{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,23]],"date-time":"2026-07-23T18:22:15Z","timestamp":1784830935576,"version":"3.55.0"},"reference-count":37,"publisher":"MDPI AG","issue":"17","license":[{"start":{"date-parts":[[2022,8,30]],"date-time":"2022-08-30T00:00:00Z","timestamp":1661817600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Survival with Pancreatic Cancer Foundation, Utrecht, Netherlands","award":["AOK_LUMC-2017-2"],"award-info":[{"award-number":["AOK_LUMC-2017-2"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>The adenoviruses (AdVs) isolated from humans are taxonomically grouped in seven different species in the Mastadenovirus genus (HAdV-A through G). AdVs isolated from apes are often included in one of the human AdV species. Here we describe the sequence analyses of ten new AdVs that are related to the HAdV-C species and that were isolated from healthy western lowland gorillas, bonobos, chimpanzees, and orangutans kept in Dutch zoos. We analyzed these viruses and compared their genome sequences to those of human- and ape-derived AdV sequences in the NCBI GenBank database. Our data demonstrated that the ape-derived viruses clustering to HAdV-C are markedly distinct from the human HAdV-C species in the size and nucleotide composition (%GC) of their genome, differ in the amino-acid sequence of AdV proteins, and have longer RGD-loops in their penton-base proteins. The viruses form three well-separated clades (the human, the gorilla, and the combined group of the bonobo and chimpanzee viruses), and we propose that these should each be given species-level ranks. The Ad-lumc005 AdV isolated from orangutans was found to be very similar to the gorilla AdVs, and bootstrap inference provided evidence of recombination between the orangutan AdV and the gorilla AdVs. This suggests that this virus may not be a genuine orangutan AdV but may have been transferred from a gorilla to an orangutan host.<\/jats:p>","DOI":"10.3390\/ijms23179832","type":"journal-article","created":{"date-parts":[[2022,8,30]],"date-time":"2022-08-30T01:37:55Z","timestamp":1661823475000},"page":"9832","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Genome Analyses of Ten New Ape Adenoviruses with Similarity to Human Mastadenovirus C"],"prefix":"10.3390","volume":"23","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1844-9247","authenticated-orcid":false,"given":"Selas T. F.","family":"Bots","sequence":"first","affiliation":[{"name":"Department of Cell and Chemical Biology, Leiden University Medical Center, 2333 ZC Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4910-4655","authenticated-orcid":false,"given":"Vera","family":"Kemp","sequence":"additional","affiliation":[{"name":"Department of Cell and Chemical Biology, Leiden University Medical Center, 2333 ZC Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Iris J. C.","family":"Dautzenberg","sequence":"additional","affiliation":[{"name":"Department of Cell and Chemical Biology, Leiden University Medical Center, 2333 ZC Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9443-8377","authenticated-orcid":false,"given":"Rob C.","family":"Hoeben","sequence":"additional","affiliation":[{"name":"Department of Cell and Chemical Biology, Leiden University Medical Center, 2333 ZC Leiden, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"a013003","DOI":"10.1101\/cshperspect.a013003","article-title":"Adenovirus DNA replication","volume":"5","author":"Hoeben","year":"2013","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Khanal, S., Ghimire, P., and Dhamoon, A.S. (2018). The Repertoire of Adenovirus in Human Disease: The Innocuous to the Deadly. Biomedicines, 6.","DOI":"10.20944\/preprints201801.0267.v1"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"8263","DOI":"10.1128\/JVI.77.15.8263-8271.2003","article-title":"Replication-deficient human adenovirus type 35 vectors for gene transfer and vaccination: Efficient human cell infection and bypass of preexisting adenovirus immunity","volume":"77","author":"Vogels","year":"2003","journal-title":"J. Virol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1128\/AEM.01316-09","article-title":"Quantitative detection of human adenoviruses in wastewater and combined sewer overflows influencing a Michigan river","volume":"76","author":"Fong","year":"2010","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"570","DOI":"10.3181\/00379727-84-20714","article-title":"Isolation of a cytopathogenic agent from human adenoids undergoing spontaneous degeneration in tissue culture","volume":"84","author":"Rowe","year":"1953","journal-title":"Proc. Soc. Exp. Biol. Med."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1848","DOI":"10.1002\/1873-3468.13717","article-title":"Cell transformation by the adenovirus oncogenes E1 and E4","volume":"594","author":"Ip","year":"2020","journal-title":"FEBS Lett."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"200225","DOI":"10.1016\/j.tvr.2021.200225","article-title":"Almost famous: Human adenoviruses (and what they have taught us about cancer)","volume":"12","author":"Tessier","year":"2021","journal-title":"Tumour Virus Res."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1016\/j.coviro.2021.03.006","article-title":"Adenovirus\u2014A blueprint for gene delivery","volume":"48","author":"Greber","year":"2021","journal-title":"Curr. Opin. Virol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3660","DOI":"10.1002\/1873-3468.13687","article-title":"Adenoviruses across the animal kingdom: A walk in the zoo","volume":"593","author":"Harrach","year":"2019","journal-title":"FEBS Lett."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"5703","DOI":"10.1128\/JVI.00491-11","article-title":"Toward an integrated human adenovirus designation system that utilizes molecular and serological data and serves both clinical and fundamental virology","volume":"85","author":"Aoki","year":"2011","journal-title":"J. Virol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"5701","DOI":"10.1128\/JVI.00354-11","article-title":"Using the whole-genome sequence to characterize and name human adenoviruses","volume":"85","author":"Seto","year":"2011","journal-title":"J. Virol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1039","DOI":"10.1038\/s41598-018-37249-4","article-title":"Molecular Evolution of Human Adenovirus (HAdV) Species C","volume":"9","author":"Dhingra","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1099\/vir.0.83057-0","article-title":"Evidence of frequent recombination among human adenoviruses","volume":"89","author":"Lukashev","year":"2008","journal-title":"J. Gen. Virol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2182","DOI":"10.1038\/s41598-019-38719-z","article-title":"Recombination analysis of Human mastadenovirus C whole genomes","volume":"9","author":"Rivailler","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1016\/j.virol.2013.05.014","article-title":"Computational analysis of four human adenovirus type 4 genomes reveals molecular evolution through two interspecies recombination events","volume":"443","author":"Dehghan","year":"2013","journal-title":"Virology"},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Bots, S.T.F., and Hoeben, R.C. (2020). Non-Human Primate-Derived Adenoviruses for Future Use as Oncolytic Agents?. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21144821"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1604","DOI":"10.1099\/jgv.0.000465","article-title":"Genome analysis of four Old World monkey adenoviruses supports the proposed species classification of primate adenoviruses and reveals signs of possible homologous recombination","volume":"97","author":"Podgorski","year":"2016","journal-title":"J. Gen. Virol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2072","DOI":"10.1093\/molbev\/msv090","article-title":"Multiple Cross-Species Transmission Events of Human Adenoviruses (HAdV) during Hominine Evolution","volume":"32","author":"Hoppe","year":"2015","journal-title":"Mol. Biol. Evol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1006\/viro.2000.0350","article-title":"Circumvention of vector-specific neutralizing antibody response by alternating use of human and non-human adenoviruses: Implications in gene therapy","volume":"272","author":"Moffatt","year":"2000","journal-title":"Virology"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1089\/hum.2021.216","article-title":"Non-human primate adenoviruses of the Human Adenovirus B species are potent and broadly-acting oncolytic vector candidates","volume":"33","author":"Bots","year":"2022","journal-title":"Hum. Gene Ther."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"8270","DOI":"10.1128\/JVI.00048-07","article-title":"Phylogenetic analysis and structural predictions of human adenovirus penton proteins as a basis for tissue-specific adenovirus vector design","volume":"81","author":"Madisch","year":"2007","journal-title":"J. Virol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"380","DOI":"10.1016\/j.meegid.2018.08.020","article-title":"The possible origin of human adenovirus type 3: Evidence of natural genetic recombination between human and simian adenovirus","volume":"65","author":"Han","year":"2018","journal-title":"Infect. Genet. Evol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e00564-19","DOI":"10.1128\/JVI.00564-19","article-title":"A zoonotic adenoviral human pathogen emerged through genomic recombination among human and nonhuman simian hosts","volume":"93","author":"Dehghan","year":"2019","journal-title":"J. Virol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"73","DOI":"10.7589\/0090-3558-39.1.73","article-title":"Health evaluation of free-ranging and semi-captive orangutans (Pongo pygmaeus pygmaeus) in Sabah, Malaysia","volume":"39","author":"Kilbourn","year":"2003","journal-title":"J. Wildl. Dis."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Roy, S., Vandenberghe, L.H., Kryazhimskiy, S., Grant, R., Calcedo, R., Yuan, X., Keough, M., Sandhu, A., Wang, Q., and Medina-Jaszek, C.A. (2009). Isolation and characterization of adenoviruses persistently shed from the gastrointestinal tract of non-human primates. PLoS Pathog., 5.","DOI":"10.1371\/journal.ppat.1000503"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"6811","DOI":"10.1128\/jvi.68.10.6811-6814.1994","article-title":"Multiple adenovirus serotypes use alpha v integrins for infection","volume":"68","author":"Mathias","year":"1994","journal-title":"J. Virol."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Nemerow, G.R., and Stewart, P.L. (2016). Insights into Adenovirus Uncoating from Interactions with Integrins and Mediators of Host Immunity. Viruses, 8.","DOI":"10.3390\/v8120337"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"309","DOI":"10.1016\/0092-8674(93)90231-E","article-title":"Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment","volume":"73","author":"Wickham","year":"1993","journal-title":"Cell"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"11491","DOI":"10.1128\/JVI.01214-09","article-title":"Cryo-electron microscopy structure of an adenovirus-integrin complex indicates conformational changes in both penton base and integrin","volume":"83","author":"Lindert","year":"2009","journal-title":"J. Virol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"3165","DOI":"10.1007\/s00705-015-2575-z","article-title":"Taxonomy proposal for Old World monkey adenoviruses: Characterisation of several non-human, non-ape primate adenovirus lineages","volume":"160","author":"Panto","year":"2015","journal-title":"Arch. Virol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1073\/pnas.54.2.547","article-title":"Biochemical studies on adenovirus multiplication. IX. Chemical and base composition analysis of 28 human adenoviruses","volume":"54","author":"Pina","year":"1965","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1111\/cla.12422","article-title":"Genomics-based re-examination of the taxonomy and phylogeny of human and simian Mastadenoviruses: An evolving whole genomes approach, revealing putative zoonosis, anthroponosis, and amphizoonosis","volume":"36","author":"Kang","year":"2020","journal-title":"Cladistics"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1089\/hum.1996.7.2-215","article-title":"Characterization of 911: A new helper cell line for the titration and propagation of early region 1-deleted adenoviral vectors","volume":"7","author":"Fallaux","year":"1996","journal-title":"Hum. Gene Ther."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1160","DOI":"10.1093\/bib\/bbx108","article-title":"MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization","volume":"20","author":"Katoh","year":"2019","journal-title":"Brief. Bioinform."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1547","DOI":"10.1093\/molbev\/msy096","article-title":"MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms","volume":"35","author":"Kumar","year":"2018","journal-title":"Mol. Biol. Evol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1128\/JVI.73.1.152-160.1999","article-title":"Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination","volume":"73","author":"Lole","year":"1999","journal-title":"J. Virol."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Tu, S.L., Staheli, J.P., McClay, C., McLeod, K., Rose, T.M., and Upton, C. (2018). Base-By-Base Version 3: New Comparative Tools for Large Virus Genomes. Viruses, 10.","DOI":"10.3390\/v10110637"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/17\/9832\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:19:57Z","timestamp":1760141997000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/17\/9832"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,30]]},"references-count":37,"journal-issue":{"issue":"17","published-online":{"date-parts":[[2022,9]]}},"alternative-id":["ijms23179832"],"URL":"https:\/\/doi.org\/10.3390\/ijms23179832","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,30]]}}}