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Viruses2025; 17(7); 947; doi: 10.3390/v17070947

Equine Parvovirus-Hepatitis Population Dynamics in a Single Horse over 16 Years.

Abstract: Many viruses mutate rapidly to adapt to host defenses, and for some of these viruses, the result is long-term infection in individual hosts. The work described here examines the infection and long-term maintenance of a newly identified virus, equine parvovirus-hepatitis (EqPV-H), in an individual horse. This description is possible because of a hypervariable region in the capsid gene; sequence variants were tracked by high-throughput sequencing of serum samples taken over a 16-year period. The data support the hypothesis that EqPV-H infection resulted in a sequence variant bottleneck. The continuing infection evolved into a complex viral population showing a pattern of emergence, dominance, and recession with replacement. This is the first temporal description of the capsid gene evolution of EqPV-H in a single animal.
Publication Date: 2025-07-04 PubMed ID: 40733563PubMed Central: PMC12299937DOI: 10.3390/v17070947Google Scholar: Lookup
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  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The article reports on the long-term study of the mutation and persistence of equine parvovirus-hepatitis (EqPV-H) virus in a single horse over a span of 16 years. The research utilized high-throughput sequencing to track the progression of viral genomic variations in the horse’s serum samples and notes a unique pattern of emergence, dominance, and recession in virus population.

Investigation into Equine Parvovirus-Hepatitis Infection

  • The research carries out a detailed study of the infection and long-term survival of the equine parvovirus-hepatitis (EqPV-H) virus within one horse. This evolved due to a hypervariable region in the capsid gene.
  • By analysing this highly mutable region, the researchers were able to monitor how the virus mutated and adapted in the host over the 16 years of the study.
  • The research provides valuable insights into how viruses evolve to thrive within a host despite the host’s inherent immune responses.

High-Throughput Sequencing and Detection of Sequence Variant Bottleneck

  • The research relies on high-throughput sequencing, a method known for its speed and efficiency in analysing vast quantities of DNA sequences, to track the virus variants in the serum samples from the horse.
  • The results indicate a sequence variant bottleneck, which refers to a sharp decrease in the genetic diversity of the virus population.
  • The term ‘bottleneck’ is used to describe the reduction in variability of the virus due to some pressure that resulted in the majority of variants not surviving.
  • Such bottlenecks are useful in understanding how viruses survive and adapt within hosts and can provide insights into developing more effective treatments.

Emergence, Dominance, and Recession in Virus Population

  • An interesting phenomenon observed in the study was the pattern of emergence, dominance, and recession within the viral population. Over the 16-year study period, different variants of the virus emerged, dominated the host environment, then receded, and were replaced by new emerging variants.
  • This pattern shows how the virus population within a host is not static; instead, it changes and adapts over time to better survive in the host environment.
  • Understanding this changing population can help in addressing long-term chronic infections and the development of resistance to antiviral medications.

Cite This Article

APA
Scupham AJ. (2025). Equine Parvovirus-Hepatitis Population Dynamics in a Single Horse over 16 Years. Viruses, 17(7), 947. https://doi.org/10.3390/v17070947

Publication

ISSN: 1999-4915
NlmUniqueID: 101509722
Country: Switzerland
Language: English
Volume: 17
Issue: 7
PII: 947

Researcher Affiliations

Scupham, Alexandra J
  • Animal and Plant Health Inspection Service, Center for Veterinary Biologics, Ames, IA 50010, USA.

MeSH Terms

  • Animals
  • Horses
  • Horse Diseases / virology
  • Parvoviridae Infections / veterinary
  • Parvoviridae Infections / virology
  • Parvovirus / genetics
  • Parvovirus / classification
  • Parvovirus / isolation & purification
  • Phylogeny
  • Capsid Proteins / genetics
  • High-Throughput Nucleotide Sequencing
  • Hepatitis, Viral, Animal / virology
  • Genetic Variation
  • Evolution, Molecular

Conflict of Interest Statement

The author declares no conflicts of interest.

References

This article includes 71 references
  1. Theiler A. Acute liver-atrophy and parenchymatus hepatitis in horses. 5th and 6th Reports of the Director of Veterinary Research. Dept. of Agriculture, Union of South Africa; Pretoria, South Africa: 1918; pp. 7–164.
  2. Ramsauer A.S., Badenhorst M., Cavalleri J.V. Equine Parvovirus Hepatitis. Equine Vet. J. 2021;53:886–894.
    doi: 10.1111/evj.13477pmc: PMC8457058pubmed: 34101906google scholar: lookup
  3. Divers T.J., Tennant B.C., Kumar A., McDonough S., Cullen J., Bhuva N., Jain K., Chauhan L.S., Scheel T.K.H., Lipkin W.I.. New Parvovirus Associated with Serum Hepatitis in Horses after Inoculation of Common Biological Product. Emerg. Infect. Dis. 2018;24:303–310.
    doi: 10.3201/eid2402.171031pmc: PMC5782890pubmed: 29350162google scholar: lookup
  4. Tomlinson J.E., Zan de Walle G.R., Divers T.J. What Do We Know About Hepatitis Viruses in Horses?. Vet. Clin. N. Am. Equine Pract. 2019;35:351–362.
    doi: 10.1016/j.cveq.2019.03.001pubmed: 31084975google scholar: lookup
  5. Tomlinson J.E., Kapoor A., Kumar A., Tennant B.C., Laverack M.A., Beard L., Delph K., Davis E., Schott Ii H., Lascola K.. Viral testing of 18 consecutive cases of equine serum hepatitis: A prospective study (2014–2018). J. Vet. Intern. Med. 2018;33:251–257.
    doi: 10.1111/jvim.15368pmc: PMC6335536pubmed: 30520162google scholar: lookup
  6. Tomlinson J.E., Tennant B.C., Struzyna A., Mrad D., Browne N., Whelchel D., Johnson P.J., Jamieson C., Lohr C.V., Bildfell R.. Viral testing of 10 cases of Theiler’s disease and 37 in-contact horses in the absence of equine biologic product administration: A prospective study (2014–2018). J. Vet. Intern. Med. 2018;33:258–265.
    doi: 10.1111/jvim.15362pmc: PMC6335540pubmed: 30520132google scholar: lookup
  7. Jager M.C., Choi E., Tomlinson J.E., Van de Walle G. Naturally acquired equine parvovirus-hepatitis is associated with a wide range of hepatic lesions in horses. Vet. Pathol. 2023;61:442–452.
    doi: 10.1177/03009858231214024pmc: PMC11068485pubmed: 38018088google scholar: lookup
  8. Baird J., Tegtmeyer B., Arroyo L., Stang A., Bruggemann Y., Hazlett M., Steinmann E. The association of Equine Parvovirus-Hepatitis (EqPV-H) with cases of non-biologic-associated Theiler’s disease on a farm in Ontario, Canada. Vet. Microbiol. 2020;242:108575.
    doi: 10.1016/j.vetmic.2019.108575pubmed: 32122586google scholar: lookup
  9. Mietzsch M., Penzes J.J., Agbandje-McKenna M. Twenty-Five Years of Structural Parvovirology. Viruses 2019;11:362.
    doi: 10.3390/v11040362pmc: PMC6521121pubmed: 31010002google scholar: lookup
  10. Ros C., Gerber M., Kempf C. Conformational changes in the VP1-unique region of native human parvovirus B19 lead to exposure of internal sequences that play a role in virus neutralization and infectivity. J. Virol. 2006;80:12017–12024.
    doi: 10.1128/JVI.01435-06pmc: PMC1676260pubmed: 17020940google scholar: lookup
  11. Lakshmanan R.V., Hull J.A., Berry L., Burg M., Bothner B., McKenna R., Agbandje-McKenna M. Structural Dynamics and Activity of B19V VP1u during the pHs of Cell Entry and Endosomal Trafficking. Viruses 2022;14:1922.
    doi: 10.3390/v14091922pmc: PMC9505059pubmed: 36146728google scholar: lookup
  12. Ros C., Bieri J., Leisi R. The VP1u of Human Parvovirus B19: A Multifunctional Capsid Protein with Biotechnological Applications. Viruses 2020;12:1463.
    doi: 10.3390/v12121463pmc: PMC7765992pubmed: 33352888google scholar: lookup
  13. Domingo E., Sabo D., Taniguchi T., Weissmann C. Nucleotide sequence heterogeneity of an RNA phage population. Cell 1978;13:735–744.
    doi: 10.1016/0092-8674(78)90223-4pubmed: 657273google scholar: lookup
  14. Domingo E., Soria M.E., Gallego I., de Avila A.I., Garcia-Crespo C., Martinez-Gonzalez B., Gomez J., Briones C., Gregori J., Quer J.. A new implication of quasispecies dynamics: Broad virus diversification in absence of external perturbations. Infect. Genet. Evol. 2020;82:104278.
    doi: 10.1016/j.meegid.2020.104278pubmed: 32165244google scholar: lookup
  15. Duffy S., Shackelton L.A., Holmes E.C. Rates of evolutionary change in viruses: Patterns and determinants. Nat. Rev. Genet. 2008;9:267–276.
    doi: 10.1038/nrg2323pubmed: 18319742google scholar: lookup
  16. Li C., Candotti D., Allain J.P. Production and characterization of monoclonal antibodies specific for a conserved epitope within hepatitis C virus hypervariable region 1. J. Virol. 2001;75:12412–12420.
  17. Hijikata M., Kato N., Ootsuyama Y., Nakagawa M., Ohkoshi S., Shimotohno K. Hypervariable regions in the putative glycoprotein of hepatitis C virus. Biochem. Biophys. Res. Commun. 1991;175:220–228.
    doi: 10.1016/S0006-291X(05)81223-9pubmed: 1847805google scholar: lookup
  18. Martell M., Esteban J.I., Quer J., Genesca J., Weiner A., Esteban R., Guardia J., Gomez J. Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: Quasispecies nature of HCV genome distribution. J. Virol. 1992;66:3225–3229.
  19. Higashi Y., Kakumu S., Yoshioka K., Wakita T., Mizokami M., Ohba K., Ito Y., Ishikawa T., Takayanagi M., Nagai Y. Dynamics of genome change in the E2/NS1 region of hepatitis C virus in vivo. Virology 1993;197:659–668.
    doi: 10.1006/viro.1993.1641pubmed: 8249288google scholar: lookup
  20. Eigen M., Schuster P. The hypercycle. A principle of natural self-organization. Naturwissenschaften 1978;65:7–41.
    doi: 10.1007/BF00420631pubmed: 593400google scholar: lookup
  21. Epstein I.R., Eigen M. Selection and self-organization of self-reproducing macromolecules under the constraint of constant flux. Biophys. Chem. 1979;10:153–160.
    doi: 10.1016/0301-4622(79)85035-8pubmed: 486701google scholar: lookup
  22. Lu G., Wu L., Ou J., Li S. Equine Parvovirus-Hepatitis in China: Characterization of Its Genetic Diversity and Evidence for Natural Recombination Events Between the Chinese and American Strains. Front. Vet. Sci. 2020;7:121.
    doi: 10.3389/fvets.2020.00121pmc: PMC7076910pubmed: 32211433google scholar: lookup
  23. Lu G., Sun L., Ou J., Xu H., Wu L., Li S. Identification and genetic characterization of a novel parvovirus associated with serum hepatitis in horses in China. Emerg. Microbes Infect. 2018;7:170.
    doi: 10.1038/s41426-018-0174-2pmc: PMC6198012pubmed: 30348940google scholar: lookup
  24. Yoon J., Park T., Kim A., Song H., Park B.J., Ahn H.S., Go H.J., Kim D.H., Lee J.B., Park S.Y.. First report of equine parvovirus-hepatitis and equine hepacivirus coinfection in horses in Korea. Transbound. Emerg. Dis. 2022;69:2735–2746.
    doi: 10.1111/tbed.14425pubmed: 34919324google scholar: lookup
  25. Vengust M., Jager M.C., Zalig V., Cociancich V., Laverack M., Renshaw R.W., Dubovi E., Tomlinson J.E., Van de Walle G.R., Divers T.J. First report of equine parvovirus-hepatitis-associated Theiler’s disease in Europe. Equine Vet. J. 2020;52:841–847.
    doi: 10.1111/evj.13254pmc: PMC7483838pubmed: 32145096google scholar: lookup
  26. Stamenkovic G.G., Cirkovic V.S., Siljic M.M., Blagojevic J.V., Knezevic A.M., Joksic I.D., Stanojevic M.P. Substitution rate and natural selection in parvovirus B19. Sci. Rep. 2016;6:35759.
    doi: 10.1038/srep35759pmc: PMC5075947pubmed: 27775080google scholar: lookup
  27. Shackelton L.A., Parrish C.R., Truyen U., Holmes E.C. High rate of viral evolution associated with the emergence of carnivore parvovirus. Proc. Natl. Acad. Sci. USA 2005;102:379–384.
    doi: 10.1073/pnas.0406765102pmc: PMC544290pubmed: 15626758google scholar: lookup
  28. Gregori J., Rodriguez-Frias F., Quer J. Viral Quasispecies Diversity and Evolution. A Bioinformatics Molecular Approach. Il Pensiero Scientifico Editore; Rome, Italy: 2023.
  29. Domingo E. Quasispecies: From Theory to Experimental Systems. Volume 392. Springer; Cham, Switzerland: 2016. p. 360.
  30. Kariuki S.M., Selhorst P., Arien K.K., Dorfman J.R. The HIV-1 transmission bottleneck. Retrovirology 2017;14:22.
    doi: 10.1186/s12977-017-0343-8pmc: PMC5364581pubmed: 28335782google scholar: lookup
  31. Wang G.P., Sherrill-Mix S.A., Chang K.M., Quince C., Bushman F.D. Hepatitis C virus transmission bottlenecks analyzed by deep sequencing. J. Virol. 2010;84:6218–6228.
    doi: 10.1128/JVI.02271-09pmc: PMC2876626pubmed: 20375170google scholar: lookup
  32. Escarmis C., Lazaro E., Manrubia S.C. Population bottlenecks in quasispecies dynamics. Curr. Top. Microbiol. Immunol. 2006;299:141–170.
    pubmed: 16568898
  33. Lahner E., Brigatti C., Marzinotto I., Carabotti M., Scalese G., Davidson H.W., Wenzlau J.M., Bosi E., Piemonti L., Annibale B.. Luminescent Immunoprecipitation System (LIPS) for Detection of Autoantibodies Against ATP4A and ATP4B Subunits of Gastric Proton Pump H+,K+-ATPase in Atrophic Body Gastritis Patients. Clin. Transl. Gastroenterol. 2017;8:e215.
    doi: 10.1038/ctg.2016.71pmc: PMC5288605pubmed: 28102858google scholar: lookup
  34. Burbelo P.D., Goldman R., Mattson T.L. A simplified immunoprecipitation method for quantitatively measuring antibody responses in clinical sera samples by using mammalian-produced Renilla luciferase-antigen fusion proteins. BMC Biotechnol. 2005;5:22.
    doi: 10.1186/1472-6750-5-22pmc: PMC1208859pubmed: 16109166google scholar: lookup
  35. Lahner E., Marzinotto I., Brigatti C., Davidson H., Wenzlau J., Piemonti L., Annibale B., Lampasona V. Measurement of Autoantibodies to Gastric H+,K+-ATPase (ATP4A/B) Using a Luciferase Immunoprecipitation System (LIPS). Methods Mol. Biol. 2019;1901:113–131.
    pubmed: 30539573
  36. Scupham A.J., Tong C. Detection of Equine parvovirus-hepatitis and efficacy of governmental regulation for equine biologics purity. J. Vet. Diagn. Investig. 2024;37:79–85.
    doi: 10.1177/10406387241292343pmc: PMC11559848pubmed: 39506428google scholar: lookup
  37. Bushnell B., Rood J., Singer E. BBMerge—Accurate paired shotgun read merging via overlap. PLoS ONE 2017;12:e0185056.
  38. Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002;30:3059–3066.
    doi: 10.1093/nar/gkf436pmc: PMC135756pubmed: 12136088google scholar: lookup
  39. Stamatakis A. RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 2014;30:1312–1313.
  40. Pielou E.C. The measurement of diversity in different types of biological collectio. J. Theor. Biol. 1966;13:131–144.
  41. Gregori J., Perales C., Rodriguez-Frias F., Esteban J.I., Quer J., Domingo E. Viral quasispecies complexity measures. Virology 2016;493:227–237.
    doi: 10.1016/j.virol.2016.03.017pubmed: 27060566google scholar: lookup
  42. Ramirez C., Gregori J., Buti M., Tabernero D., Camos S., Casillas R., Quer J., Esteban R., Homs M., Rodriguez-Frias F. A comparative study of ultra-deep pyrosequencing and cloning to quantitatively analyze the viral quasispecies using hepatitis B virus infection as a model. Antivir. Res. 2013;98:273–283.
  43. Murrell B., Moola S., Mabona A., Weighill T., Sheward D., Kosakovsky Pond S.L., Scheffler K. FUBAR: A fast, unconstrained bayesian approximation for inferring selection. Mol. Biol. Evol. 2013;30:1196–1205.
    doi: 10.1093/molbev/mst030pmc: PMC3670733pubmed: 23420840google scholar: lookup
  44. Murrell B., Wertheim J.O., Moola S., Weighill T., Scheffler K., Kosakovsky Pond S.L. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 2012;8:e1002764.
  45. Gregori J., Ibanez-Lligona M., Quer J. Quantifying In-Host Quasispecies Evolution. Int. J. Mol. Sci. 2023;24:1301.
    doi: 10.3390/ijms24021301pmc: PMC9867078pubmed: 36674827google scholar: lookup
  46. Xie Q., Chapman M.S. Canine parvovirus capsid structure, analyzed at 2.9 A resolution. J. Mol. Biol. 1996;264:497–520.
    doi: 10.1006/jmbi.1996.0657pubmed: 8969301google scholar: lookup
  47. Venkatakrishnan B., Yarbrough J., Domsic J., Bennett A., Bothner B., Kozyreva O.G., Samulski R.J., Muzyczka N., McKenna R., Agbandje-McKenna M. Structure and dynamics of adeno-associated virus serotype 1 VP1-unique N-terminal domain and its role in capsid trafficking. J. Virol. 2013;87:4974–4984.
    doi: 10.1128/JVI.02524-12pmc: PMC3624325pubmed: 23427155google scholar: lookup
  48. Zadori Z., Szelei J., Lacoste M.C., Li Y., Gariepy S., Raymond P., Allaire M., Nabi I.R., Tijssen P. A viral phospholipase A2 is required for parvovirus infectivity. Dev. Cell. 2001;1:291–302.
    doi: 10.1016/S1534-5807(01)00031-4pubmed: 11702787google scholar: lookup
  49. Carter B.J. Variant and Defective Interfering Parvoviruses. In: Berns K.I., editor. The Parvoviruses. Springer; Boston, MA, USA: 1984.
  50. Battilani M., Balboni A., Ustulin M., Giunti M., Scagliarini A., Prosperi S. Genetic complexity and multiple infections with more Parvovirus species in naturally infected cats. Vet. Res. 2011;42:43.
    doi: 10.1186/1297-9716-42-43pmc: PMC3059301pubmed: 21366901google scholar: lookup
  51. Battilani M., Scagliarini A., Ciulli S., Morganti L., Prosperi S. High genetic diversity of the VP2 gene of a canine parvovirus strain detected in a domestic cat. Virology 2006;352:22–26.
    doi: 10.1016/j.virol.2006.06.002pubmed: 16822535google scholar: lookup
  52. Domingo E. Quasispecies: Concepts and Implications for Virology. Springer; New York, NY, USA: 2006.
  53. Woo H.J., Reifman J. A quantitative quasispecies theory-based model of virus escape mutation under immune selection. Proc. Natl. Acad. Sci. USA 2012;109:12980–12985.
    doi: 10.1073/pnas.1117201109pmc: PMC3420195pubmed: 22826258google scholar: lookup
  54. Lange A., Mills R.E., Lange C.J., Stewart M., Devine S.E., Corbett A.H. Classical nuclear localization signals: Definition, function, and interaction with importin alpha. J. Biol. Chem. 2007;282:5101–5105.
    doi: 10.1074/jbc.R600026200pmc: PMC4502416pubmed: 17170104google scholar: lookup
  55. Lu J., Wu T., Zhang B., Liu S., Song W., Qiao J., Ruan H. Types of nuclear localization signals and mechanisms of protein import into the nucleus. Cell Commun. Signal. 2021;19:60.
    doi: 10.1186/s12964-021-00741-ypmc: PMC8140498pubmed: 34022911google scholar: lookup
  56. Boisvert M., Bouchard-Levesque V., Fernandes S., Tijssen P. Classic nuclear localization signals and a novel nuclear localization motif are required for nuclear transport of porcine parvovirus capsid proteins. J. Virol. 2014;88:11748–11759.
    doi: 10.1128/JVI.01717-14pmc: PMC4178750pubmed: 25078698google scholar: lookup
  57. Liu P., Chen S., Wang M., Cheng A. The role of nuclear localization signal in parvovirus life cycle. Virol. J. 2017;14:80.
    doi: 10.1186/s12985-017-0745-1pmc: PMC5391597pubmed: 28410597google scholar: lookup
  58. Lombardo E., Ramirez J.C., Garcia J., Almendral J.M. Complementary roles of multiple nuclear targeting signals in the capsid proteins of the parvovirus minute virus of mice during assembly and onset of infection. J. Virol. 2002;76:7049–7059.
  59. Xie H.L., Wang Z., Cui S.J., Zhang C.F., Cui Y.D. The epitope of the VP1 protein of porcine parvovirus. Virol. J. 2010;7:161.
    doi: 10.1186/1743-422X-7-161pmc: PMC2912839pubmed: 20637107google scholar: lookup
  60. Kattenbelt J.A., Stevens M.P., Gould A.R. Sequence variation in the Newcastle disease virus genome. Virus Res. 2006;116:168–184.
  61. Nie Z., Bergeron D., Subbramanian R.A., Yao X.J., Checroune F., Rougeau N., Cohen E.A. The putative alpha helix 2 of human immunodeficiency virus type 1 Vpr contains a determinant which is responsible for the nuclear translocation of proviral DNA in growth-arrested cells. J. Virol. 1998;72:4104–4115.
  62. Pellerin M., Lopez-Aguirre Y., Penin F., Dhumeaux D., Pawlotsky J.M. Hepatitis C virus quasispecies variability modulates nonstructural protein 5A transcriptional activation, pointing to cellular compartmentalization of virus-host interactions. J. Virol. 2004;78:4617–4627.
  63. Lopez de Turiso J.A., Cortes E., Ranz A., Garcia J., Sanz A., Vela C., Casal J.I. Fine mapping of canine parvovirus B cell epitopes. Pt 10. J. Gen. Virol. 1991;72:2445–2456.
    doi: 10.1099/0022-1317-72-10-2445pubmed: 1919526google scholar: lookup
  64. Saikawa T., Anderson S., Momoeda M., Kajigaya S., Young N.S. Neutralizing linear epitopes of B19 parvovirus cluster in the VP1 unique and VP1-VP2 junction regions. J. Virol. 1993;67:3004–3009.
  65. Rimmelzwaan G.F., Poelen M.C., Meloen R.H., Carlson J., UytdeHaag F.G., Osterhaus A.D. Delineation of canine parvovirus T cell epitopes with peripheral blood mononuclear cells and T cell clones from immunized dogs. Pt 10. J. Gen. Virol. 1990;71:2321–2329.
    doi: 10.1099/0022-1317-71-10-2321pubmed: 1700064google scholar: lookup
  66. de Souza A.R., Yamin M., Gava D., Zanella J.R.C., Gatti M.S.V., Bonafe C.F.S., de Lima Neto D.F. Porcine parvovirus VP1/VP2 on a time series epitope mapping: Exploring the effects of high hydrostatic pressure on the immune recognition of antigens. Virol. J. 2019;16:75.
    doi: 10.1186/s12985-019-1165-1pmc: PMC6547530pubmed: 31159841google scholar: lookup
  67. Bonsch C., Zuercher C., Lieby P., Kempf C., Ros C. The globoside receptor triggers structural changes in the B19 virus capsid that facilitate virus internalization. J. Virol. 2010;84:11737–11746.
    doi: 10.1128/JVI.01143-10pmc: PMC2977879pubmed: 20826697google scholar: lookup
  68. Kawase M., Momoeda M., Young N.S., Kajigaya S. Most of the VP1 unique region of B19 parvovirus is on the capsid surface. Virology 1995;211:359–366.
    doi: 10.1006/viro.1995.1418pubmed: 7544049google scholar: lookup
  69. Rosenfeld S.J., Yoshimoto K., Kajigaya S., Anderson S., Young N.S., Field A., Warrener P., Bansal G., Collett M.S. Unique region of the minor capsid protein of human parvovirus B19 is exposed on the virion surface. J. Clin. Investig. 1992;89:2023–2029.
    doi: 10.1172/JCI115812pmc: PMC295912pubmed: 1376332google scholar: lookup
  70. Kaufmann B., Chipman P.R., Kostyuchenko V.A., Modrow S., Rossmann M.G. Visualization of the externalized VP2 N termini of infectious human parvovirus B19. J. Virol. 2008;82:7306–7312.
    doi: 10.1128/JVI.00512-08pmc: PMC2493345pubmed: 18508892google scholar: lookup
  71. Wilke C.O., Wang J.L., Ofria C., Lenski R.E., Adami C. Evolution of digital organisms at high mutation rates leads to survival of the flattest. Nature 2001;412:331–333.
    doi: 10.1038/35085569pubmed: 11460163google scholar: lookup

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