1887

Abstract

Bovine papillomavirus types 1 and 2 (BPV-1 and BPV-2) are known to induce common equine skin tumours, termed sarcoids. Recently, it was demonstrated that vaccination with BPV-1 virus-like particles (VLPs) is safe and highly immunogenic in horses. To establish a BPV-1 challenge model for evaluation of the protective potential of BPV-1 VLPs, four foals were injected intradermally with infectious BPV-1 virions and with viral genome-based and control inocula, and monitored daily for tumour development. Blood was taken before inoculation and at weekly intervals. BPV-1-specific serum antibodies were detected by a pseudo-virion neutralization assay. Total nucleic acids extracted from tumours, intact skin and PBMCs were tested for the presence of BPV-1 DNA and mRNA using PCR and RT-PCR, respectively. Intralesional E5 oncoprotein expression was determined by immunofluorescence. Pseudo-sarcoids developed exclusively at sites inoculated with virions. Tumours became palpable 11–32 days after virion challenge, reached a size of ≤20 mm in diameter and then resolved in ≤6 months. No neutralizing anti-BPV-1 serum antibodies were detectable pre- or post-challenge. BPV-1 DNA was present in lesions but not in intact skin. In PBMCs, viral DNA was already detectable before lesions were first palpable, in concentrations correlating directly with tumour growth kinetics. PBMCs from two of two foals also harboured E5 mRNA. Immunofluorescence revealed the presence of the E5 protein in tumour fibroblasts, but not in the apparently normal epidermis overlying the lesions. Together with previous findings obtained in horses and cows, these data suggest that papillomavirus infection may include a viraemic phase.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.033670-0
2011-10-01
2019-10-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/10/2437.html?itemId=/content/journal/jgv/10.1099/vir.0.033670-0&mimeType=html&fmt=ahah

References

  1. Amtmann E. , Müller H. , Sauer G. . ( 1980; ). Equine connective tissue tumors contain unintegrated bovine papilloma virus DNA. . J Virol 35:, 962–964.[PubMed]
    [Google Scholar]
  2. Bogaert L. , Martens A. , De Baere C. , Gasthuys F. . ( 2005; ). Detection of bovine papillomavirus DNA on the normal skin and in the habitual surroundings of horses with and without equine sarcoids. . Res Vet Sci 79:, 253–258. [CrossRef] [PubMed]
    [Google Scholar]
  3. Bogaert L. , Martens A. , Kast W. M. , Van Marck E. , De Cock H. . ( 2010; ). Bovine papillomavirus DNA can be detected in keratinocytes of equine sarcoid tumors. . Vet Microbiol 146:, 269–275. [CrossRef] [PubMed]
    [Google Scholar]
  4. Borzacchiello G. , Roperto F. , Campo M. S. , Venuti A. . ( 2010; ). 1st International Workshop on Papillomavirus E5 Oncogene – a report. . Virology 408:, 135–137. [CrossRef] [PubMed]
    [Google Scholar]
  5. Brandt S. , Haralambus R. , Shafti-Keramat S. , Steinborn R. , Stanek C. , Kirnbauer R. . ( 2008a; ). A subset of equine sarcoids harbours BPV-1 DNA in a complex with L1 major capsid protein. . Virology 375:, 433–441. [CrossRef] [PubMed]
    [Google Scholar]
  6. Brandt S. , Haralambus R. , Schoster A. , Kirnbauer R. , Stanek C. . ( 2008b; ). Peripheral blood mononuclear cells represent a reservoir of bovine papillomavirus DNA in sarcoid-affected equines. . J Gen Virol 89:, 1390–1395. [CrossRef] [PubMed]
    [Google Scholar]
  7. Brandt S. , Apprich V. , Hackl V. , Tober R. , Danzer M. , Kainzbauer C. , Gabriel C. , Stanek C. , Kofler J. . ( 2011a; ). Prevalence of bovine papillomavirus and Treponema DNA in bovine digital dermatitis lesions. . Vet Microbiol 148:, 161–167. [CrossRef] [PubMed]
    [Google Scholar]
  8. Brandt S. , Schoster A. , Tober R. , Kainzbauer C. , Burgstaller J. P. , Haralambus R. , Steinborn R. , Hinterhofer C. , Stanek C. . ( 2011b; ). Consistent detection of bovine papillomavirus in lesions, intact skin and peripheral blood mononuclear cells of horses affected by hoof canker. . Equine Vet J 43:, 202–209. [CrossRef] [PubMed]
    [Google Scholar]
  9. Brandt S. , Tober R. , Corteggio A. , Burger S. , Sabitzer S. , Walter I. , Kainzbauer C. , Steinborn R. , Nasir L. , Borzacchiello G. . ( 2011c; ). BPV-1 infection is not confined to the dermis but also involves the epidermis of equine sarcoids. . Vet Microbiol 150:, 35–40. [CrossRef] [PubMed]
    [Google Scholar]
  10. Breitburd F. , Kirnbauer R. , Hubbert N. L. , Nonnenmacher B. , Trin-Dinh-Desmarquet C. , Orth G. , Schiller J. T. , Lowy D. R. . ( 1995; ). Immunization with viruslike particles from cottontail rabbit papillomavirus (CRPV) can protect against experimental CRPV infection. . J Virol 69:, 3959–3963.[PubMed]
    [Google Scholar]
  11. Campo M. S. . ( 2006a; ). Introduction. . In Papillomavirus Research: From Natural History to Vaccines and Beyond, pp. 1–2. Edited by Campo M. S. . . Norfolk, UK:: Caister Academic Press;.
    [Google Scholar]
  12. Campo M. S. . ( 2006b; ). Bovine papillomavirus: old system, new lessons?. In Papillomavirus Research: From Natural History to Vaccines and Beyond, pp. 373–387. Edited by Campo M. S. . . Norfolk, UK:: Caister Academic Press;.
    [Google Scholar]
  13. Chambers G. , Ellsmore V. A. , O’Brien P. M. , Reid S. W. J. , Love S. , Campo M. S. , Nasir L. . ( 2003; ). Association of bovine papillomavirus with the equine sarcoid. . J Gen Virol 84:, 1055–1062. [CrossRef] [PubMed]
    [Google Scholar]
  14. Chow L. T. , Broker T. R. . ( 2006; ). Mechanisms and regulation of papillomavirus DNA replication. . In Papillomavirus Research: From Natural History to Vaccines and Beyond, pp. 53–71. Edited by Campo M. S. . . Norfolk, UK:: Caister Academic Press;.
    [Google Scholar]
  15. Coleman N. , Birley H. D. , Renton A. M. , Hanna N. F. , Ryait B. K. , Byrne M. , Taylor-Robinson D. , Stanley M. A. . ( 1994; ). Immunological events in regressing genital warts. . Am J Clin Pathol 102:, 768–774.[PubMed]
    [Google Scholar]
  16. Day P. M. , Lowy D. R. , Schiller J. T. . ( 2003; ). Papillomaviruses infect cells via a clathrin-dependent pathway. . Virology 307:, 1–11. [CrossRef] [PubMed]
    [Google Scholar]
  17. de Freitas A. C. , de Carvalho C. , Brunner O. , Birgel E. H. Jr , Melville Paiva Dellalibera A. M. , Benesi F. J. , Gregory L. , Beçak W. , de Cassia Stocco dos Santos R. . ( 2003; ). Viral DNA sequences in peripheral blood and vertical transmission of the virus: a discussion about BPV-1. . Braz J Microbiol 34:, 76–78. [CrossRef]
    [Google Scholar]
  18. Giroglou T. , Florin L. , Schäfer F. , Streeck R. E. , Sapp M. . ( 2001; ). Human papillomavirus infection requires cell surface heparan sulfate. . J Virol 75:, 1565–1570. [CrossRef] [PubMed]
    [Google Scholar]
  19. Hainisch E. K. , Brandt S. , Shafti-Keramat S. , van den Hoven R. , Kirnbauer R. . ( 2011; ). Safety and immunogenicity of BPV-1 L1 virus-like particles in a dose-escalation vaccination trial in horses. . Equine Vet J (in press). [CrossRef]
    [Google Scholar]
  20. Joyce J. G. , Tung J. S. , Przysiecki C. T. , Cook J. C. , Lehman E. D. , Sands J. A. , Jansen K. U. , Keller P. M. . ( 1999; ). The L1 major capsid protein of human papillomavirus type 11 recombinant virus-like particles interacts with heparin and cell-surface glycosaminoglycans on human keratinocytes. . J Biol Chem 274:, 5810–5822. [CrossRef] [PubMed]
    [Google Scholar]
  21. Kirnbauer R. . ( 1996; ). Papillomavirus-like particles for serology and vaccine development. . Intervirology 39:, 54–61.[PubMed]
    [Google Scholar]
  22. Kirnbauer R. , Chandrachud L. M. , O’Neil B. W. , Wagner E. R. , Grindlay G. J. , Armstrong A. , McGarvie G. M. , Schiller J. T. , Lowy D. R. , Campo M. S. . ( 1996; ). Virus-like particles of bovine papillomavirus type 4 in prophylactic and therapeutic immunization. . Virology 219:, 37–44. [CrossRef] [PubMed]
    [Google Scholar]
  23. Knottenbelt D. C. . ( 2005; ). A suggested clinical classification for the equine sarcoid. . Clin Tech Equine Pract 4:, 278–295. [CrossRef]
    [Google Scholar]
  24. Knowles G. , O’Neil B. W. , Campo M. S. . ( 1996; ). Phenotypical characterization of lymphocytes infiltrating regressing papillomas. . J Virol 70:, 8451–8458.[PubMed]
    [Google Scholar]
  25. Kohrgruber N. , Gröger M. , Meraner P. , Kriehuber E. , Petzelbauer P. , Brandt S. , Stingl G. , Rot A. , Maurer D. . ( 2004; ). Plasmacytoid dendritic cell recruitment by immobilized CXCR3 ligands. . J Immunol 173:, 6592–6602.[PubMed] [CrossRef]
    [Google Scholar]
  26. Lancaster W. D. . ( 1981; ). Apparent lack of integration of bovine papillomavirus DNA in virus-induced equine and bovine tumor cells and virus-transformed mouse cells. . Virology 108:, 251–255. [CrossRef] [PubMed]
    [Google Scholar]
  27. Lancaster W. D. , Olson C. , Meinke W. . ( 1977; ). Bovine papillomavirus: presence of virus-specific DNA sequences in naturally occurring equine tumors. . Proc Natl Acad Sci U S A 74:, 524–528. [CrossRef]
    [Google Scholar]
  28. Marais H. J. , Nel P. , Bertschinger H. J. , Schoeman J. P. , Zimmerman D. . ( 2007; ). Prevalence and body distribution of sarcoids in South African Cape mountain zebra (Equus zebra zebra). . J S Afr Vet Assoc 78:, 145–148.[PubMed] [CrossRef]
    [Google Scholar]
  29. Marchetti B. , Gault E. A. , Cortese M. S. , Yuan Z. , Ellis S. A. , Nasir L. , Campo M. S. . ( 2009; ). Bovine papillomavirus type 1 oncoprotein E5 inhibits equine MHC class I and interacts with equine MHC I heavy chain. . J Gen Virol 90:, 2865–2870. [CrossRef] [PubMed]
    [Google Scholar]
  30. Nasir L. , Campo M. S. . ( 2008; ). Bovine papillomaviruses: their role in the aetiology of cutaneous tumours of bovids and equids. . Vet Dermatol 19:, 243–254. [CrossRef] [PubMed]
    [Google Scholar]
  31. Nasir L. , Reid S. W. J. . ( 1999; ). Bovine papillomaviral gene expression in equine sarcoid tumours. . Virus Res 61:, 171–175. [CrossRef] [PubMed]
    [Google Scholar]
  32. Nasir L. , Reid S. W. J. . ( 2006; ). Bovine papillomaviruses and equine sarcoids. . In Papillomavirus Research: From Natural History to Vaccines and Beyond, pp. 389–397. Edited by Campo M. S. . . Norfolk, UK:: Caister Academic Press;.
    [Google Scholar]
  33. Olson C. Jr , Cook R. H. . ( 1951; ). Cutaneous sarcoma-like lesions of the horse caused by the agent of bovine papilloma. . Proc Soc Exp Biol Med 77:, 281–284.[PubMed] [CrossRef]
    [Google Scholar]
  34. Pastrana D. V. , Buck C. B. , Pang Y. Y. , Thompson C. D. , Castle P. E. , FitzGerald P. C. , Krüger Kjaer S. , Lowy D. R. , Schiller J. T. . ( 2004; ). Reactivity of human sera in a sensitive, high-throughput pseudovirus-based papillomavirus neutralization assay for HPV16 and HPV18. . Virology 321:, 205–216. [CrossRef] [PubMed]
    [Google Scholar]
  35. Ragland W. L. , Spencer G. R. . ( 1969; ). Attempts to relate bovine papilloma virus to the cause of equine sarcoid: equidae inoculated intradermally with bovine papilloma virus. . Am J Vet Res 30:, 743–752.[PubMed]
    [Google Scholar]
  36. Roden R. B. , Kirnbauer R. , Jenson A. B. , Lowy D. R. , Schiller J. T. . ( 1994; ). Interaction of papillomaviruses with the cell surface. . J Virol 68:, 7260–7266.[PubMed]
    [Google Scholar]
  37. Roden R. B. , Greenstone H. L. , Kirnbauer R. , Booy F. P. , Jessie J. , Lowy D. R. , Schiller J. T. . ( 1996; ). In vitro generation and type-specific neutralization of a human papillomavirus type 16 virion pseudotype. . J Virol 70:, 5875–5883.[PubMed]
    [Google Scholar]
  38. Roperto S. , Brun R. , Paolini F. , Urraro C. , Russo V. , Borzacchiello G. , Pagnini U. , Raso C. , Rizzo C. et al. & other authors ( 2008; ). Detection of bovine papillomavirus type 2 in the peripheral blood of cattle with urinary bladder tumours: possible biological role. . J Gen Virol 89:, 3027–3033. [CrossRef] [PubMed]
    [Google Scholar]
  39. Roperto S. , Comazzi S. , Ciusani E. , Paolini F. , Borzacchiello G. , Esposito I. , Lucà R. , Russo V. , Urraro C. et al. & other authors ( 2011; ). PBMCs are additional sites of productive infection of bovine papillomavirus type 2. . J Gen Virol 92:, 1787–1794. [CrossRef] [PubMed]
    [Google Scholar]
  40. Schiller J. T. . ( 2007; ). Papillomavirus vaccines. . In The Papillomaviruses, pp. 337–369. Edited by Garcia R. , DiMaio D. . . New York:: Springer;. [CrossRef]
    [Google Scholar]
  41. Schiller J. T. , Day P. M. , Kines R. C. . ( 2010; ). Current understanding of the mechanism of HPV infection. . Gynecol Oncol 118: (Suppl.), S12–S17. [CrossRef] [PubMed]
    [Google Scholar]
  42. Scott D. W. , Miller W. H. Jr . ( 2003; ). Sarcoid. . In Equine Dermat ology, pp. 719–731. St Louis, Missouri, USA:: Elsevier Science;.
    [Google Scholar]
  43. Shafti-Keramat S. , Handisurya A. , Kriehuber E. , Meneguzzi G. , Slupetzky K. , Kirnbauer R. . ( 2003; ). Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. . J Virol 77:, 13125–13135. [CrossRef] [PubMed]
    [Google Scholar]
  44. Shafti-Keramat S. , Schellenbacher C. , Handisurya A. , Christensen N. , Reininger B. , Brandt S. , Kirnbauer R. . ( 2009; ). Bovine papillomavirus type 1 (BPV1) and BPV2 are closely related serotypes. . Virology 393:, 1–6. [CrossRef] [PubMed]
    [Google Scholar]
  45. Smith J. L. , Campos S. K. , Ozbun M. A. . ( 2007; ). Human papillomavirus type 31 uses a caveolin 1- and dynamin 2-mediated entry pathway for infection of human keratinocytes. . J Virol 81:, 9922–9931. [CrossRef] [PubMed]
    [Google Scholar]
  46. Spoden G. , Freitag K. , Husmann M. , Boller K. , Sapp M. , Lambert C. , Florin L. . ( 2008; ). Clathrin- and caveolin-independent entry of human papillomavirus type 16 – involvement of tetraspanin-enriched microdomains (TEMs). . PLoS ONE 3:, e3313. [CrossRef] [PubMed]
    [Google Scholar]
  47. Stocco dos Santos R. C. , Lindsey C. J. , Ferraz O. P. , Pinto J. R. , Mirandola R. S. , Benesi F. J. , Birgel E. H. , Pereira C. A. , Beçak W. . ( 1998; ). Bovine papillomavirus transmission and chromosomal aberrations: an experimental model. . J Gen Virol 79:, 2127–2135.[PubMed]
    [Google Scholar]
  48. Suzich J. A. , Ghim S. J. , Palmer-Hill F. J. , White W. I. , Tamura J. K. , Bell J. A. , Newsome J. A. , Jenson A. B. , Schlegel R. . ( 1995; ). Systemic immunization with papillomavirus L1 protein completely prevents the development of viral mucosal papillomas. . Proc Natl Acad Sci U S A 92:, 11553–11557. [CrossRef] [PubMed]
    [Google Scholar]
  49. Villa L. L. , Costa R. L. , Petta C. A. , Andrade R. P. , Ault K. A. , Giuliano A. R. , Wheeler C. M. , Koutsky L. A. , Malm C. et al. & other authors ( 2005; ). Prophylactic quadrivalent human papillomavirus (types 6, 11, 16, and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase II efficacy trial. . Lancet Oncol 6:, 271–278. [CrossRef] [PubMed]
    [Google Scholar]
  50. Voss J. L. . ( 1969; ). Transmission of equine sarcoid. . Am J Vet Res 30:, 183–191.[PubMed]
    [Google Scholar]
  51. Yuan Z. , Philbey A. W. , Gault E. A. , Campo M. S. , Nasir L. . ( 2007; ). Detection of bovine papillomavirus type 1 genomes and viral gene expression in equine inflammatory skin conditions. . Virus Res 124:, 245–249. [CrossRef] [PubMed]
    [Google Scholar]
  52. Zinkernagel R. M. . ( 2003; ). On natural and artificial vaccinations. . Annu Rev Immunol 21:, 515–546. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.033670-0
Loading
/content/journal/jgv/10.1099/vir.0.033670-0
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