A novel hepatitis B virus species discovered in capuchin monkeys sheds new light on the evolution of primate hepadnaviruses

dc.contributorSistema FMUSP-HC: Faculdade de Medicina da Universidade de São Paulo (FMUSP) e Hospital das Clínicas da FMUSP
dc.contributor.authorSOUZA, Breno Frederico de Carvalho Dominguez
dc.contributor.authorKOENIG, Alexander
dc.contributor.authorRASCHE, Andrea
dc.contributor.authorCARNEIRO, Ianei de Oliveira
dc.contributor.authorSTEPHAN, Nora
dc.contributor.authorCORMAN, Victor Max
dc.contributor.authorROPPERT, Pia Luise
dc.contributor.authorGOLDMANN, Nora
dc.contributor.authorKEPPER, Ramona
dc.contributor.authorMUELLER, Simon Franz
dc.contributor.authorVOELKER, Christof
dc.contributor.authorSOUZA, Alex Junior Souza de
dc.contributor.authorGOMES-GOUVEA, Michele Soares
dc.contributor.authorMOREIRA-SOTO, Andres
dc.contributor.authorSTOECKER, Andreas
dc.contributor.authorNASSAL, Michael
dc.contributor.authorFRANKE, Carlos Roberto
dc.contributor.authorPINHO, Joao Renato Rebello
dc.contributor.authorSOARES, Manoel do Carmo Pereira
dc.contributor.authorGEYER, Joachim
dc.contributor.authorLEMEY, Philippe
dc.contributor.authorDROSTEN, Christian
dc.contributor.authorNETTO, Eduardo Martins
dc.contributor.authorGLEBE, Dieter
dc.contributor.authorDREXLER, Jan Felix
dc.date.accessioned2018-07-05T18:07:26Z
dc.date.available2018-07-05T18:07:26Z
dc.date.issued2018
dc.description.abstractBackground & Aims:All known hepatitis B virus (HBV) genotypes occur in humans and hominoid Old World non-human primates (NHPs). The divergent woolly monkey HBV (WMHBV) forms another orthohepadnavirus species. The evolutionary origins of HBV are unclear. Methods: We analysed sera from 124 Brazilian monkeys collected during 2012-2016 for hepadnaviruses using molecular and serological tools, and conducted evolutionary analyses. Results: We identified a novel orthohepadnavirus species in capuchin monkeys (capuchin monkey hepatitis B virus [CMHBV]). We found CMHBV-specific antibodies in five animals and high CMHBV concentrations in one animal. Noninflammatory, probably chronic infection was consistent with an intact preCore domain, low genetic variability, core deletions in deep sequencing, and no elevated liver enzymes. Cross-reactivity of antisera against surface antigens suggested antigenic relatedness of HBV, CMHBV, and WMHBV. Infection-determining CMHBV surface peptides bound to the human HBV receptor (human sodium taurocholate co-transporting polypeptide), but preferentially interacted with the capuchin monkey receptor homologue. CMHBV and WMHBV pseudo-types infected human hepatoma cells via the human sodium tralised by HBV vaccine-derived antibodies, suggesting that cross-species infections may be possible. Ancestral state reconstructions and sequence distance comparisons associated HBV with humans, whereas primate hepadnaviruses as a whole were projected to NHP ancestors. Co-phylogenetic analyses yielded evidence for co-speciation of hepadnaviruses and New World NHP. Bayesian hypothesis testing yielded strong support for an association of the HBV stem lineage with hominoid ancestors. Neither CMHBV nor WMHBV was likely the ancestor of the divergent human HBV genotypes found in American natives. Conclusions: Our data suggest ancestral co-speciation of hepadnaviruses and NHP, and an Old World origin of the divergent HBV genotypes FAH. The identification of a novel primate hepadnavirus offers new perspectives for urgently needed animal models of chronic hepatitis B. Lay summary: The origins of HBV are unclear. The new orthohepadnavirus species from Brazilian capuchin monkeys resembled HBV in elicited infection patterns and could infect human liver cells using the same receptor as HBV. Evolutionary analyses suggested that primate HBV-related viruses might have emerged in African ancestors of New World monkeys millions of years ago. HBV was associated with hominoid primates, including humans and apes, suggesting evolutionary origins of HBV before the formation of modern humans. HBV genotypes F/H found in American natives were divergent from those found in American monkeys, and likely introduced along prehistoric human migration. Our results elucidate the evolutionary origins and dispersal of primate HBV, identify a new orthohepadnavirus reservoir, and enable new perspectives for animal models of hepatitis B. (C) 2018 European Association for the Study of the Liver.
dc.description.indexMEDLINE
dc.description.sponsorshipGerman Research Foundation (DFG.) [DR 810/1-1, GL 595/4-1, SFB 1021/2]
dc.description.sponsorshipEuropean Union's Horizon 2020 research and innovation programme through the COMPARE project [643476]
dc.description.sponsorshipUniversity of Bonn Medical Centre intramural programme (BONFOR)
dc.description.sponsorshipEuropean Union's Horizon 2020 research and innovation programme through the ZIKAlliance project [734548]
dc.identifier.citationJOURNAL OF HEPATOLOGY, v.68, n.6, p.1114-1122, 2018
dc.identifier.doi10.1016/j.jhep.2018.01.029
dc.identifier.eissn1600-0641
dc.identifier.issn0168-8278
dc.identifier.urihttps://observatorio.fm.usp.br/handle/OPI/27144
dc.language.isoeng
dc.publisherELSEVIER SCIENCE BV
dc.relation.ispartofJournal of Hepatology
dc.rightsrestrictedAccess
dc.rights.holderCopyright ELSEVIER SCIENCE BV
dc.subjectHepatitis B virus
dc.subjectViral evolution
dc.subjectNew World
dc.subjectPrimate
dc.subjectHuman dispersal
dc.subject.othercebus-apella
dc.subject.othernonhuman-primates
dc.subject.othersurface-antigen
dc.subject.otherhbv infection
dc.subject.otherwild primates
dc.subject.othergenotype-f
dc.subject.otherorigin
dc.subject.otherworld
dc.subject.otherhumans
dc.subject.otherhepatocytes
dc.subject.wosGastroenterology & Hepatology
dc.titleA novel hepatitis B virus species discovered in capuchin monkeys sheds new light on the evolution of primate hepadnaviruses
dc.typearticle
dc.type.categoryoriginal article
dc.type.versionpublishedVersion
dspace.entity.typePublication
hcfmusp.affiliation.countryBélgica
hcfmusp.affiliation.countryAlemanha
hcfmusp.affiliation.countryisode
hcfmusp.affiliation.countryisobe
hcfmusp.author.externalSOUZA, Breno Frederico de Carvalho Dominguez:Univ Bonn, Med Ctr, Inst Virol, Bonn, Germany; Univ Fed Bahia, Univ Hosp Prof Edgard Santos, Infect Dis Res Lab, Salvador, BA, Brazil
hcfmusp.author.externalKOENIG, Alexander:Justus Liebig Univ, Natl Reference Ctr Hepatitis & Viruses B D, Inst Med Virol, D-35392 Giessen, Germany; Deutsch Zentrum Infekt Forsch, German Ctr Infect Res, Berlin, Germany
hcfmusp.author.externalRASCHE, Andrea:Univ Bonn, Med Ctr, Inst Virol, Bonn, Germany; Deutsch Zentrum Infekt Forsch, German Ctr Infect Res, Berlin, Germany; Humboldt Univ, Freie Univ Berlin, Charite Univ Med Berlin, Berlin, Germany; Berlin Inst Hlth, Inst Virol, Berlin, Germany
hcfmusp.author.externalCARNEIRO, Ianei de Oliveira:Univ Fed Bahia, Sch Vet Med, Salvador, BA, Brazil
hcfmusp.author.externalSTEPHAN, Nora:Justus Liebig Univ, Natl Reference Ctr Hepatitis & Viruses B D, Inst Med Virol, D-35392 Giessen, Germany; Deutsch Zentrum Infekt Forsch, German Ctr Infect Res, Berlin, Germany
hcfmusp.author.externalCORMAN, Victor Max:Univ Bonn, Med Ctr, Inst Virol, Bonn, Germany; Deutsch Zentrum Infekt Forsch, German Ctr Infect Res, Berlin, Germany; Humboldt Univ, Freie Univ Berlin, Charite Univ Med Berlin, Berlin, Germany; Berlin Inst Hlth, Inst Virol, Berlin, Germany
hcfmusp.author.externalROPPERT, Pia Luise:Justus Liebig Univ, Natl Reference Ctr Hepatitis & Viruses B D, Inst Med Virol, D-35392 Giessen, Germany; Deutsch Zentrum Infekt Forsch, German Ctr Infect Res, Berlin, Germany
hcfmusp.author.externalGOLDMANN, Nora:Justus Liebig Univ, Natl Reference Ctr Hepatitis & Viruses B D, Inst Med Virol, D-35392 Giessen, Germany; Deutsch Zentrum Infekt Forsch, German Ctr Infect Res, Berlin, Germany
hcfmusp.author.externalKEPPER, Ramona:Justus Liebig Univ, Natl Reference Ctr Hepatitis & Viruses B D, Inst Med Virol, D-35392 Giessen, Germany; Deutsch Zentrum Infekt Forsch, German Ctr Infect Res, Berlin, Germany
hcfmusp.author.externalMUELLER, Simon Franz:Justus Liebig Univ Giessen, Biomed Res Ctr Seltersberg, Inst Pharmacol & Toxicol, Giessen, Germany
hcfmusp.author.externalVOELKER, Christof:Univ Bonn, Inst Biochem & Mol Biol, Bonn, Germany
hcfmusp.author.externalSOUZA, Alex Junior Souza de:Evandro Chagas Inst, Hepatol Sect, Belem, Para, Brazil; Univ Sao Paulo, Fac Vet Med & Anim Sci, Dept Pathol, Sao Paulo, Brazil
hcfmusp.author.externalMOREIRA-SOTO, Andres:Univ Bonn, Med Ctr, Inst Virol, Bonn, Germany; Humboldt Univ, Freie Univ Berlin, Charite Univ Med Berlin, Berlin, Germany; Berlin Inst Hlth, Inst Virol, Berlin, Germany
hcfmusp.author.externalSTOECKER, Andreas:Univ Fed Bahia, Univ Hosp Prof Edgard Santos, Infect Dis Res Lab, Salvador, BA, Brazil
hcfmusp.author.externalNASSAL, Michael:Univ Hosp Freiburg, Dept Internal Med Mol Biol 2, Freiburg, Germany
hcfmusp.author.externalFRANKE, Carlos Roberto:Univ Fed Bahia, Sch Vet Med, Salvador, BA, Brazil
hcfmusp.author.externalSOARES, Manoel do Carmo Pereira:Evandro Chagas Inst, Hepatol Sect, Belem, Para, Brazil
hcfmusp.author.externalGEYER, Joachim:Justus Liebig Univ Giessen, Biomed Res Ctr Seltersberg, Inst Pharmacol & Toxicol, Giessen, Germany
hcfmusp.author.externalLEMEY, Philippe:Katholieke Univ Leuven, Rega Inst, Dept Microbiol & Immunol, Leuven, Belgium
hcfmusp.author.externalDROSTEN, Christian:Univ Bonn, Med Ctr, Inst Virol, Bonn, Germany; Deutsch Zentrum Infekt Forsch, German Ctr Infect Res, Berlin, Germany; Humboldt Univ, Freie Univ Berlin, Charite Univ Med Berlin, Berlin, Germany; Berlin Inst Hlth, Inst Virol, Berlin, Germany
hcfmusp.author.externalNETTO, Eduardo Martins:Univ Fed Bahia, Univ Hosp Prof Edgard Santos, Infect Dis Res Lab, Salvador, BA, Brazil
hcfmusp.author.externalGLEBE, Dieter:Justus Liebig Univ, Natl Reference Ctr Hepatitis & Viruses B D, Inst Med Virol, D-35392 Giessen, Germany; Deutsch Zentrum Infekt Forsch, German Ctr Infect Res, Berlin, Germany
hcfmusp.author.externalDREXLER, Jan Felix:Univ Bonn, Med Ctr, Inst Virol, Bonn, Germany; Deutsch Zentrum Infekt Forsch, German Ctr Infect Res, Berlin, Germany; Humboldt Univ, Freie Univ Berlin, Charite Univ Med Berlin, Berlin, Germany; Berlin Inst Hlth, Inst Virol, Berlin, Germany
hcfmusp.citation.scopus48
hcfmusp.contributor.author-fmusphcMICHELE SOARES GOMES GOUVEA
hcfmusp.contributor.author-fmusphcJOAO RENATO REBELLO PINHO
hcfmusp.description.beginpage1114
hcfmusp.description.endpage1122
hcfmusp.description.issue6
hcfmusp.description.volume68
hcfmusp.origemWOS
hcfmusp.origem.pubmed29428874
hcfmusp.origem.scopus2-s2.0-85044504062
hcfmusp.origem.wosWOS:000432491000003
hcfmusp.publisher.cityAMSTERDAM
hcfmusp.publisher.countryNETHERLANDS
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