1887

Abstract

Bovine papillomavirus (BPV) induces papillomas in cattle; in the great majority of cases, these regress due to the host immune response, but they can persist and progress to malignancy. Even in the absence of malignant transformation, BPV infection persists for a significant period of time before activation of the host immune system, suggesting that the host immune system is unaware of, or disabled by, BPV. E5 is the major oncoprotein of BPV, which, in addition to its transforming properties, downregulates the expression and transport to the cell surface of major histocompatibility complex class I (MHC I). Here, it is shown that co-expression of MHC I and E5 in papillomas caused by BPV-4 infection is mutually exclusive, in agreement with the inhibition of surface MHC I expression by E5 that is observed . The inhibition of MHC expression in E5-expressing papilloma cells could explain the long period that is required for activation of the immune response and has implications for the progression of papillomas to the malignant stage; absence of peptide presentation by MHC I to cytotoxic T lymphocytes would allow the infected cells to evade the host cellular immune response and allow the lesions to persist.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.80128-0
2004-10-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/85/10/vir852809.html?itemId=/content/journal/jgv/10.1099/vir.0.80128-0&mimeType=html&fmt=ahah

References

  1. Anderson R. A., Scobie L., O'Neil B. W., Grindlay G. J., Campo M. S. 1997; Viral proteins of bovine papillomavirus type 4 during the development of alimentary canal tumours. Vet J 154:69–78 [CrossRef]
    [Google Scholar]
  2. Ashrafi G. H., Tsirimonaki E., Marchetti B., O'Brien P. M., Sibbet G. J., Andrew L., Campo M. S. 2002; Down-regulation of MHC class I by bovine papillomavirus E5 oncoproteins. Oncogene 21:248–259 [CrossRef]
    [Google Scholar]
  3. Ashrafi G. H., Haghshenas M. R., Marchetti B., O'Brien P. M., Campo M. S. 2004; The E5 protein of human papillomavirus type 16 selectively down-regulates surface HLA class I. Int J Cancer (in press
    [Google Scholar]
  4. Bontkes H. J., Walboomers J. M., Meijer C. J., Helmerhorst T. J., Stern P. L. 1998; Specific HLA class I down-regulation is an early event in cervical dysplasia associated with clinical progression. Lancet 351:187–188 [CrossRef]
    [Google Scholar]
  5. Burnett S., Jareborg N., DiMaio D. 1992; Localization of bovine papillomavirus type 1 E5 protein to transformed basal keratinocytes and permissive differentiated cells in fibropapilloma tissue. Proc Natl Acad Sci U S A 89:5665–5669 [CrossRef]
    [Google Scholar]
  6. Campo M. S. 1997; Bovine papillomavirus and cancer. Vet J 154:175–188 [CrossRef]
    [Google Scholar]
  7. Campo M. S. 2002; Animal models of papillomavirus pathogenesis. Virus Res 89:249–261 [CrossRef]
    [Google Scholar]
  8. Campo M. S., O'Neil B. W., Barron R. J., Jarrett W. F. 1994; Experimental reproduction of the papilloma-carcinoma complex of the alimentary canal in cattle. Carcinogenesis 15:1597–1601 [CrossRef]
    [Google Scholar]
  9. Chandrachud L. M., O'Neil B. W., Jarrett W. F. H., Grindlay G. J., McGarvie G. M., Campo M. S. 1994; Humoral immune response to the E7 protein of bovine papillomavirus type 4 and identification of B-cell epitopes. Virology 200:98–104 [CrossRef]
    [Google Scholar]
  10. Chandrachud L. M., Grindlay G. J., McGarvie G. M., O'Neil B. W., Wagner E. R., Jarrett W. F. H., Campo M. S. 1995; Vaccination of cattle with the N-terminus of L2 is necessary and sufficient for preventing infection by bovine papillomavirus-4. Virology 211:204–208 [CrossRef]
    [Google Scholar]
  11. Chang J.-L., Tsao Y.-P., Liu D.-W., Huang S.-J., Lee W.-H., Chen S.-L. 2001; The expression of HPV-16 E5 protein in squamous neoplastic changes in the uterine cervix. J Biomed Sci 8:206–213 [CrossRef]
    [Google Scholar]
  12. Frazer I. H., Thomas R., Zhou J. 8 other authors 1999; Potential strategies utilised by papillomavirus to evade host immunity. Immunol Rev 168:131–142 [CrossRef]
    [Google Scholar]
  13. Georgopoulos N. T., Proffitt J. L., Blair G. E. 2000; Transcriptional regulation of the major histocompatibility complex (MHC) class I heavy chain, TAP1 and LMP2 genes by the human papillomavirus (HPV) type 6b, 16 and 18 E7 oncoproteins. Oncogene 19:4930–4935 [CrossRef]
    [Google Scholar]
  14. Jarrett W. F. H. 1985; The natural history of bovine papillomavirus infections. Adv Viral Oncol 5:83–102
    [Google Scholar]
  15. Kirnbauer R., Chandrachud L. M., O'Neil B. W. 7 other authors 1996; Virus-like particles of bovine papillomavirus type 4 in prophylactic and therapeutic immunization. Virology 219:37–44 [CrossRef]
    [Google Scholar]
  16. Knowles G., O'Neil B. W., Campo M. S. 1996; Phenotypical characterization of lymphocytes infiltrating regressing papillomas. J Virol 70:8451–8458
    [Google Scholar]
  17. Marchetti B., Ashrafi G. H., Tsirimonaki E., O'Brien P. M., Campo M. S. 2002; The bovine papillomavirus oncoprotein E5 retains MHC class I molecules in the Golgi apparatus and prevents their transport to the cell surface. Oncogene 21:7808–7816 [CrossRef]
    [Google Scholar]
  18. McGarvie G. M., Grindlay G. J., Chandrachud L. M., O'Neil B. W., Jarrett W. F., Campo M. S. 1995; T cell responses to BPV-4 E7 during infection and mapping of T cell epitopes. Virology 206:504–510 [CrossRef]
    [Google Scholar]
  19. O'Brien P. M., Campo M. S. 2002; Evasion of host immunity directed by papillomavirus-encoded proteins. Virus Res 88:103–117 [CrossRef]
    [Google Scholar]
  20. Tindle R. W. 2002; Immune evasion in human papillomavirus-associated cervical cancer. Nat Rev Cancer 2:59–64 [CrossRef]
    [Google Scholar]
  21. Toye P. G., MacHugh N. D., Bensaid A. M., Alberti S., Teale A. J., Morrison W. I. 1990; Transfection into mouse L cells of genes encoding two serologically and functionally distinct bovine class I MHC molecules from a MHC-homozygous animal: evidence for a second class I locus in cattle. Immunology 70:20–26
    [Google Scholar]
  22. Tsirimonaki E., O'Neil B. W., Williams R., Campo M. S. 2003; Extensive papillomatosis of the bovine upper gastrointestinal tract. J Comp Pathol 129:93–99 [CrossRef]
    [Google Scholar]
  23. Vambutas A., DeVoti J., Pinn W., Steinberg B. M., Bonagura V. R. 2001; Interaction of human papillomavirus type 11 E7 protein with TAP-1 results in the reduction of ATP-dependent peptide transport. Clin Immunol 101:94–99 [CrossRef]
    [Google Scholar]
  24. zur Hausen H. 2002; Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2:342–350 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.80128-0
Loading
/content/journal/jgv/10.1099/vir.0.80128-0
Loading

Data & Media loading...

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