Viral whole genome sequencing reveals high variations in APOBEC3 editing between HPV risk categories.


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:
Oct 2024
Historique:
revised: 23 09 2024
received: 05 02 2024
accepted: 30 09 2024
medline: 14 10 2024
pubmed: 14 10 2024
entrez: 14 10 2024
Statut: ppublish

Résumé

High-risk human papillomavirus (HPV) infections are responsible for cervical cancer. However, little is known about the differences between HPV types and risk categories regarding their genetic diversity and particularly APOBEC3-induced mutations - which contribute to the innate immune response to HPV. Using a capture-based next-generation sequencing, 156 HPV whole genome sequences covering 43 HPV types were generated from paired cervical and anal swabs of 30 Togolese female sex workers (FSWs) sampled in 2017. Genetic diversity and APOBEC3-induced mutations were assessed at the viral whole genome and gene levels. Thirty-four pairwise sequence comparisons covering 24 HPV types in cervical and anal swabs revealed identical infections in the two anatomical sites. Differences in genetic diversity among HPV types was observed between patients. The E6 gene was significantly less conserved in low-risk HPVs (lrHPVs) compared to high-risk HPVs (hrHPVs) (p = 0.009). APOBEC3-induced mutations were found to be more common in lrHPVs than in hrHPVs (p = 0.005), supported by our data and by using large HPV sequence collections from the GenBank database. Focusing on the most common lrHPVs 6 and 11 and hrHPVs 16 and 18, APOBEC3-induced mutations were predominantly found in the E4 and E6 genes in lrHPVs, but were almost absent in these genes in hrHPVs. The variable APOBEC3 mutational signatures could contribute to the different oncogenic potentials between HPVs. Further studies are needed to conclusively determine whether APOBEC3 editing levels are associated to the carcinogenic potential of HPVs at the type and sublineage scales.

Identifiants

pubmed: 39400339
doi: 10.1002/jmv.70002
doi:

Substances chimiques

APOBEC3 proteins, human EC 3.5.4.5
APOBEC Deaminases EC 3.5.4.5
Cytidine Deaminase EC 3.5.4.5

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e70002

Informations de copyright

© 2024 The Author(s). Journal of Medical Virology published by Wiley Periodicals LLC.

Références

Rodriguez AC, Schiffman M, Herrero R, et al. Rapid clearance of human papillomavirus and implications for clinical focus on persistent infections. J Natl Cancer Inst. 2008;100:513‐517.
Plummer M, Schiffman M, Castle PE, Maucort‐Boulch D, Wheeler CM. A 2‐Year prospective study of human papillomavirus persistence among women with a cytological diagnosis of atypical squamous cells of undetermined significance or Low‐Grade squamous intraepithelial lesion. J Infect Dis. 2007;195:1582‐1589.
de Martel C, Plummer M, Vignat J, Franceschi S. Worldwide burden of cancer attributable to HPV by site, country and HPV type. Int J Cancer. 2017;141:664‐670.
Ferlay J, Colombet M, Soerjomataram I, et al. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer. 2019;144:1941‐1953.
Bray F, Parkin DM, Gnangnon F, et al. Cancer in sub‐Saharan Africa in 2020: a review of current estimates of the national burden, data gaps, and future needs. Lancet Oncol. 2022;23:719‐728.
IARC. Cervix Uteri, Globocan 2020. Available at: https://gco.iarc.fr/today/data/factsheets/cancers/23-Cervix-uteri-fact-sheet.pdf. Accessed 19 October 2022.
Cervical Cancer Survival Rates | Cancer 5 Year Survival Rates. Available at: https://www.cancer.org/cancer/cervical-cancer/detection-diagnosis-staging/survival.html. Accessed 16 May 2022.
Muñoz N, Bosch FX, de Sanjosé S, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003;348:518‐527.
Bzhalava D, Eklund C, Dillner J. International standardization and classification of human papillomavirus types. Virology. 2015;476:341‐344.
Bernard H‐U, Calleja‐Macias IE, Dunn ST. Genome variation of human papillomavirus types: phylogenetic and medical implications. Int J Cancer. 2006;118:1071‐1076.
Latsuzbaia A, Wienecke‐Baldacchino A, Tapp J, et al. Characterization and diversity of 243 complete human papillomavirus genomes in cervical swabs using next generation sequencing. Viruses. 2020;12:1437.
Wakabayashi R, Nakahama Y, Nguyen V, Espinoza JL. The Host‐Microbe interplay in human Papillomavirus‐Induced carcinogenesis. Microorganisms. 2019;7:199.
Antaño‐Arias R, Del Moral‐Hernández O, Ortiz‐Ortiz J, et al. E6/E7 variants of human papillomavirus 16 associated with cervical carcinoma in women in Southern Mexico. Pathogens. 2021;10:773.
Yao Y, Yan Z, Dai S, et al. Human papillomavirus type 16 E1 mutations associated with cervical cancer in a han Chinese population. Int J Med Sci. 2019;16:1042‐1049.
Alexandrov LB, Nik‐Zainal S, Wedge DC, et al. Signatures of mutational processes in human cancer. Nature. 2013;500:415‐421.
Burns MB, Temiz NA, Harris RS. Evidence for APOBEC3B mutagenesis in multiple human cancers. Nature Genet. 2013;45:977‐983.
Roberts SA, Lawrence MS, Klimczak LJ, et al. An APOBEC cytidine deaminase mutagenesis pattern is widespread in human cancers. Nat Genet. 2013;45(9):970‐976. doi:10.1038/ng.2702
Vartanian J‐P, Guétard D, Henry M, Wain‐Hobson S. Evidence for editing of human papillomavirus DNA by APOBEC3 in benign and precancerous lesions. Science. 2008;320:230‐233.
Warren CJ, Xu T, Guo K, et al. APOBEC3A functions as a restriction factor of human papillomavirus. J Virol. 2015;89:688‐702.
Chen S, Li X, Qin J, et al. APOBEC3A possesses anticancer and antiviral effects by differential inhibition of HPV E6 and E7 expression on cervical cancer. Int J Clin Exp Med. 2015;8:10548‐10557.
Warren C, Westrich J, Doorslaer K, Pyeon D. Roles of APOBEC3A and APOBEC3B in human papillomavirus infection and disease progression. Viruses. 2017;9:233.
Vieira VC, Leonard B, White EA, et al. Human papillomavirus E6 triggers upregulation of the antiviral and cancer genomic DNA deaminase APOBEC3B. mBio. 2014;5:e02234‐14.
Zhu B, Xiao Y, Yeager M, et al. Mutations in the HPV16 genome induced by APOBEC3 are associated with viral clearance. Nat Commun. 2020;11:886.
Warren CJ, Santiago ML, Pyeon D. APOBEC3: friend or foe in human papillomavirus infection and oncogenesis? Annual Review of Virology. 2022;9:375‐395.
ICO/IARC Information Centre on HPV and Cancer. Togo: human papillomavirus and related cancers, fact sheet. 2023. 2023. Accessed October 8, 2024. https://hpvcentre.net/statistics/reports/TGO_FS.pdf
Ferré VM, Ekouevi DK, Gbeasor‐Komlanvi FA, et al. Prevalence of human papillomavirus, human immunodeficiency virus and other sexually transmitted infections among female sex workers in Togo: a national cross‐sectional survey. Clin Microbiol Infect. 2019;25:1560.e1‐1560.e7.
Lin C, Slama J, Gonzalez P, et al. Cervical determinants of anal HPV infection and high‐grade anal lesions in women: a collaborative pooled analysis. Lancet Infect Dis. 2019;19:880‐891.
Nasioutziki M, Chatzistamatiou K, Loufopoulos P‐D, et al. Cervical, anal and oral HPV detection and HPV type concordance among women referred for colposcopy. Infect Agent Cancer. 2020;15:22.
Guler T, Uygur D, Uncu M, et al. Coexisting anal human papilloma virus infection in heterosexual women with cervical HPV infection. Arch Gynecol Obstet. 2013;288:667‐672.
Thorsteinsson K, Storgaard M, Katzenstein TL, et al. Prevalence of cervical, oral, and anal human papillomavirus infection in women living with HIV in Denmark ‐ the SHADE cohort study. J Clin Virol. 2018;105:64‐71.
Hernandez BY, McDuffie K, Zhu X, et al. Anal human papillomavirus infection in women and its relationship with cervical infection. Cancer Epidemiol Biomarkers Prevent. 2005;14:2550‐2556.
Morhason‐Bello IO, Baisley K, Pavon MA, et al. Oral, genital and anal human papillomavirus infections among female sex workers in Ibadan, Nigeria. PLoS One. 2022;17:e0265269.
Kojic EM, Cu‐Uvin S, Conley L, et al. Human papillomavirus infection and cytologic abnormalities of the anus and cervix among HIV‐infected women in the study to understand the natural history of HIV/AIDS in the era of effective therapy (the SUN study). Sex Transm Dis. 2011;38:253‐259.
Doorbar J. The E4 protein; structure, function and patterns of expression. Virology. 2013;445:80‐98.
Mirabello L, Yeager M, Yu K, et al. HPV16 E7 genetic conservation is critical to carcinogenesis. Cell. 2017;170:1164‐1174.e6.
Schwarz E, Freese UK, Gissmann L, et al. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature. 1985;314:111‐114.
Doorbar J. Molecular biology of human papillomavirus infection and cervical cancer. Clin Sci. 2006;110:525‐541.
Tummers B, Van Der Burg S. High‐Risk human papillomavirus targets crossroads in immune signaling. Viruses. 2015;7:2485‐2506.
Trujillo‐Cirilo L, Torres‐Corioriles EI, Rangel‐Corona R, Corona‐Ortega MT, Weiss‐Steider B. Evidence that the viral oncoproteins E6 and E7 of HPV induce the expression of a functional IL‐2R on cervical cancer cells. Cytokine. 2021;148:155592.
Chiang C, Pauli E‐K, Biryukov J, et al. The human papillomavirus E6 oncoprotein targets USP15 and TRIM25 to suppress RIG‐I‐Mediated innate immune signaling. J Virol. 2018;92:e01737‐17.
Amador‐Molina A, Hernández‐Valencia J, Lamoyi E, Contreras‐Paredes A, Lizano M. Role of innate immunity against human papillomavirus (HPV) infections and effect of adjuvants in promoting specific immune response. Viruses. 2013;5:2624‐2642.
Smith NJ, Fenton TR. The APOBEC3 genes and their role in cancer: insights from human papillomavirus. J Mol Endocrinol. 2019;62:R269‐R287.
Wakae K, Aoyama S, Wang Z, et al. Detection of hypermutated human papillomavirus type 16 genome by next‐generation sequencing. Virology. 2015;485:460‐466.
Hirose Y, Onuki M, Tenjimbayashi Y, et al. Within‐Host variations of human papillomavirus reveal APOBEC signature mutagenesis in the viral genome. J Virol. 2018;92:e00017‐e00018.
Mariaggi A‐A, Péré H, Perrier M, et al. Presence of human papillomavirus (HPV) apolipoprotein B messenger RNA editing, catalytic Polypeptide‐Like 3 (APOBEC)‐related minority variants in HPV‐16 genomes from anal and cervical samples but not in HPV‐52 and HPV‐58. J Infect Dis. 2018;218:1027‐1036.
Clifford GM, Tully S, Franceschi S. Carcinogenicity of human papillomavirus (HPV) types in HIV‐Positive women: a meta‐analysis from HPV infection to cervical cancer. Clin Infect Dis. 2017;64:1228‐1235.
Guan P, Howell‐Jones R, Li N, et al. Human papillomavirus types in 115,789 HPV‐positive women: a meta‐analysis from cervical infection to cancer. Int J Cancer. 2012;131:2349‐2359.
Murakami I, Egawa N, Griffin H, et al. Roles for E1‐independent replication and E6‐mediated p53 degradation during low‐risk and high‐risk human papillomavirus genome maintenance. PLoS Pathog. 2019;15:e1007755.
Venkatesan S, Rosenthal R, Kanu N, et al. Perspective: APOBEC mutagenesis in drug resistance and immune escape in HIV and cancer evolution. Ann Oncol. 2018;29:563‐572.
Holmes A, Lameiras S, Jeannot E, et al. Mechanistic signatures of HPV insertions in cervical carcinomas. NPJ Genom Med. 2016;1:16004.
Van Doorslaer K, Li Z, Xirasagar S, et al. The papillomavirus episteme: a major update to the papillomavirus sequence database. Nucleic Acids Res 2017;45:D499‐D506.
Li H, Durbin R. Fast and accurate short read alignment with Burrows‐Wheeler transform. Bioinformatics. 2009;25:1754‐1760.
Danecek P, Bonfield JK, Liddle J, et al. Twelve years of SAMtools and BCFtools. Gigascience. 2021;10:giab008.
Sievers F, Wilm A, Dineen D, et al. Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7:539.
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403‐410.

Auteurs

Valentine Marie Ferré (VM)

Université Paris Cité, Inserm IAME UMR 1137, Paris, F-75018, France.
Service de Virologie, AP-HP, Hôpital Bichat - Claude Bernard, Paris, F-75018, France.

Romain Coppée (R)

Université Paris Cité, Inserm IAME UMR 1137, Paris, F-75018, France.

Fifonsi A Gbeasor-Komlanvi (FA)

Département de Santé Publique, Université de Lomé, Faculté des Sciences de la Santé, Lomé, Togo.
Centre Africain de Recherche en Epidémiologie et en Santé Publique (CARESP), Lomé, Togo.

Sophie Vacher (S)

Department of Genetics, Institut Curie, PSL Research University, Paris, France.

Antoine Bridier-Nahmias (A)

Université Paris Cité, Inserm IAME UMR 1137, Paris, F-75018, France.

Margot Bucau (M)

Département de Pathologie, AP-HP, Hôpital Bichat-Claude Bernard, Paris, F-75018, France.

Mounerou Salou (M)

Université de Lomé, Centre de Biologie Moléculaire et d'Immunologie, Lomé, Togo.

Sonia Lameiras (S)

Institut Curie, Genomics of Excellence (ICGex) Platform, PSL Research University, Paris, France.

Anne Couvelard (A)

Département de Pathologie, AP-HP, Hôpital Bichat-Claude Bernard, Paris, F-75018, France.
Université de Paris, Centre of Research on Inflammation, Paris, INSERM U1149, France.

Anoumou Claver Dagnra (AC)

Université de Lomé, Centre de Biologie Moléculaire et d'Immunologie, Lomé, Togo.
Programme national de lutte contre le sida et les infections sexuellement transmissibles, Lomé, Togo.

Ivan Bieche (I)

Department of Genetics, Institut Curie, PSL Research University, Paris, France.
INSERM U1016, Faculty of Pharmaceutical and Biological Sciences, Paris Cité University, Paris, France.

Diane Descamps (D)

Université Paris Cité, Inserm IAME UMR 1137, Paris, F-75018, France.
Service de Virologie, AP-HP, Hôpital Bichat - Claude Bernard, Paris, F-75018, France.

Didier K Ekouevi (DK)

Département de Santé Publique, Université de Lomé, Faculté des Sciences de la Santé, Lomé, Togo.
ISPED, Université de Bordeaux & Centre INSERM U1219 - Bordeaux Population Health, Bordeaux, France.

Jade Ghosn (J)

Université Paris Cité, Inserm IAME UMR 1137, Paris, F-75018, France.
Service de Maladies Infectieuses et Tropicales, AP-HP, Hôpital Bichat-Claude Bernard, Paris, F-75018, France.

Charlotte Charpentier (C)

Université Paris Cité, Inserm IAME UMR 1137, Paris, F-75018, France.
Service de Virologie, AP-HP, Hôpital Bichat - Claude Bernard, Paris, F-75018, France.

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