1887

Abstract

Bats carry diverse RNA viruses, some of which are responsible for human diseases. Compared to bat-borne RNA viruses, relatively little information is known regarding bat-borne DNA viruses. In this study, we isolated and characterized three novel bat adenoviruses (BtAdV WIV9–11) from . Their genomes, which are highly similar to each other but distinct from those of previously sequenced adenoviruses (AdVs), are 37 545, 37 566 and 38 073 bp in size, respectively. An unusually large E3 gene was identified in their genomes. Phylogenetic and taxonomic analyses suggested that these isolates represent a distinct species of the genus . Cell susceptibility assays revealed a broad cell tropism for these isolates, indicating that they have a potentially wide host range. Our results expand the understanding of genetic diversity of bat AdVs.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000470
2016-07-01
2019-12-14
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/7/1625.html?itemId=/content/journal/jgv/10.1099/jgv.0.000470&mimeType=html&fmt=ahah

References

  1. Anthony S. J., Epstein J. H., Murray K. A., Navarrete-Macias I., Zambrana-Torrelio C. M., Solovyov A., Ojeda-Flores R., Arrigo N. C., Islam A. et al. 2013; A strategy to estimate unknown viral diversity in mammals. MBio4:e0059800513 [CrossRef][PubMed]
    [Google Scholar]
  2. Appel M., Bistner S. I., Menegus M., Albert D. A., Carmichael L. E.. 1973; Pathogenicity of low-virulence strains of two canine adenovirus types. Am J Vet Res34:543–550[PubMed]
    [Google Scholar]
  3. Bahr U., Schöndorf E., Handermann M., Darai G.. 2003; Molecular anatomy of Tupaia (tree shrew) adenovirus genome; evolution of viral genes and viral phylogeny. Virus Genes27:29–48[PubMed][CrossRef]
    [Google Scholar]
  4. Baker K. S., Leggett R. M., Bexfield N. H., Alston M., Daly G., Todd S., Tachedjian M., Holmes C. E., Crameri S. et al. 2013; Metagenomic study of the viruses of african straw-coloured fruit bats: Detection of a chiropteran poxvirus and isolation of a novel adenovirus. Virology441:95–106[CrossRef]
    [Google Scholar]
  5. Benkö M., Harrach B.. 2003; Molecular evolution of adenoviruses. Curr Top Microbiol Immunol272:3–35[PubMed]
    [Google Scholar]
  6. Burgert H. G., Kvist S.. 1985; An adenovirus type 2 glycoprotein blocks cell surface expression of human histocompatibility class I antigens. Cell41:987–997 [CrossRef][PubMed]
    [Google Scholar]
  7. Burgert H. G., Maryanski J. L., Kvist S.. 1987; "E3/19K" protein of adenovirus type 2 inhibits lysis of cytolytic T lymphocytes by blocking cell-surface expression of histocompatibility class I antigens. Proc Natl Acad Sci U S A84:1356–1360[PubMed][CrossRef]
    [Google Scholar]
  8. Casas I., Vazquez-Moron S., Juste J., Falcon A., Aznar C., Ibanez C., Pozo F., Ruiz G., Berciano J. M. et al. 2010; Adenovirus groups in western Palaearctic bats in Spain GenBank Accession No: JX065117 to JX065129
    [Google Scholar]
  9. Chen L. H., Wu Z. Q., Hu Y. F., Yang F., Yang J., Jin Q.. 2012; [Genetic diversity of adenoviruses in bats of China]. Bing Du Xue Bao28:403–408[PubMed]
    [Google Scholar]
  10. Chua K. B., Bellini W. J., Rota P. A., Harcourt B. H., Tamin A., Lam S. K., Ksiazek T. G., Rollin P. E., Zaki S. R. et al. 2000; Nipah virus: a recently emergent deadly paramyxovirus. Science288:1432–1435 [CrossRef][PubMed]
    [Google Scholar]
  11. Corman V. M., Baldwin H. J., Tateno A. F., Zerbinati R. M., Annan A., Owusu M., Nkrumah E. E., Maganga G. D., Oppong S., other authors. 2015; Evidence for an ancestral association of human coronavirus 229E with Bats. J Virol89:11858–11870 [CrossRef][PubMed]
    [Google Scholar]
  12. Crameri G., Todd S., Grimley S., McEachern J. A., Marsh G. A., Smith C., Tachedjian M., De Jong C., Virtue E. R. et al. 2009; Establishment, immortalisation and characterisation of pteropid bat cell lines. PLoS One4:e8266 [CrossRef][PubMed]
    [Google Scholar]
  13. Dán A., Ruzsics Z., Russell W. C., Benkö M., Harrach B.. 1998; Analysis of the hexon gene sequence of bovine adenovirus type 4 provides further support for a new adenovirus genus (Atadenovirus). J Gen Virol79:1453–1460 [CrossRef][PubMed]
    [Google Scholar]
  14. Davison A. J., Wright K. M., Harrach B.. 2000; DNA sequence of frog adenovirus. J Gen Virol81:2431–2439 [CrossRef][PubMed]
    [Google Scholar]
  15. Davison A. J., Benko M., Harrach B.. 2003; Genetic content and evolution of adenoviruses. J Gen Virol84:2895–2908 [CrossRef][PubMed]
    [Google Scholar]
  16. De Jong J. C., Wermenbol A. G., Verweij-Uijterwaal M. W., Slaterus K. W., Wertheim-Van Dillen P., Van Doornum G. J., Khoo S. H., Hierholzer J. C.. 1999; Adenoviruses from human immunodeficiency virus-infected individuals, including two strains that represent new candidate serotypes Ad50 and Ad51 of species B1 and D, respectively. J Clin Microbiol37:3940–3945[PubMed]
    [Google Scholar]
  17. DeBey B. M., Lehmkuhl H. D., Chard-Bergstrom C., Hobbs L. A.. 2001; Ovine adenovirus serotype 7-associated mortality in lambs in the United States. Vet Pathol38:644–648 [CrossRef][PubMed]
    [Google Scholar]
  18. Deryckere F., Burgert H. G.. 1996; Early region 3 of adenovirus type 19 (subgroup D) encodes an hla-binding protein distinct from that of subgroups B and C. J Virol70:2832–2841[PubMed]
    [Google Scholar]
  19. Echavarría M.. 2008; Adenoviruses in immunocompromised hosts. Clin Microbiol Rev21:704–715 [CrossRef][PubMed]
    [Google Scholar]
  20. Elsing A., Burgert H. G.. 1998; The adenovirus E3/10.4K-14.5K proteins down-modulate the apoptosis receptor Fas/Apo-1 by inducing its internalization. Proc Natl Acad Sci U S A95:10072–10077 [CrossRef][PubMed]
    [Google Scholar]
  21. Farkas S. L., Harrach B., Benko M.. 2008; Completion of the genome analysis of snake adenovirus type 1, a representative of the reptilian lineage within the novel genus atadenovirus. Virus Res132:132–139 [CrossRef][PubMed]
    [Google Scholar]
  22. Fessler S. P., Delgado-Lopez F., Horwitz M. S.. 2004; Mechanisms of E3 modulation of immune and inflammatory responses. Curr Top Microbiol Immunol273:113–135 [CrossRef][PubMed]
    [Google Scholar]
  23. Frazer K. A., Pachter L., Poliakov A., Rubin E. M., Dubchak I.. 2004; VISTA: computational tools for comparative genomics. Nucleic Acids Res32:W273–W279 [CrossRef][PubMed]
    [Google Scholar]
  24. Frohman M. A., Dush M. K., Martin G. R.. 1988; Rapid production of full-length cDNAS from rare transcripts: Amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A85:8998–9002 [CrossRef][PubMed]
    [Google Scholar]
  25. Ge X. Y., Li J. L., Yang X. L., Chmura A. A., Zhu G., Epstein J. H., Mazet J. K., Hu B., Zhang W. et al. 2013; Isolation and characterization of a bat sars-like coronavirus that uses the ACE2 receptor. Nat New Biol503:535–538[CrossRef]
    [Google Scholar]
  26. Geisbert T. W., Bailey M., Hensley L., Asiedu C., Geisbert J., Stanley D., Honko A., Johnson J., Mulangu S., other authors. 2011; Recombinant adenovirus serotype 26 (Ad26) and Ad35 vaccine vectors bypass immunity to Ad5 and protect nonhuman primates against ebolavirus challenge. J Virol85:4222–4233 [CrossRef][PubMed]
    [Google Scholar]
  27. Ghebremedhin B.. 2014; Human adenovirus: Viral pathogen with increasing importance. Eur J Microbiol Immunol (Bp)4:26–33 [CrossRef]
    [Google Scholar]
  28. Gooding L. R., Elmore L. W., Tollefson A. E., Brady H. A., Wold W. S.. 1988; A 14,700 MW protein from the E3 region of adenovirus inhibits cytolysis by tumor necrosis factor. Cell53:341–346 [CrossRef][PubMed]
    [Google Scholar]
  29. Harrach B., Benkö M., Both G. W., Brown M., Davison A. J., Echavarría M., Hess M., Jones M. S., Kajon A. et al. 2011; Family Adenoviridae. In Virus Taxonomy Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses pp.125–141 Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J.. San Diego: Elsevier;
    [Google Scholar]
  30. Hemmi S., Vidovszky M. Z., Ruminska J., Ramelli S., Decurtins W., Greber U. F., Harrach B.. 2011; Genomic and phylogenetic analyses of murine adenovirus 2. Virus Res160:128–135 [CrossRef][PubMed]
    [Google Scholar]
  31. Hess M., Blöcker H., Brandt P., Blocker H.. 1997; The complete nucleotide sequence of the egg drop syndrome virus: An intermediate between mastadenoviruses and aviadenoviruses. Virology238:145–156 [CrossRef]
    [Google Scholar]
  32. Hofmayer S., Madisch I., Darr S., Rehren F., Heim A.. 2009; Unique sequence features of the human adenovirus 31 complete genomic sequence are conserved in clinical isolates. BMC Genomics10:557 [CrossRef]
    [Google Scholar]
  33. Horton T. M., Ranheim T. S., Aquino L., Kusher D. I., Saha S. K., Ware C. F., Wold W. S., Gooding L. R.. 1991; Adenovirus E3 14.7K protein functions in the absence of other adenovirus proteins to protect transfected cells from tumor necrosis factor cytolysis. J Virol65:2629–2639[PubMed]
    [Google Scholar]
  34. Hoşnut F. Ö., Özçay F., Malbora B., Hızlı S., Özbek N.. 2014; Severe adenovirus infection associated with hemophagocytic lymphohistiocytosis. Turk J Haematol31:103–105 [CrossRef][PubMed]
    [Google Scholar]
  35. Ishiko H., Shimada Y., Konno T., Hayashi A., Ohguchi T., Tagawa Y., Aoki K., Ohno S., Yamazaki S.. 2008; Novel human adenovirus causing nosocomial epidemic keratoconjunctivitis. J Clin Microbiol46:2002–2008 [CrossRef][PubMed]
    [Google Scholar]
  36. 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]
  37. Käll L., Krogh A., Sonnhammer E. L.. 2004; A combined transmembrane topology and signal peptide prediction method. J Mol Biol338:1027–1036 [CrossRef][PubMed]
    [Google Scholar]
  38. Kearse M., Moir R., Wilson A., Stones-Havas S., Cheung M., Sturrock S., Buxton S., Cooper A., Markowitz S. et al. 2012; Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics28:1647–1649 [CrossRef][PubMed]
    [Google Scholar]
  39. Kelley L. A., Mezulis S., Yates C. M., Wass M. N., Sternberg M. J.. 2015; The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc10:845–858 [CrossRef][PubMed]
    [Google Scholar]
  40. Kohl C., Vidovszky M. Z., Mühldorfer K., Dabrowski P. W., Radonić A., Nitsche A., Wibbelt G., Kurth A., Harrach B.. 2012; Genome analysis of bat adenovirus 2: Indications of interspecies transmission. J Virol86:1888–1892 [CrossRef][PubMed]
    [Google Scholar]
  41. 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]
  42. Kovács E. R., Jánoska M., Dán A., Harrach B., Benko M.. 2010; Recognition and partial genome characterization by non-specific DNA amplification and PCR of a new siadenovirus species in a sample originating from Parus major, a great tit. J Virol Methods163:262–268 [CrossRef][PubMed]
    [Google Scholar]
  43. Kovács G. M., LaPatra S. E., D'Halluin J. C., Benko M.. 2003; Phylogenetic analysis of the hexon and protease genes of a fish adenovirus isolated from white sturgeon (Acipenser transmontanus) supports the proposal for a new adenovirus genus. Virus Res98:27–34[PubMed][CrossRef]
    [Google Scholar]
  44. Kremer E. J., Boutin S., Chillon M., Danos O.. 2000; Canine adenovirus vectors: An alternative for adenovirus-mediated gene transfer. J Virol74:505–512[PubMed][CrossRef]
    [Google Scholar]
  45. Ledgerwood J. E., DeZure A. D., Stanley D. A., Novik L., Enama M. E., Berkowitz N. M., Hu Z., Joshi G., Ploquin A. et al. 2014; Chimpanzee adenovirus vector ebola vaccine - preliminary report. N Engl J Med [CrossRef][PubMed]
    [Google Scholar]
  46. Leroy E. M., Kumulungui B., Pourrut X., Rouquet P., Hassanin A., Yaba P., Délicat A., Paweska J. T., Gonzalez J. J. et al. 2005; Fruit bats as reservoirs of Ebola virus. Nat New Biol438:575–576[CrossRef]
    [Google Scholar]
  47. Lewis P. F., Schmidt M. A., Lu X., Erdman D. D., Campbell M., Thomas A., Cieslak P. R., Grenz L. D., Tsaknardis L. et al. 2009; A community-based outbreak of severe respiratory illness caused by human adenovirus serotype 14. J Infect Dis199:1427–1434 [CrossRef][PubMed]
    [Google Scholar]
  48. Li W., Shi Z., Yu M., Ren W., Smith C., Epstein J. H., Wang H., Crameri G., Hu Z. et al. 2005; Bats are natural reservoirs of SARS-like coronaviruses. Science310:676–679 [CrossRef][PubMed]
    [Google Scholar]
  49. Li Y., Ge X., Zhang H., Zhou P., Zhu Y., Zhang Y., Yuan J., Wang L. F., Shi Z.. 2010; Host range, prevalence, and genetic diversity of adenoviruses in bats. J Virol84:3889–3897 [CrossRef][PubMed]
    [Google Scholar]
  50. Lima F. E., Cibulski S. P., Elesbao F., Carnieli Junior P., Batista H. B., Roehe P. M., Franco A. C.. 2013; First detection of adenovirus in the vampire bat (Desmodus rotundus) in Brazil. Virus Genes47:378–381 [CrossRef][PubMed]
    [Google Scholar]
  51. Liu L., Qian Y., Zhang Y., Deng J., Jia L., Dong H.. 2014; Adenoviruses associated with acute diarrhea in children in Beijing, China. PLoS One9:e88791 [CrossRef][PubMed]
    [Google Scholar]
  52. Maeda K., Hondo E., Terakawa J., Kiso Y., Nakaichi N., Endoh D., Sakai K., Morikawa S., Mizutani T.. 2008; Isolation of novel adenovirus from fruit bat (Pteropus dasymallus yayeyamae). Emerg Infect Dis14:347–349 [CrossRef][PubMed]
    [Google Scholar]
  53. McSharry B. P., Burgert H. G., Owen D. P., Stanton R. J., Prod'homme V., Sester M., Koebernick K., Groh V., Spies T. et al. 2008; Adenovirus E3/19K promotes evasion of NK cell recognition by intracellular sequestration of the NKG2D ligands major histocompatibility complex class I chain-related proteins A and B. J Virol82:4585–4594 [CrossRef][PubMed]
    [Google Scholar]
  54. Nicklin S. A., Wu E., Nemerow G. R., Baker A. H.. 2005; The influence of adenovirus fiber structure and function on vector development for gene therapy. Mol Ther12:384–393 [CrossRef][PubMed]
    [Google Scholar]
  55. Parcell B. J., McIntyre P. G., Yirrell D. L., Fraser A., Quinn M., Templeton K., Christie S., Romanes F.. 2015; Prison and community outbreak of severe respiratory infection due to adenovirus type 14p1 in Tayside, UK. J Public Health (Oxf)37:64–69 [CrossRef][PubMed]
    [Google Scholar]
  56. Pauly M., Hoppe E., Mugisha L., Petrzelkova K., Akoua-Koffi C., Couacy-Hymann E., Anoh A. E., Mossoun A., Schubert G. et al. 2014; High prevalence and diversity of species D adenoviruses (HAdV-D) in human populations of four Sub-Saharan countries. Virol J11:25 [CrossRef][PubMed]
    [Google Scholar]
  57. Raut C. G., Yadav P. D., Towner J. S., Amman B. R., Erickson B. R., Cannon D. L., Sivaram A., Basu A., Nichol S. T. et al. 2012; Isolation of a novel adenovirus from Rousettus leschenaultii bats from India. Intervirology55:488–490 [CrossRef][PubMed]
    [Google Scholar]
  58. Reed L. J., Muench H.. 1938; A simple method of estimating fifty percent endpoints. Am J Epidemiol27:493–497
    [Google Scholar]
  59. Roberts D. M., Nanda A., Havenga M. J. E., Abbink P., Lynch D. M., Ewald B. A., Liu J., Thorner A. R., Swanson P. E. et al. 2006; Hexon-chimaeric adenovirus serotype 5 vectors circumvent pre-existing anti-vector immunity. Nat New Biol441:239–243[CrossRef]
    [Google Scholar]
  60. Rocholl C., Gerber K., Daly J., Pavia A. T., Byington C. L.. 2004; Adenoviral infections in children: the impact of rapid diagnosis. Pediatrics113:e5156 [CrossRef][PubMed]
    [Google Scholar]
  61. 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]
  62. Ryan M. A., Gray G. C., Smith B., McKeehan J. A., Hawksworth A. W., Malasig M. D.. 2002; Large epidemic of respiratory illness due to adenovirus types 7 and 3 in healthy young adults. Clin Infect Dis34:577–582 [CrossRef][PubMed]
    [Google Scholar]
  63. San Martín C., Burnett. R. M.. 2003; Structural studies on adenoviruses. Curr Top Microbiol Immunol272:57–94[PubMed]
    [Google Scholar]
  64. Sharma A., Li X., Bangari D. S., Mittal S. K.. 2009; Adenovirus receptors and their implications in gene delivery. Virus Res143:184–194 [CrossRef][PubMed]
    [Google Scholar]
  65. Shisler J., Yang C., Walter B., Ware C. F., Gooding L. R.. 1997; The adenovirus E3-10.4K/14.5K complex mediates loss of cell surface Fas (CD95) and resistance to Fas-induced apoptosis. J Virol71:8299–8306[PubMed]
    [Google Scholar]
  66. Simmons N. B.. 2005; Order Chiroptera. In Mammal Species of the World: A taxonomic and geographic reference pp.312–529 Edited by Wilson D. E., Reeder D. M.. Maryland: Johns Hopkins University Press;
    [Google Scholar]
  67. Sonntag M., Mühldorfer K., Speck S., Wibbelt G., Kurth A.. 2009; New adenovirus in bats, Germany. Emerg Infect Dis15:2052–2055 [CrossRef][PubMed]
    [Google Scholar]
  68. Stewart A. R., Tollefson A. E., Krajcsi P., Yei S. P., Wold W. S.. 1995; The adenovirus E3 10.4K and 14.5K proteins, which function to prevent cytolysis by tumor necrosis factor and to down-regulate the epidermal growth factor receptor, are localized in the plasma membrane. J Virol69:172–181[PubMed]
    [Google Scholar]
  69. Swango L. J., Wooding W. L. Jr, Binn L. N.. 1970; A comparison of the pathogenesis and antigenicity of infectious canine hepatitis virus and the A26-61 virus strain (toronto). J Am Vet Med Assoc156:1687–1696[PubMed]
    [Google Scholar]
  70. Thomas M. A., Lichtenstein D. L., Krajcsi P., Wold W. S.. 2007; A real-time PCR method to rapidly titer adenovirus stocks. Methods Mol Med130:185–192[PubMed]
    [Google Scholar]
  71. Uchino J., Curiel D. T., Ugai H.. 2014; Species D human adenovirus type 9 exhibits better virus-spread ability for antitumor efficacy among alternative serotypes. PLoS One9:e87342 [CrossRef][PubMed]
    [Google Scholar]
  72. Ursu K., Harrach B., Matiz K., Benko M.. 2004; DNA sequencing and analysis of the right-hand part of the genome of the unique bovine adenovirus type 10. J Gen Virol85:593–601 [CrossRef][PubMed]
    [Google Scholar]
  73. 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]
  74. Wang L. F., Walker P. J., Poon L. L.. 2011; Mass extinctions, biodiversity and mitochondrial function: are bats 'special' as reservoirs for emerging viruses?. Curr Opin Virol1:649–657 [CrossRef][PubMed]
    [Google Scholar]
  75. 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]
  76. Windheim M., Southcombe J. H., Kremmer E., Chaplin L., Urlaub D., Falk C. S., Claus M., Mihm J., Braithwaite M. et al. 2013; A unique secreted adenovirus E3 protein binds to the leukocyte common antigen CD45 and modulates leukocyte functions. Proc Natl Acad Sci U S A110:E4884E4893 [CrossRef][PubMed]
    [Google Scholar]
  77. Wu L., Zhou P., Ge X., Wang L. F., Baker M. L., Shi Z.. 2013; Deep RNA sequencing reveals complex transcriptional landscape of a bat adenovirus. J Virol87:503–511 [CrossRef][PubMed]
    [Google Scholar]
  78. Ye W., Liu R., Pan C., Jiang W., Zhang L., Guan Z., Wu J., Ying X., Li L.. 2014; Multicenter randomized phase 2 clinical trial of a recombinant human endostatin adenovirus in patients with advanced head and neck carcinoma. Mol Ther22:1221–1229 [CrossRef][PubMed]
    [Google Scholar]
  79. Yang X. L., Tan B., Wang B., Li W., Wang N., Luo C. M., Wang M. N., Zhang W., Li B. et al. 2015; Isolation and identification of bat viruses closely related to human, porcine and mink orthoreoviruses. J Gen Virol96:3525–3531 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000470
Loading
/content/journal/jgv/10.1099/jgv.0.000470
Loading

Data & Media loading...

Most Cited This Month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error