vaughan TG, Barido-Sottani J, et al. BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Comput Biol. 2019; 15(4):e1006650.
- 26Bielejec F, Baele G, Vrancken B, Suchard MA, Rambaut A, Lemey P. Sprea D3: interactive visualization of spatiotemporal history and trait evolutionary processes. Mol Biol Evol. 2016; 33(8): 2167-2169.
- 27Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014; 30(9): 1312-1313.
- 28Ragonnet-Cronin M, Hodcroft E, Hué S, et al. Automated analysis of phylogenetic clusters. BMC Bioinformatics. 2013; 14: 317.
- 29Bartlett SR, Wertheim JO, Bull RA, et al. A molecular transmission network of recent hepatitis C infection in people with and without HIV: implications for targeted treatment strategies. J Viral Hepatitis. 2017; 24(5): 404-411.
- 30Li X, Xue Y, Lin YI, et al. Evolutionary dynamics and complicated genetic transmission network patterns of HIV-1 CRF01_AE among MSM in Shanghai, China. Sci Rep. 2016; 6:34729.
- 31Nakano T, Lu L, He Y, Fu Y, Robertson BH, Pybus OG. Population genetic history of hepatitis C virus 1b infection in China. J Gen Virol. 2006; 87(1): 73-82.
- 32Magiorkinis G, Magiorkinis E, Paraskevis D, et al. The global spread of hepatitis C virus 1a and 1b: a phylodynamic and phylogeographic analysis. PLoS Med. 2009; 6(12):e1000198.
- 33Wang Y, Wu HY, Zhao XC, et al. Evolutionary characteristics and positive selection site of hepatitis C virus isolated in intravenous drug users in Pudong new district, Shanghai. Zhonghua Liu Xing Bing Xue Za Zhi. 2017; 38(3): 378-383.
- 34Qian H-Z, Schumacher JE, Chen HT, Ruan Y-H. Injection drug use and HIV/AIDS in China: review of current situation, prevention and policy implications. Harm Reduct J. 2006; 3(1): 4.
- 35Chu TX, Levy JA. Injection drug use and HIV/AIDS transmission in China. Cell Res. 2005; 15(11): 865-869.
- 36Bao Y-P, Liu Z-M, Lu L. Review of HIV and HCV infection among drug users in China. Curr Opin Psychiatry. 2010; 23(3): 187-194.
- 37Liu Y, Hsiang MS, Zhou H, et al. Malaria in overseas labourers returning to China: an analysis of imported malaria in Jiangsu Province, 2001–2011. Malar J. 2014; 13(1): 29.
- 38Bao YP, Liu ZM. Systematic review of HIV and HCV infection among drug users in China. Int J STD AIDS. 2009; 20(6): 399-405.
- 39Zhang C, Wu N, Liu J, et al. HCV subtype characterization among injection drug users: implication for a crucial role of Zhenjiang in HCV transmission in China. PLoS One. 2011; 6(2):e16817.
- 40Yuan H, Liu Z, Wu X, et al. Evolutionary characteristics and genetic transmission patterns of predominant HIV-1 subtypes among men who have sex with men in China. Int J Infect Dis. 2020; 90: 125-131.
- 41Pang X, Wei H, Huang J, et al. Patterns and risk of HIV-1 transmission network among men who have sex with men in Guangxi, China. Sci Rep. 2021; 11(1): 513.
- 42Thorpe LE, Ouellet LJ, Hershow R, et al. Risk of hepatitis C virus infection among young adult injection drug users who share injection equipment. Am J Epidemiol. 2002; 155(7): 645-653.
- 43Wertheim JO, Oster AM, Johnson JA, et al. Transmission fitness of drug-resistant HIV revealed in a surveillance system transmission network. Virus Evol. 2017; 3(1):vex008.
- 44Christiansen MT, Hullegie SJ, Schutten M, et al. Use of whole genome sequencing in the Dutch Acute HCV in HIV study: focus on transmitted antiviral resistance. Clin Microbiol Infect. 2017; 23(2): 123.e1-123.e4.
- 45Jiang H, Zhang X, Zhang C, et al. Trends of HIV, hepatitis C virus and syphilis seroprevalence among injection and non-injection drug users in southwestern China, 2010–2017. AIDS Care. 2020: 1–6. doi:10.1080/09540121.2020.1856320
- 46Gupta RK, Jordan MR, Sultan BJ, et al. Global trends in antiretroviral resistance in treatment-naive individuals with HIV after rollout of antiretroviral treatment in resource-limited settings: a global collaborative study and meta-regression analysis. Lancet (London, England). 2012; 380(9849): 1250-1258.
- 47Bowen DG, Walker CM. Mutational escape from CD8+ T cell immunity: HCV evolution, from chimpanzees to man. J Exp Med. 2005; 201(11): 1709-1714.
- 48De Francesco R. Molecular virology of the hepatitis C virus. J Hepatol. 1999; 31: 47-53.
- 49Colomba GME, Urone N, Marco VD, Ferraro D. Phylodynamic analysis and implication of HCV genotype 4 variability on antiviral drug response and T-cell recognition. Viruses. 2020; 12(12):1363.