1887

Abstract

Within the family Adenoviridae, presently is the single species approved officially for monkey adenoviruses (AdVs), whilst the establishment of six further species ( to Simian mastadenovirus G) has been proposed in the last few years. We examined the genetic content and phylogenetic relationships of four Old World monkey (OWM) AdV types [namely simian AdV (SAdV)-8, -11, -16 and -19] for which it had been proposed that they should be classified into different AdV species: SAdV-11 to , and the other three viruses into three novel species. By full genome sequencing, we identified gene contents characteristic for the genus . Among the 36 ORFs, 2 genes of different lengths, predicted to encode the adenoviral cellular attachment protein (the fibre), were found. The E3 regions contained six genes, present in every OWM AdV, but lacked the E3 19K gene, which has seemingly appeared only in the ape (hominid) AdV lineages during evolution. For the first time in SAdVs, two other exons belonging to the gene of the so-called U exon protein were also predicted. Phylogenetic calculations, based on the fibre-1 and the major capsid protein, the hexon, implied that recombination events might have happened between different AdV species. Phylogeny inference, based on the viral DNA-dependent DNA polymerase and the penton base protein, further supported the species classification proposed earlier.

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2016-07-01
2019-12-12
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References

  1. Alonso-Padilla J., Papp T., Kaján G. L., Benkö M., Havenga M., Lemckert A., Harrach B., Baker A. H.. 2016; Development of novel adenoviral vectors to overcome challenges observed with HAdV-5-based constructs. Mol Ther24:6––16 [CrossRef][PubMed]
    [Google Scholar]
  2. Benkö M.. 2015; Adenoviruses: pathogenesis. In Reference Module in Biomedical Sciences. Amsterdam:: Elsevier;
    [Google Scholar]
  3. Benkö M., Harrach B., Kremer E. J.. 2014; Do nonhuman primate or bat adenoviruses pose a risk for human health?. Future Microbiol9:269–272 [CrossRef][PubMed]
    [Google Scholar]
  4. Berriman M., Rutherford K.. 2003; Viewing and annotating sequence data with Artemis. Brief Bioinform4:124–132 [CrossRef][PubMed]
    [Google Scholar]
  5. Chiu C. Y., Yagi S., Lu X., Yu G., Chen E. C., Liu M., Dick E. J., Carey K. D., Erdman D. D., other authors. 2013; A novel adenovirus species associated with an acute respiratory outbreak in a baboon colony and evidence of coincident human infection. MBio4:e0008413 [CrossRef][PubMed]
    [Google Scholar]
  6. Crawford-Miksza L. K., Schnurr D. P.. 1996; Adenovirus serotype evolution is driven by illegitimate recombination in the hypervariable regions of the hexon protein. Virol224:357–367 [CrossRef]
    [Google Scholar]
  7. Davison A. J., Telford E. A., Watson M. S., McBride K., Mautner V.. 1993; The DNA sequence of adenovirus type 40. J Mol Biol234:1308–1316 [CrossRef][PubMed]
    [Google Scholar]
  8. Dehghan S., Seto J., Jones M. S., Dyer D. W., Chodosh J., Seto D.. 2013a; Simian adenovirus type 35 has a recombinant genome comprising human and simian adenovirus sequences, which predicts its potential emergence as a human respiratory pathogen. Virology447:265–273 [CrossRef]
    [Google Scholar]
  9. Dehghan S., Seto J., Liu E. B., Walsh M. P., Dyer D. W., Chodosh J., Seto D.. 2013b; Computational analysis of four human adenovirus type 4 genomes reveals molecular evolution through two interspecies recombination events. Virol443:197–207 [CrossRef]
    [Google Scholar]
  10. Doszpoly A., Wellehan J. F., Childress A. L., Tarján Z. L., Kovács E. R., Harrach B., Benk M., Tarjan Z.. 2013; Partial characterization of a new adenovirus lineage discovered in testudinoid turtles. Infect Genet Evol17:106–112 [CrossRef][PubMed]
    [Google Scholar]
  11. Harrach B.. 2014; Adenoviruses: general features. In Reference Module in Biomedical Sciences. Amsterdam:: Elsevier; [CrossRef]
    [Google Scholar]
  12. Hull R. N., Minner J. R., Smith J. W.. 1956; New viral agents recovered from tissue cultures of monkey kidney cells. I. Origin and properties of cytopathogenic agents S.V.1, S.V.2, S.V.4, S.V.5, S.V.6, S.V.11, S.V.12 and S.V.15. Am J Hyg63:204–215[PubMed]
    [Google Scholar]
  13. Jones M. S., Harrach B., Ganac R. D., Gozum M. M., Dela Cruz W. P., Riedel B., Pan C., Delwart E. L., Schnurr D. P.. 2007; New adenovirus species found in a patient presenting with gastroenteritis. J Virol81:5978–5984 [CrossRef][PubMed]
    [Google Scholar]
  14. Kaján G. L., Stefancsik R., Ursu K., Palya V., Benkö M.. 2010; The first complete genome sequence of a non-chicken aviadenovirus, proposed to be turkey adenovirus 1. Virus Res153:226–233 [CrossRef][PubMed]
    [Google Scholar]
  15. Kaján G. L., Davison A. J., Palya V., Harrach B., Benkö M.. 2012; Genome sequence of a waterfowl aviadenovirus, goose adenovirus 4. J Gen Virol93:2457–2465[CrossRef]
    [Google Scholar]
  16. Kidd A. H., Garwicz D., Öberg M.. 1995; Human and simian adenoviruses: phylogenetic inferences from analysis of VA RNA genes. Virol207:32–45 [CrossRef]
    [Google Scholar]
  17. Kiss I., Matiz K., Allard A., Wadell G., Benkö M.. 1996; Detection of homologous DNA sequences in animal adenoviruses by polymerase chain reaction. Acta Vet Hung44:243–251[PubMed]
    [Google Scholar]
  18. Kovács E. R., Benko M.. 2009; Confirmation of a novel siadenovirus species detected in raptors: partial sequence and phylogenetic analysis. Virus Res140:64–70 [CrossRef][PubMed]
    [Google Scholar]
  19. Kovács G. M., Davison A. J., Zakhartchouk A. N., Harrach B.. 2004; Analysis of the first complete genome sequence of an Old World monkey adenovirus reveals a lineage distinct from the six human adenovirus species. J Gen Virol85:2799–2807 [CrossRef][PubMed]
    [Google Scholar]
  20. Kovács G. M., Harrach B., Zakhartchouk A. N., Davison A. J.. 2005; Complete genome sequence of simian adenovirus 1: an Old World monkey adenovirus with two fiber genes. J Gen Virol86:1681–1686 [CrossRef][PubMed]
    [Google Scholar]
  21. Larsson S., Svensson C., Akusjärvi G.. 1986; Characterization of a low-molecular-weight virus-associated (VA) RNA encoded by simian adenovirus type 7 which functionally can substitute for adenovirus type 5 VA RNAI. J Virol60:635–644[PubMed]
    [Google Scholar]
  22. Lole K. S., Bollinger R. C., Paranjape R. S., Gadkari D., Kulkarni S. S., Novak N. G., Ingersoll R., Sheppard H. W., Ray S. C.. 1999; Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol73:152–160[PubMed]
    [Google Scholar]
  23. Lopez-Gordo E., Podgorski I. I., Downes N., Alemany R.. 2014; Circumventing antivector immunity: potential use of nonhuman adenoviral vectors. Hum Gene Ther25:285–300 [CrossRef][PubMed]
    [Google Scholar]
  24. Malouli D., Howell G. L., Legasse A. W., Kahl C., Axthelm M. K., Hansen S. G., Früh K.. 2014; Full genome sequence analysis of a novel adenovirus of rhesus macaque origin indicates a new simian adenovirus type and species. Virol Rep3–4:18–29 [CrossRef][PubMed]
    [Google Scholar]
  25. Marek A., Kosiol C., Harrach B., Kaján G. L., Schlötterer C., Hess M.. 2013; The first whole genome sequence of a fowl adenovirus B strain enables interspecies comparisons within the genus adenovirus. Vet Microbiol166:250–256 [CrossRef][PubMed]
    [Google Scholar]
  26. Marek A., Ballmann M. Z., Kosiol C., Harrach B., Hess M., Schlötterer C.. 2014a; Whole-genome sequences of two turkey adenovirus types reveal the existence of two unknown lineages that merit the establishment of novel species within the genus aviadenovirus. J Gen Virol95:156–170 [CrossRef]
    [Google Scholar]
  27. Marek A., Kaján G. L., Kosiol C., Harrach B., Schlötterer C., Hess M.. 2014b; Complete genome sequences of pigeon adenovirus 1 and duck adenovirus 2 extend the number of species within the genus aviadenovirus. Virol462–463:107–114 [CrossRef]
    [Google Scholar]
  28. Pantó L., Podgorski I. I., Jánoska M., Márkó O., Harrach B.. 2015; Taxonomy proposal for Old World monkey adenoviruses: characterisation of several non-human, non-ape primate adenovirus lineages. Arch Virol160:3165–3177 [CrossRef][PubMed]
    [Google Scholar]
  29. Pénzes J. J., Menéndez-Conejero R., Condezo G. N., Ball I., Papp T., Doszpoly A., Paradela A., Pérez-Berná A. J., López-Sanz M., other authors. 2014; Molecular characterization of a lizard adenovirus reveals the first atadenovirus with two fiber genes and the first adenovirus with either one short or three long fibers per penton. J Virol88:11304–11314 [CrossRef][PubMed]
    [Google Scholar]
  30. Pring-Akerblom P., Trijssenaar F. E. J., Adrian T.. 1995; Sequence characterization and comparison of human adenovirus subgenus B and E hexons. Virol212:232–236 [CrossRef]
    [Google Scholar]
  31. Rapoza N. P.. 1967; A classification of simian adenoviruses based on hemagglutination. Am J Epidemiol86:736–745[PubMed]
    [Google Scholar]
  32. Roy S., Vandenberghe L. H., Kryazhimskiy S., Grant R., Calcedo R., Yuan X., Keough M., Sandhu A., Wang Q., other authors. 2009; Isolation and characterization of adenoviruses persistently shed from the gastrointestinal tract of non-human primates. PLoS Pathog5:e1000503 [CrossRef][PubMed]
    [Google Scholar]
  33. Roy S., Clawson D. S., Adam V. S., Medina A., Wilson J. M.. 2011; Construction of gene transfer vectors based on simian adenovirus 7. J Gen Virol92:1749–1753 [CrossRef][PubMed]
    [Google Scholar]
  34. Roy S., Sandhu A., Medina A., Clawson D. S., Wilson J. M.. 2012; Adenoviruses in fecal samples from asymptomatic rhesus macaques, United States. Emerg Infect Dis18:1081–1088 [CrossRef][PubMed]
    [Google Scholar]
  35. Tarján Z. L., Pénzes J. J., Tóth R. P., Benkö M.. 2014; First detection of circovirus-like sequences in amphibians and novel putative circoviruses in fishes. Acta Vet Hung62:134–144 [CrossRef][PubMed]
    [Google Scholar]
  36. To K. K., Tse H., Chan W. M., Choi G. K., Zhang A. J., Sridhar S., Wong S. C., Chan J. F., Chan A. S., other authors. 2014; A novel psittacine adenovirus identified during an outbreak of avian chlamydiosis and human psittacosis: zoonosis associated with virus-bacterium coinfection in birds. PLoS Negl Trop Dis8:e3318 [CrossRef][PubMed]
    [Google Scholar]
  37. Tollefson A. E., Ying B., Doronin K., Sidor P. D., Wold W. S.. 2007; Identification of a new human adenovirus protein encoded by a novel late l-strand transcription unit. J Virol81:12918–12926 [CrossRef][PubMed]
    [Google Scholar]
  38. Vidovszky M., Kohl C., Boldogh S., Görföl T., Wibbelt G., Kurth A., Harrach B.. 2015; Random sampling of the central European bat fauna reveals the existence of numerous hitherto unknown adenoviruses. Acta Vet Hung63:508–525 [CrossRef][PubMed]
    [Google Scholar]
  39. Walsh M. P., Seto J., Liu E. B., Dehghan S., Hudson N. R., Lukashev A. N., Ivanova O., Chodosh J., Dyer D. W., other authors. 2011; Computational analysis of two species C human adenoviruses provides evidence of a novel virus. J Clin Microbiol49:3482–3490 [CrossRef][PubMed]
    [Google Scholar]
  40. Wellehan J. F., Johnson A. J., Harrach B., Benkö M., Pessier A. P., Johnson C. M., Garner M. M., Childress A., Jacobson E. R.. 2004; Detection and analysis of six lizard adenoviruses by consensus primer PCR provides further evidence of a reptilian origin for the atadenoviruses. J Virol78:13366–13369 [CrossRef][PubMed]
    [Google Scholar]
  41. Zhao J., Zhong Q., Zhao Y., Hu Y. X., Zhang G. Z.. 2015; Pathogenicity and complete genome characterization of fowl adenoviruses isolated from chickens associated with inclusion body hepatitis and hydropericardium syndrome in China. PLoS One10:e0133073 [CrossRef][PubMed]
    [Google Scholar]
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