Improved hepatitis delta virus genome characterization by single molecule full-length genome sequencing combined with VIRiONT pipeline.
HDV editing
genotyping
hepatitis delta virus (HDV)
local pipeline
long-read sequencing
whole-genome sequencing
Journal
Journal of medical virology
ISSN: 1096-9071
Titre abrégé: J Med Virol
Pays: United States
ID NLM: 7705876
Informations de publication
Date de publication:
03 2023
03 2023
Historique:
revised:
08
02
2023
received:
30
09
2022
accepted:
28
02
2023
medline:
30
3
2023
pubmed:
8
3
2023
entrez:
7
3
2023
Statut:
ppublish
Résumé
Hepatitis B virus (HBV) and hepatitis D virus (HDV) coinfection confers a greater risk for accelerated liver disease progression. Full-length characterization of HDV genome is necessary to understand pathogenesis and treatment response. However, owing to its high variability and tight structure, sequencing approaches remain challenging. Herein, we present a workflow to amplify, sequence, and analyze the whole HDV genome in a single fragment. Sequencing was based on the Oxford Nanopore Technologies long-read sequencing followed by a turnkey analysis pipeline (VIRiONT, VIRal in-house ONT sequencing analysis pipeline) that we developed and make available online for free. For the first time, HDV genome was successfully amplified and full-length sequenced in a single fragment, allowing accurate subtyping from 30 clinical samples. High variability of edition, a crucial step in viral life cycle, was found among samples (from 0% to 59%). Additionally, a new subtype of HDV genotype 1 was identified. We provide a complete workflow for assessment of HDV genome at full-length quasispecies resolution overcoming genome assembly issues and helping to identify modifications throughout the whole genome. This will help a better understanding of the impact of genotype/subtype, viral dynamics, and structural variants on HDV pathogenesis and treatment response.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e28634Informations de copyright
© 2023 The Authors. Journal of Medical Virology published by Wiley Periodicals LLC.
Références
Yurdaydın C, Idilman R, Bozkaya H, Bozdayi AM. Natural history and treatment of chronic delta hepatitis. J Viral Hepatitis. 2010;17:749-756.
Farci P, Niro G. Clinical features of hepatitis D. Semin Liver Dis. 2012;32:228-236.
Caredda F, Rossi E, Monforte A, et al. Hepatitis B virus-associated coinfection and superinfection with agent: indistinguishable disease with different outcome. J Infect Dis. 1985;151:925-928.
Roulot D, Brichler S, Layese R, et al. Origin, HDV genotype and persistent viremia determine outcome and treatment response in patients with chronic hepatitis Delta. J Hepatol. 2020;73:1046-1062. doi:10.1016/j.jhep.2020.06.038
Tseligka ED, Clément S, Negro F. HDV pathogenesis: unravelling ariadne's thread. Viruses. 2021;13:778.
Chen HY, Shen DT, Ji DZ, et al. Prevalence and burden of hepatitis D virus infection in the global population: a systematic review and meta-analysis. Gut. 2019;68:512-521.
Stockdale AJ, Kreuels B, Henrion MYR, et al. The global prevalence of hepatitis D virus infection: systematic review and meta-analysis. J Hepatol. 2020;73:523-532.
Stockdale AJ, Kreuels B, Henrion MRY, Giorgi E, Kyomuhangi I, Geretti AM. Hepatitis D prevalence: problems with extrapolation to global population estimates. Gut. 2020;69:396-397.
Wedemeyer H, Negro F. Devil hepatitis D: an orphan disease or largely underdiagnosed? Gut. 2019;68:381-382.
Chen PJ, Kalpana G, Goldberg J, et al. Structure and replication of the genome of the hepatitis delta virus. Proc Natl Acad Sci U S A. 1986;83:8774-8778.
Le Gal F, Brichler S, Drugan T, et al. Genetic diversity and worldwide distribution of the deltavirus genus: a study of 2,152 clinical strains. Hepatology. 2017;66:1826-1841.
Hsu C-W, Juang HH, Kuo CY, et al. Structural pattern differences in unbranched rod-like RNA of hepatitis delta virus affect RNA editing. Viruses. 2019;11:934.
Sureau C, Negro F. The hepatitis delta virus: replication and pathogenesis. J Hepatol. 2016;64:S102-S116.
Casey JL. Control of ADAR1 editing of hepatitis delta virus RNAs. Curr Top Microbiol Immunol. 2012;353:123-143.
Dziri S, Rodriguez C, Gerber A, et al. Variable in vivo hepatitis D virus (HDV) RNA editing rates according to the HDV genotype. Viruses. 2021;13:1572.
Wang W, Lempp FA, Schlund F, et al. Assembly and infection efficacy of hepatitis B virus surface protein exchanges in 8 hepatitis D virus genotype isolates. J Hepatol. 2021;75:311-323. doi:10.1016/j.jhep.2021.03.025
Ivaniushina V, Radjef N, Alexeeva M, et al. Hepatitis delta virus genotypes I and II cocirculate in an endemic area of Yakutia, Russia. J Gen Virol. 2001;82:2709-2718.
Abeywickrama-Samarakoon N, Cortay JC, Sureau C, et al. Hepatitis Delta Virus histone mimicry drives the recruitment of chromatin remodelers for viral RNA replication. Nat Commun. 2020;11:419.
Homs M, Rodriguez-Frias F, Gregori J, et al. Evidence of an exponential decay pattern of the hepatitis delta virus evolution rate and fluctuations in quasispecies complexity in long-term studies of chronic delta infection. PLoS One. 2016;11:e0158557.
Wu S, Zhang Y, Tang Y, et al. Molecular epidemiology and clinical characteristics of hepatitis delta virus (HDV) infected patients with elevated transaminases in Shanghai, China. BMC Infect Dis. 2020;20:565.
Hospices Civils de Lyon. Creation of a Cohort for the Quantitation and Characterization of Circulating Viral RNAs as a New Biomarker of Hepatitis B Functional Cure. 2021. https://clinicaltrials.gov/ct2/show/NCT03825458
Scholtes C, Icard V, Amiri M, et al. Standardized one-step real-time reverse transcription-PCR assay for universal detection and quantification of hepatitis delta virus from clinical samples in the presence of a heterologous internal-control RNA. J Clin Microbiol. 2012;50:2126-2128.
Kay A, Melo da Silva E, Pedreira H, et al. HBV/HDV co-infection in the Western Brazilian Amazonia: an intriguing mutation among HDV genotype 3 carriers. J Viral Hepatitis. 2014;21:921-924.
Dohm JC, Peters P, Stralis-Pavese N, Himmelbauer H. Benchmarking of long-read correction methods. NAR Genom Bioinform. 2020;2:lqaa037.
Koren S, Rhie A, Walenz BP, et al. De novo assembly of haplotype-resolved genomes with trio binning. Nat Biotechnol. 2018;36:1174-1182.
Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH, Phillippy AM. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 2017;27:722-736.
De Coster W, D'Hert S, Schultz DT, Cruts M, Van Broeckhoven C. NanoPack: visualizing and processing long-read sequencing data. Bioinformatics. 2018;34:2666-2669.
Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094-3100.
Quinlan AR, Hall IM. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics. 2010;26:841-842.
Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004;32:1792-1797.
Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987;4:406-425.
Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980;16:111-120.
Köster J, Rahmann S. Snakemake-a scalable bioinformatics workflow engine. Bioinformatics. 2018;34:3600.
Dény P, Drugan C, Gatherer D, Kay AC, Le Gal F, Drugan T. Hepatitis D Virus clades and genotypes: a practical approach. In: Rizzetto M, Smedile A, eds. Viruses. Vol 4. Il Pensiero Scientifico Editore; 2019:49-80.
Weirather JL, de Cesare M, Wang Y, et al. Comprehensive comparison of pacific biosciences and Oxford nanopore technologies and their applications to transcriptome analysis. F1000Research. 2017;6:100.
Yan Z, Zeng J, Yu Y, et al. HBVcircle: A novel tool to investigate hepatitis B virus covalently closed circular DNA. J Hepatol. 2017;66:1149-1157.
Luo X, Kang X, Schönhuth A. Strainline: full-length de novo viral haplotype reconstruction from noisy long reads. Genome Biol. 2022;23:29.
Kumar S, Stecher G, Tamura K. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol. 2016;33:1870-1874.
Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol. 2003;52:696-704.
Ronquist F, Teslenko M, van der Mark P, et al. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol. 2012;61:539-542.
Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783-791.
Pflüger LS, Nörz D, Volz T, et al. Clinical establishment of a laboratory developed quantitative HDV PCR assay on the cobas6800 high-throughput system. JHEP Reports. 2021;3:100356.
Le Gal F, Dziri S, Gerber A, et al. Performance characteristics of a new consensus commercial kit for hepatitis D virus RNA viral load quantification. J Clin Microbiol. 2017;55:431-441.
Radjef N, Gordien E, Ivaniushina V, et al. Molecular phylogenetic analyses indicate a wide and ancient radiation of African hepatitis delta virus, suggesting a deltavirus genus of at least seven major clades. J Virol. 2004;78:2537-2544.
Butler EK, Rodgers MA, Coller KE, et al. High prevalence of hepatitis delta virus in Cameroon. Sci Rep. 2018;8:11617.
Karimzadeh H, Usman Z, Frishman D, Roggendorf M. Genetic diversity of hepatitis D virus genotype-1 in Europe allows classification into subtypes. J Viral Hepatitis. 2019;26:900-910.
Lucifora J, Delphin M. Current knowledge on hepatitis delta virus replication. Antiviral Res. 2020;179:104812.
Sopena S, Godoy C, Tabernero D, et al. Quantitative characterization of hepatitis delta virus genome edition by next-generation sequencing. Virus Res. 2018;243:52-59.
Groc S, Abbate JL, Le Gal F, et al. High prevalence and diversity of hepatitis B and hepatitis delta virus in Gabon. J Viral Hepatitis. 2019;26:170-182.
Zakh R, Churkin A, Totzeck F, et al. A mathematical analysis of HDV genotypes: from molecules to cells. Mathematics. 2021;9:2063.
Rizzetto M. Targeting hepatitis D. Semin Liver Dis. 2018;38:066-072.
Sandmann L, Cornberg M. Experimental drugs for the treatment of hepatitis D. J Exp Pharmacol. 2021;13:461-468.