Inoculation of young horses with bovine papillomavirus type 1 virions leads to early infection of PBMCS prior to pseudo-sarcoid formation

Journal of General Virology

Volumn 92, Issue 10, 2011, Pages 2437-2445

  Hartl, Bettina ^a   Hainisch, Edmund K ^a   Shafti Keramat, Saeed ^b   Kirnbauer, Reinhard ^b   Corteggio, Annunziata ^c   Borzacchiello, Giuseppe ^c   Tober, Reinhard ^d   Kainzbauer, Christina ^a   Pratscher, Barbara ^a   Brandt, Sabine ^a  

^a UNIVERSITY OF VETERINARY MEDICINE   (Austria)

^b UNIVERSITY OF VIENNA   (Austria)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; ONCOPROTEIN; VIRUS ANTIBODY; VIRUS DNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BOVINE PAPILLOMAVIRUS TYPE 1; COLT; CONTROLLED STUDY; FEMALE; FILLY; FOAL; HORSE; HORSE DISEASE; IMMUNOFLUORESCENCE; MALE; NONHUMAN; PAPILLOMAVIRUS INFECTION; PERIPHERAL BLOOD MONONUCLEAR CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOTUMOR; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SKIN CANCER; VIREMIA; VIRION; VIRUS CARCINOGENESIS; VIRUS GENOME; VIRUS NEUTRALIZATION;

ANIMALS; ANTIBODIES, VIRAL; BOVINE PAPILLOMAVIRUS 1; DISEASE MODELS, ANIMAL; DNA, VIRAL; FLUORESCENT ANTIBODY TECHNIQUE, DIRECT; HORSES; LEUKOCYTES, MONONUCLEAR; NEUTRALIZATION TESTS; ONCOGENE PROTEINS, VIRAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SARCOIDOSIS; SKIN;

BOVINE PAPILLOMAVIRUS; BOVINE PAPILLOMAVIRUS TYPE 1; BOVINE PAPILLOMAVIRUS TYPE 2; EQUIDAE; PAPILLOMAVIRIDAE;

EID: 80052931403     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.033670-0     Document Type: Article

References (52)

1. Amtmann, E., Müller, H. & Sauer, G. (1980). Equine connective tissue tumors contain unintegrated bovine papilloma virus DNA. J Virol 35, 962-964.
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.
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.
4. Borzacchiello, G., Roperto, F., Campo, M. S. & Venuti, A. (2010). 1st International Workshop on Papillomavirus E5 Oncogene - a report. Virology 408, 135-137.
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.
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.
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.
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.
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.
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.
11. Campo, M. S. (2006a). Introduction. In Papillomavirus Research: From Natural History to Vaccines and Beyond, pp. 1-2. Edited by M. S. Campo. Norfolk, UK: Caister Academic Press.
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 M. S. Campo. Norfolk, UK: Caister Academic Press.
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.
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 M. S. Campo. Norfolk, UK: Caister Academic Press.
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.
16. Day, P. M., Lowy, D. R. & Schiller, J. T. (2003). Papillomaviruses infect cells via a clathrin-dependent pathway. Virology 307, 1-11.
17. de Freitas, A. C., de Carvalho, C., Brunner, O., Birgel, E. H., Jr, Melville Paiva Dellalibera, A. M., Benesi, F. J., Gregory, L., Becak, 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.
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.
19. Hainisch, E. K., Brandt, S., Shafti-Keramat, S., van den Hoven, R. & Kirnbauer, R. (2011). Safety and immunogenicity of BPV-1 L1 viruslike particles in a dose-escalation vaccination trial in horses. Equine Vet J (in press).
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.
21. Kirnbauer, R. (1996). Papillomavirus-like particles for serology and vaccine development. Intervirology 39, 54-61.
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.
23. Knottenbelt, D. C. (2005). A suggested clinical classification for the equine sarcoid. Clin Tech Equine Pract 4, 278-295.
24. Knowles, G., O'Neil, B. W. & Campo, M. S. (1996). Phenotypical characterization of lymphocytes infiltrating regressing papillomas. J Virol 70, 8451-8458.
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.
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.
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.
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.
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.
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.
31. Nasir, L. & Reid, S. W. J. (1999). Bovine papillomaviral gene expression in equine sarcoid tumours. Virus Res 61, 171-175.
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 M. S. Campo. Norfolk, UK: Caister Academic Press.
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.
34. Pastrana, D. V., Buck, C. B., Pang, Y. Y., Thompson, C. D., Castle, P. E., FitzGerald, P. C., KrügerKjaer, 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.
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.
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.
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.
38. Roperto, S., Brun, R., Paolini, F., Urraro, C., Russo, V., Borzacchiello, G., Pagnini, U., Raso, C., Rizzo, C. & 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.
39. Roperto, S., Comazzi, S., Ciusani, E., Paolini, F., Borzacchiello, G., Esposito, I., Lucà, R., Russo, V., Urraro, C. & other authors (2011). PBMCs are additional sites of productive infection of bovine papillomavirus type 2. J Gen Virol 92, 1787-1794.
40. Schiller, J. T. (2007). Papillomavirus vaccines. In The Papillomaviruses, pp. 337-369. Edited by R. Garcia & D. DiMaio. New York: Springer.
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.
42. Scott, D. W. & Miller, W. H., Jr (2003). Sarcoid. In Equine Dermat ology, pp. 719-731.St Louis, Missouri, USA: Elsevier Science.
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.
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.
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.
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.
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. & Bec ̧ ak, W. (1998). Bovine papillomavirus transmission and chromosomal aberrations: an experimental model. J Gen Virol 79, 2127-2135.
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.
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. & 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.
50. Voss, J. L. (1969). Transmission of equine sarcoid. Am J Vet Res 30, 183-191.
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.
52. Zinkernagel, R. M. (2003). On natural and artificial vaccinations. Annu Rev Immunol 21, 515-546.