1887

Abstract

Parvoviruses are small single-stranded DNA viruses that are ubiquitous in nature. Infections with both autonomous and helper-virus dependent parvoviruses are common in both human and animal populations, and many animals are host to a number of different parvoviral species. Despite the epidemiological importance of parvoviruses, the presence and role of genome recombination within or among parvoviral species has not been well characterized. Here we show that natural recombination may be widespread in these viruses. Different genome regions of both porcine parvoviruses and Aleutian mink disease viruses have conflicting phylogenetic histories, providing evidence for recombination within each of these two species. Further, the rodent parvoviruses show complex evolutionary histories for separate genomic regions, suggesting recombination at the interspecies level.

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2007-12-01
2019-11-12
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References

  1. Alexandersen, S., Bloom, M. E. & Wolfinbarger, J. ( 1988; ). Evidence of restricted viral replication in adult mink infected with Aleutian disease of mink parvovirus. J Virol 62, 1495–1507.
    [Google Scholar]
  2. Allen, J. M., Debelak, D. J., Reynolds, T. C. & Miller, A. D. ( 1997; ). Identification and elimination of replication-competent adeno-associated virus (AAV) that can arise by nonhomologous recombination during AAV vector production. J Virol 71, 6816–6822.
    [Google Scholar]
  3. Awadalla, P. ( 2003; ). The evolutionary genomics of pathogen recombination. Nat Rev Genet 4, 50–60.[CrossRef]
    [Google Scholar]
  4. Badgett, M. R., Auer, A., Carmichael, L. E., Parrish, C. R. & Bull, J. J. ( 2002; ). Evolutionary dynamics of viral attenuation. J Virol 76, 10524–10529.[CrossRef]
    [Google Scholar]
  5. Becker, S. D., Bennett, M., Stewart, J. P. & Hurst, J. L. ( 2007; ). Serological survey of virus infection among wild house mice (Mus domesticus) in the UK. Lab Anim 41, 229–238.[CrossRef]
    [Google Scholar]
  6. Besselsen, D. G., Romero, M. J., Wagner, A. M., Henderson, K. S. & Livingston, R. S. ( 2006; ). Identification of novel murine parvovirus strains by epidemiological analysis of naturally infected mice. J Gen Virol 87, 1543–1556.[CrossRef]
    [Google Scholar]
  7. Brandenburger, A. & Velu, T. ( 2004; ). Autonomous parvovirus vectors: preventing the generation of wild-type or replication-competent virus. J Gene Med 6, S203–S211.[CrossRef]
    [Google Scholar]
  8. Brown, T. T., Jr, Paul, P. S. & Mengeling, W. L. ( 1980; ). Response of conventionally raised weanling pigs to experimental infection with a virulent strain of porcine parvovirus. Am J Vet Res 41, 1221–1224.
    [Google Scholar]
  9. Bugert, J. J. & Darai, G. ( 2000; ). Poxvirus homologues of cellular genes. Virus Genes 21, 111–133.[CrossRef]
    [Google Scholar]
  10. Cotmore, S. F. & Tattersall, P. ( 2003; ). Resolution of parvovirus dimer junctions proceeds through a novel heterocruciform intermediate. J Virol 77, 6245–6254.[CrossRef]
    [Google Scholar]
  11. Edgar, R. C. ( 2004; ). muscle: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32, 1792–1797.[CrossRef]
    [Google Scholar]
  12. Fleischmann, W. J. ( 1996; ). Medical Microbiology, 4th edition. Edited by S. Baron. Galveston, TX: The University of Texas Medical Branch at Galveston.
  13. 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]
  14. Gottschalck, E., Alexandersen, S., Cohn, A., Poulsen, L. A., Bloom, M. E. & Aasted, B. ( 1991; ). Nucleotide sequence analysis of Aleutian mink disease parvovirus shows that multiple virus types are present in infected mink. J Virol 65, 4378–4386.
    [Google Scholar]
  15. Gottschalck, E., Alexandersen, S., Storgaard, T., Bloom, M. E. & Aasted, B. ( 1994; ). Sequence comparison of the non-structural genes of four different types of Aleutian mink disease parvovirus indicates an unusual degree of variability. Arch Virol 138, 213–231.[CrossRef]
    [Google Scholar]
  16. Guérin, B. & Pozzi, N. ( 2005; ). Viruses in boar semen: detection and clinical as well as epidemiological consequences regarding disease transmission by artificial insemination. Theriogenology 63, 556–572.[CrossRef]
    [Google Scholar]
  17. Hino, S. & Miyata, H. ( 2007; ). Torque teno virus (TTV): current status. Rev Med Virol 17, 45–57.[CrossRef]
    [Google Scholar]
  18. Hokynar, K., Soderlund-Venermo, M., Pesonen, M., Ranki, A., Kiviluoto, O., Partio, E. K. & Hedman, K. ( 2002; ). A new parvovirus genotype persistent in human skin. Virology 302, 224–228.[CrossRef]
    [Google Scholar]
  19. Jackson, M. K., Ellis, L. C., Morrey, J. D., Li, Z. Z. & Barnard, D. L. ( 1996; ). Progression of Aleutian disease in natural and experimentally induced infections of mink. Am J Vet Res 57, 1753–1758.
    [Google Scholar]
  20. Jacoby, R. O., Johnson, E. A., Ball-Goodrich, L., Smith, A. L. & McKisic, M. D. ( 1995; ). Characterization of mouse parvovirus infection by in situ hybridization. J Virol 69, 3915–3919.
    [Google Scholar]
  21. Jacoby, R. O., Ball-Goodrich, L. J., Besselsen, D. G., McKisic, M. D., Riley, L. K. & Smith, A. L. ( 1996; ). Rodent parvovirus infections. Lab Anim Sci 46, 370–380.
    [Google Scholar]
  22. Jacoby, R. O., Johnson, E. A., Paturzo, F. X. & Ball-Goodrich, L. ( 2000; ). Persistent rat virus infection in smooth muscle of euthymic and athymic rats. J Virol 74, 11841–11848.[CrossRef]
    [Google Scholar]
  23. Kosakovsky Pond, S. L., Posada, D., Gravenor, M. B., Woelk, C. H. & Frost, S. D. ( 2006; ). Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 23, 1891–1901.[CrossRef]
    [Google Scholar]
  24. Lefrere, J. J., Servant-Delmas, A., Candotti, D., Mariotti, M., Thomas, I., Brossard, Y., Lefrere, F., Girot, R., Allain, J. P. & Laperche, S. ( 2005; ). Persistent B19 infection in immunocompetent individuals: implications for transfusion safety. Blood 106, 2890–2895.[CrossRef]
    [Google Scholar]
  25. Lukashov, V. V. & Goudsmit, J. ( 2001; ). Evolutionary relationships among parvoviruses: virus-host coevolution among autonomous primate parvoviruses and links between adeno-associated and avian parvoviruses. J Virol 75, 2729–2740.[CrossRef]
    [Google Scholar]
  26. Manning, A., Willey, S. J., Bell, J. E. & Simmonds, P. ( 2007; ). Comparison of tissue distribution, persistence, and molecular epidemiology of parvovirus B19 and novel human parvoviruses PARV4 and human bocavirus. J Infect Dis 195, 1345–1352.[CrossRef]
    [Google Scholar]
  27. Martin, D. P., Williamson, C. & Posada, D. ( 2005; ). RDP2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260–262.[CrossRef]
    [Google Scholar]
  28. Mengeling, W. L. & Cutlip, R. C. ( 1975; ). Pathogenesis of in utero infection: experimental infection of five-week-old porcine fetuses with porcine parvovirus. Am J Vet Res 36, 1173–1177.
    [Google Scholar]
  29. Monci, F., Sanchez-Campos, S., Navas-Castillo, J. & Moriones, E. ( 2002; ). A natural recombinant between the geminiviruses Tomato yellow leaf curl Sardinia virus and Tomato yellow leaf curl virus exhibits a novel pathogenic phenotype and is becoming prevalent in Spanish populations. Virology 303, 317–326.[CrossRef]
    [Google Scholar]
  30. Norja, P., Hokynar, K., Aaltonen, L. M., Chen, R., Ranki, A., Partio, E. K., Kiviluoto, O., Davidkin, I., Leivo, T. & other authors ( 2006; ). Bioportfolio: lifelong persistence of variant and prototypic erythrovirus DNA genomes in human tissue. Proc Natl Acad Sci U S A 103, 7450–7453.[CrossRef]
    [Google Scholar]
  31. Parrish, C. R. & Kawaoka, Y. ( 2005; ). The origins of new pandemic viruses: the acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu Rev Microbiol 59, 553–586.[CrossRef]
    [Google Scholar]
  32. Parsyan, A., Szmaragd, C., Allain, J. P. & Candotti, D. ( 2007; ). Identification and genetic diversity of two human parvovirus B19 genotype 3 subtypes. J Gen Virol 88, 428–431.[CrossRef]
    [Google Scholar]
  33. Pereira, C. A., Leal, E. S. & Durigon, E. L. ( 2007; ). Selective regimen shift and demographic growth increase associated with the emergence of high-fitness variants of canine parvovirus. Infect Genet Evol 7, 399–409.[CrossRef]
    [Google Scholar]
  34. Porter, D. D. ( 1986; ). Aleutian disease: a persistent parvovirus infection of mink with a maximal but ineffective host humoral immune response. Prog Med Virol 33, 42–60.
    [Google Scholar]
  35. Posada, D. & Crandall, K. A. ( 1998; ). modeltest: testing the model of DNA substitution. Bioinformatics 14, 817–818.[CrossRef]
    [Google Scholar]
  36. Shackelton, L. A., Parrish, C. R., Truyen, U. & Holmes, E. C. ( 2005; ). High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc Natl Acad Sci U S A 102, 379–384.[CrossRef]
    [Google Scholar]
  37. Swofford, D. ( 2003; ). paup*: Phylogenetic Analysis Using Parsimony (*and other methods). Sunderland, MA: Sinauer Associates, Inc. Publishers.
  38. Thiry, E., Meurens, F., Muylkens, B., McVoy, M., Gogev, S., Thiry, J., Vanderplasschen, A., Epstein, A., Keil, G. & Schynts, F. ( 2005; ). Recombination in alphaherpesviruses. Rev Med Virol 15, 89–103.[CrossRef]
    [Google Scholar]
  39. Young, N. S. & Brown, K. E. ( 2004; ). Parvovirus B19. N Engl J Med 350, 586–597.[CrossRef]
    [Google Scholar]
  40. Zeeuw, E. J., Leinecker, N., Herwig, V., Selbitz, H. J. & Truyen, U. ( 2007; ). Study of the virulence and cross-neutralization capability of recent porcine parvovirus field isolates and vaccine viruses in experimentally infected pregnant gilts. J Gen Virol 88, 420–427.[CrossRef]
    [Google Scholar]
  41. Zimmermann, P., Ritzmann, M., Selbitz, H. J., Heinritzi, K. & Truyen, U. ( 2006; ). VP1 sequences of German porcine parvovirus isolates define two genetic lineages. J Gen Virol 87, 295–301.[CrossRef]
    [Google Scholar]
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