1887

Abstract

Bats are increasingly being recognized as important natural reservoirs of different viruses. Adeno-associated viruses (AAVs) are widely distributed in primates and their distribution in bats is unknown. In this study, a total of 370 faecal swab samples from 19 bat species were collected from various provinces of China and examined for the presence of AAVs. The mean prevalence rate was 22.4 % (83 positives out of 370 samples), ranging from 10 to 38.9 % among different bat species. The genome sequence spanning the entire ORFs was determined from one chosen AAV-positive sample (designated BtAAV-YNM). Phylogenetic analysis of the entire ORF coding sequences suggested that BtAAV-YNM is relatively distant to known primate AAVs, but phylogenetically closer to porcine AAV strain Po3. Further analysis of the partial ORF sequences of bat AAV samples (=49) revealed a remarkably large genetic diversity, with an average pairwise nucleotide identity of only 84.3 %. Co-presence of multiple distinctive genotypes of bat AAV within an individual sample was also observed. These results demonstrated that diverse AAVs might be widely distributed in bat populations.

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2010-10-01
2019-11-18
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References

  1. Altringham, J. D., McOwat, T. & Hammond, L. ( 1996; ). The Evolution and Diversity of Bats. Bats: Biology and Behaviour. London, UK. : Oxford University Press.
    [Google Scholar]
  2. Arbetman, A. E., Lochrie, M., Zhou, S., Wellman, J., Scallan, C., Doroudchi, M. M., Randlev, B., Patarroyo-White, S., Liu, T. & other authors ( 2005; ). Novel caprine adeno-associated virus (AAV) capsid (AAV-Go.1) is closely related to the primate AAV-5 and has unique tropism and neutralization properties. J Virol 79, 15238–15245.[CrossRef]
    [Google Scholar]
  3. Atchison, R. W., Casto, B. C. & Hammon, W. M. ( 1965; ). Adenovirus-associated defective virus particles. Science 149, 754–756.[CrossRef]
    [Google Scholar]
  4. Bantel-Schaal, U. & zur Hausen, H. ( 1984; ). Characterization of the DNA of a defective human parvovirus isolated from a genital site. Virology 134, 52–63.[CrossRef]
    [Google Scholar]
  5. Bauer, H. J. & Monreal, G. ( 1986; ). Herpesviruses provide helper functions for avian adeno-associated parvovirus. J Gen Virol 67, 181–185.[CrossRef]
    [Google Scholar]
  6. Bello, A., Tran, K., Chand, A., Doria, M., Allocca, M., Hildinger, M., Beniac, D., Kranendonk, C., Auricchio, A. & other authors ( 2009; ). Isolation and evaluation of novel adeno-associated virus sequences from porcine tissues. Gene Ther 16, 1320–1328.[CrossRef]
    [Google Scholar]
  7. Bossis, I. & Chiorini, J. A. ( 2003; ). Cloning of an avian adeno-associated virus (AAAV) and generation of recombinant AAAV particles. J Virol 77, 6799–6810.[CrossRef]
    [Google Scholar]
  8. Brown, K. E., Green, S. W. & Young, N. S. ( 1995; ). Goose parvovirus – an autonomous member of the Dependovirus genus? Virology 210, 283–291.[CrossRef]
    [Google Scholar]
  9. Chiorini, J. A., Yang, L., Liu, Y., Safer, B. & Kotin, R. M. ( 1997; ). Cloning of adeno-associated virus type 4 (AAV4) and generation of recombinant AAV4 particles. J Virol 71, 6823–6833.
    [Google Scholar]
  10. Chiorini, J. A., Kim, F., Yang, L. & Kotin, R. M. ( 1999; ). Cloning and characterization of adeno-associated virus type 5. J Virol 73, 1309–1319.
    [Google Scholar]
  11. Drummond, A. J. & Rambaut, A. ( 2007; ). beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7, 214.[CrossRef]
    [Google Scholar]
  12. Drummond, A. J., Rambaut, A., Shapiro, B. & Pybus, O. G. ( 2005; ). Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22, 1185–1192.[CrossRef]
    [Google Scholar]
  13. Drummond, A. J., Ho, S. Y., Phillips, M. J. & Rambaut, A. ( 2006; ). Relaxed phylogenetics and dating with confidence. PLoS Biol 4, e88.[CrossRef]
    [Google Scholar]
  14. Eaton, B. T., Broder, C. C. & Wang, L. F. ( 2005; ). Hendra and Nipah viruses: pathogenesis and therapeutics. Curr Mol Med 5, 805–816.[CrossRef]
    [Google Scholar]
  15. Edgar, R. C. ( 2004; ). muscle: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5, 113.[CrossRef]
    [Google Scholar]
  16. Farkas, S. L., Zadori, Z., Benko, M., Essbauer, S., Harrach, B. & Tijssen, P. ( 2004; ). A parvovirus isolated from royal python (Python regius) is a member of the genus Dependovirus. J Gen Virol 85, 555–561.[CrossRef]
    [Google Scholar]
  17. Gao, G. P., Alvira, M. R., Wang, L., Calcedo, R., Johnston, J. & Wilson, J. M. ( 2002; ). Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc Natl Acad Sci U S A 99, 11854–11859.[CrossRef]
    [Google Scholar]
  18. Gao, G., Alvira, M. R., Somanathan, S., Lu, Y., Vandenberghe, L. H., Rux, J. J., Calcedo, R., Sanmiguel, J., Abbas, Z. & Wilson, J. M. ( 2003; ). Adeno-associated viruses undergo substantial evolution in primates during natural infections. Proc Natl Acad Sci U S A 100, 6081–6086.[CrossRef]
    [Google Scholar]
  19. Gao, G., Vandenberghe, L. H., Alvira, M. R., Lu, Y., Calcedo, R., Zhou, X. & Wilson, J. M. ( 2004; ). Clades of adeno-associated viruses are widely disseminated in human tissues. J Virol 78, 6381–6388.[CrossRef]
    [Google Scholar]
  20. Goncalves, M. A. ( 2005; ). Adeno-associated virus: from defective virus to effective vector. Virol J 2, 43.[CrossRef]
    [Google Scholar]
  21. Grieger, J. C. & Samulski, R. J. ( 2005; ). Adeno-associated virus as a gene therapy vector: vector development, production and clinical applications. Adv Biochem Eng Biotechnol 99, 119–145.
    [Google Scholar]
  22. Guindon, S. & Gascuel, O. ( 2003; ). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52, 696–704.[CrossRef]
    [Google Scholar]
  23. Hess, M., Paul, G., Kling, S. & Monreal, G. ( 1995; ). Molecular characterization of two strains of the avian adeno-associated virus (AAAV). Arch Virol 140, 591–598.[CrossRef]
    [Google Scholar]
  24. Hoggan, M. D., Blacklow, N. R. & Rowe, W. P. ( 1966; ). Studies of small DNA viruses found in various adenovirus preparations: physical, biological, and immunological characteristics. Proc Natl Acad Sci U S A 55, 1467–1474.[CrossRef]
    [Google Scholar]
  25. Kumar, S., Tamura, K. & Nei, M. ( 2004; ). mega3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5, 150–163.[CrossRef]
    [Google Scholar]
  26. Lau, S. K., Woo, P. C., Li, K. S., Huang, Y., Tsoi, H. W., Wong, B. H., Wong, S. S., Leung, S. Y., Chan, K. H. & Yuen, K. Y. ( 2005; ). Severe acute respiratory syndrome coronavirus-like virus in Chinese horseshoe bats. Proc Natl Acad Sci U S A 102, 14040–14045.[CrossRef]
    [Google Scholar]
  27. Leroy, E. M., Kumulungui, B., Pourrut, X., Rouquet, P., Hassanin, A., Yaba, P., Delicat, A., Paweska, J. T., Gonzalez, J. P. & Swanepoel, R. ( 2005; ). Fruit bats as reservoirs of Ebola virus. Nature 438, 575–576.[CrossRef]
    [Google Scholar]
  28. Li, W., Shi, Z., Yu, M., Ren, W., Smith, C., Epstein, J. H., Wang, H., Crameri, G., Hu, Z. & other authors ( 2005; ). Bats are natural reservoirs of SARS-like coronaviruses. Science 310, 676–679.[CrossRef]
    [Google Scholar]
  29. 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 Virol 84, 3889–3897.[CrossRef]
    [Google Scholar]
  30. 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 Dis 14, 347–349.[CrossRef]
    [Google Scholar]
  31. Martin, D. P., Williamson, C. & Posada, D. ( 2005; ). rdp2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260–262.[CrossRef]
    [Google Scholar]
  32. Melnick, J. L., Mayor, H. D., Smith, K. & Rapp, F. ( 1965; ). Association of 20-millimicron particles with adenoviruses. J Bacteriol 90, 271–274.
    [Google Scholar]
  33. Molnar, V., Janoska, M., Harrach, B., Glavits, R., Palmai, N., Rigo, D., Sos, E. & Liptovszky, M. ( 2008; ). Detection of a novel bat gammaherpesvirus in Hungary. Acta Vet Hung 56, 529–538.[CrossRef]
    [Google Scholar]
  34. Mori, S., Wang, L., Takeuchi, T. & Kanda, T. ( 2004; ). Two novel adeno-associated viruses from cynomolgus monkey: pseudotyping characterization of capsid protein. Virology 330, 375–383.[CrossRef]
    [Google Scholar]
  35. Muzyczka, N. & Berns, K. I. ( 2001; ). Parvoviridae: the viruses and their replication. In Fields Virology, 4th edn, pp. 2327–2360. Edited by Knipe, D. M. & Howley, P. M.. Philadelphia, PA. : Lippincott, Williams & Wilkins.
    [Google Scholar]
  36. Rutledge, E. A., Halbert, C. L. & Russell, D. W. ( 1998; ). Infectious clones and vectors derived from adeno-associated virus (AAV) serotypes other than AAV type 2. J Virol 72, 309–319.
    [Google Scholar]
  37. Samulski, R. J., Berns, K. I., Tan, M. & Muzyczka, N. ( 1982; ). Cloning of adeno-associated virus into pBR322: rescue of intact virus from the recombinant plasmid in human cells. Proc Natl Acad Sci U S A 79, 2077–2081.[CrossRef]
    [Google Scholar]
  38. Schlehofer, J. R., Heilbronn, R., Georg-Fries, B. & zur Hausen, H. ( 1983; ). Inhibition of initiator-induced SV40 gene amplification in SV40-transformed Chinese hamster cells by infection with a defective parvovirus. Int J Cancer 32, 591–595.[CrossRef]
    [Google Scholar]
  39. Schlehofer, J. R., Ehrbar, M. & zur Hausen, H. ( 1986; ). Vaccinia virus, herpes simplex virus, and carcinogens induce DNA amplification in a human cell line and support replication of a helpervirus dependent parvovirus. Virology 152, 110–117.[CrossRef]
    [Google Scholar]
  40. Schmidt, M., Katano, H., Bossis, I. & Chiorini, J. A. ( 2004; ). Cloning and characterization of a bovine adeno-associated virus. J Virol 78, 6509–6516.[CrossRef]
    [Google Scholar]
  41. Schmidt, M., Grot, E., Cervenka, P., Wainer, S., Buck, C. & Chiorini, J. A. ( 2006; ). Identification and characterization of novel adeno-associated virus isolates in ATCC virus stocks. J Virol 80, 5082–5085.[CrossRef]
    [Google Scholar]
  42. Schmidt, M., Voutetakis, A., Afione, S., Zheng, C., Mandikian, D. & Chiorini, J. A. ( 2008; ). Adeno-associated virus type 12 (AAV12): a novel AAV serotype with sialic acid- and heparan sulfate proteoglycan-independent transduction activity. J Virol 82, 1399–1406.[CrossRef]
    [Google Scholar]
  43. Schnepp, B. C., Jensen, R. L., Chen, C. L., Johnson, P. R. & Clark, K. R. ( 2005; ). Characterization of adeno-associated virus genomes isolated from human tissues. J Virol 79, 14793–14803.[CrossRef]
    [Google Scholar]
  44. Schnepp, B. C., Jensen, R. L., Clark, K. R. & Johnson, P. R. ( 2009; ). Infectious molecular clones of adeno-associated virus isolated directly from human tissues. J Virol 83, 1456–1464.[CrossRef]
    [Google Scholar]
  45. Shapiro, B., Rambaut, A. & Drummond, A. J. ( 2006; ). Choosing appropriate substitution models for the phylogenetic analysis of protein-coding sequences. Mol Biol Evol 23, 7–9.
    [Google Scholar]
  46. Takeuchi, Y., Myers, R. & Danos, O. ( 2008; ). Recombination and population mosaic of a multifunctional viral gene, adeno-associated virus cap. PLoS One 3, e1634.[CrossRef]
    [Google Scholar]
  47. Towner, J. S., Pourrut, X., Albarino, C. G., Nkogue, C. N., Bird, B. H., Grard, G., Ksiazek, T. G., Gonzalez, J. P., Nichol, S. T. & Leroy, E. M. ( 2007; ). Marburg virus infection detected in a common African bat. PLoS ONE 2, e764.[CrossRef]
    [Google Scholar]
  48. Wibbelt, G., Kurth, A., Yasmum, N., Bannert, M., Nagel, S., Nitsche, A. & Ehlers, B. ( 2007; ). Discovery of herpesviruses in bats. J Gen Virol 88, 2651–2655.[CrossRef]
    [Google Scholar]
  49. Wong, S., Lau, S., Woo, P. & Yuen, K. Y. ( 2007; ). Bats as a continuing source of emerging infections in humans. Rev Med Virol 17, 67–91.[CrossRef]
    [Google Scholar]
  50. Wu, Z., Asokan, A. & Samulski, R. J. ( 2006; ). Adeno-associated virus serotypes: vector toolkit for human gene therapy. Mol Ther 14, 316–327.[CrossRef]
    [Google Scholar]
  51. Yakobson, B., Koch, T. & Winocour, E. ( 1987; ). Replication of adeno-associated virus in synchronized cells without the addition of a helper virus. J Virol 61, 972–981.
    [Google Scholar]
  52. Yalkinoglu, A. O., Heilbronn, R., Burkle, A., Schlehofer, J. R. & zur Hausen, H. ( 1988; ). DNA amplification of adeno-associated virus as a response to cellular genotoxic stress. Cancer Res 48, 3123–3129.
    [Google Scholar]
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Supplements

vol. , part 10, pp. 2601 - 2609

Similarity of Rep and Cap proteins between BtAAV-YNM and other AAVs

Similarity plot of genomes between BtAAV-YNM and other AAVs

Large-scale maximum-likelihood (ML) phylogeny of all available and relevant AAVs [Single PDF file](251 KB)



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