1887

Journal of General Virology header logo

Volume 81, Issue 2

α6 integrin is not the obligatory cell receptor for bovine papillomavirus type 4 Free

Abstract

Recently, α6 integrin has been proposed as the epithelial cell receptor for papillomavirus. This study investigated whether α6 integrin is the cellular receptor for bovine papillomavirus type 4 (BPV-4), which is strictly epitheliotropic and infects the mucous epithelium of the upper digestive tract. Primary bovine mucosal keratinocytes from the palate of a foetus (PalK) displayed high levels of α6 integrin; matched primary fibroblasts from the same biopsy (PalF) expressed almost no α6 integrin. However, BPV-4 bound both PalK and PalF to similar, saturable levels. Native BPV-4 virions infected PalK , as detected by RT–PCR of E7 RNA. Infection could be blocked by excess virus-like particles (VLPs) and by neutralizing antisera against L1–L2 and L1 VLPs or by denaturation of the virions, supporting the view that infection mimics the process . α6 integrin-negative human keratinocyte cell lines were derived from patients affected by junctional epidermolysis bullosa presenting genetic lesions in their hemidesmosomes. The level of α6 integrin expression was determined in these cell lines by immunofluorescence and FACS. Despite the absence of α6 integrin expression by BO-SV cells, they were bound by BPV-4 to similar, saturable levels as normal keratinocytes, KH-SV. Furthermore, BO-SV and KH-SV cells were both infected by BPV-4 to apparently the same extent as PalK cells. These results are consistent with the conclusion that α6 integrin is not the obligatory receptor for a bovine mucosotropic papillomavirus.

  • Received:
  • Accepted:
  • Published Online:
© Microbiology Society
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-2-327
2000-02-01
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/2/0810327a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-2-327&mimeType=html&fmt=ahah

References

  1. Agrez, M. V., Shafren, D. R., Gu, X., Cox, K., Sheppard, D. & Barry, R. D.(1997). Integrin alpha v beta 6 enhances coxsackievirus B1 lytic infection of human colon cancer cells.Virology 239, 71-77.[CrossRef] [Google Scholar]
  2. Aplin, J. D., Dawson, S. & Seif, M. W.(1996). Abnormal expression of integrin alpha 6 beta 4 in cervical intraepithelial neoplasia.British Journal of Cancer 74, 240-245.[CrossRef] [Google Scholar]
  3. Beutner, K. R. & Tyring, S.(1997). Human papillomavirus and human disease.American Journal of Medicine 102, 9-15. [Google Scholar]
  4. Broder, C. C. & Dimitrov, D. S.(1996). HIV and the 7-transmembrane domain receptors.Pathobiology 64, 171-179.[CrossRef] [Google Scholar]
  5. Campo, M. S.(1987). Papillomas and cancer in cattle.Cancer Surveys 6, 39-54. [Google Scholar]
  6. Campo, M. S.(1997). Bovine papillomavirus and cancer.Veterinary Journal 154, 175-188.[CrossRef] [Google Scholar]
  7. Cao, W., Henry, M. D., Borrow, P., Yamada, H., Elder, J. H., Ravkov, E. V., Nichol, S. T., Compans, R. W., Campbell, K. P. & Oldstone, M. B.(1998). Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus.Science 282, 2079-2081.[CrossRef] [Google Scholar]
  8. Chandrachud, L. M., Grindlay, G. J., McGarvie, G. M., O’Neil, B. W., Wagner, E. R., Jarrett, W. F. & 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]
  9. Chen, Y., Ghim, S.-j., Jenson, A. B. & Schlegel, R.(1998). Mutant canine oral papillomavirus L1 capsid proteins which form virus-like particles but lack native conformational epitopes.Journal of General Virology 79, 2137-2146. [Google Scholar]
  10. Chomczynski, P. & Sacchi, N.(1987). Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction.Analytical Biochemistry 162, 156-159. [Google Scholar]
  11. Christensen, N. D., Höpfl, R., DiAngelo, S. L., Cladel, N. M., Patrick, S. D., Welsh, P. A., Budgeon, L. R., Reed, C. A. & Kreider, J. W.(1994). Assembled baculovirus-expressed human papillomavirus type 11 L1 capsid protein virus-like particles are recognized by neutralizing monoclonal antibodies and induce high titres of neutralizing antibodies.Journal of General Virology 75, 2271-2276.[CrossRef] [Google Scholar]
  12. Christensen, N. D., Reed, C. A., Cladel, N. M., Han, R. & Kreider, J. W.(1996). Immunization with viruslike particles induces long-term protection of rabbits against challenge with cottontail rabbit papillomavirus.Journal of Virology 70, 960-965. [Google Scholar]
  13. Coulson, B. S., Londrigan, S. L. & Lee, D. J.(1997). Rotavirus contains integrin ligand sequences and a disintegrin-like domain that are implicated in virus entry into cells.Proceedings of the National Academy of Sciences, USA 94, 5389-5394.[CrossRef] [Google Scholar]
  14. de Villiers, E. M.(1998). Human papillomavirus infections in skin cancers.Biomedicine & Pharmacotherapy 52, 26-33.[CrossRef] [Google Scholar]
  15. Evander, M., Frazer, I. H., Payne, E., Qi, Y. M., Hengst, K. & McMillan, N. A.(1997). Identification of the alpha6 integrin as a candidate receptor for papillomaviruses.Journal of Virology 71, 2449-2456. [Google Scholar]
  16. Gache, Y., Romero-Graillet, C., Spadafora, A., Lepinard, C., Descamps, P., Bardon, C. B., Ortonne, J. P. & Meneguzzi, G.(1998). A novel homozygous mutation affecting integrin α6 in a case of junctional epidermolysis bullosa with pyloric atresia detected in utero by ultrasound examination.Journal of Investigative Dermatology 111, 914-916.[CrossRef] [Google Scholar]
  17. Gaukroger, J. M., Chandrachud, L. M., O’Neil, B. W., Grindlay, G. J., Knowles, G. & Campo, M. S.(1996). Vaccination of cattle with bovine papillomavirus type 4 L2 elicits the production of virus-neutralizing antibodies.Journal of General Virology 77, 1577-1583.[CrossRef] [Google Scholar]
  18. Henry, M. D. & Campbell, K. P.(1998). A role for dystroglycan in basement membrane assembly.Cell 95, 859-870.[CrossRef] [Google Scholar]
  19. Huttunen, P., Heino, J. & Hyypia, T.(1997). Echovirus 1 replication, not only virus binding to its receptor, VLA-2, is required for the induction of cellular immediate-early genes.Journal of Virology 71, 4176-4180. [Google Scholar]
  20. Kennel, S. J., Foote, L. J., Falcioni, R., Sonnenberg, A., Stringer, C. D., Crouse, C. & Hemler, M. E.(1989). Analysis of the tumor-associated antigen TSP-180. Identity with alpha 6-beta 4 in the integrin superfamily.Journal of Biological Chemistry 264, 15515-15521. [Google Scholar]
  21. Kirnbauer, R.(1996). Papillomavirus-like particles for serology and vaccine development.Intervirology 39, 54-61. [Google Scholar]
  22. Kirnbauer, R., Taub, J., Greenstone, H., Roden, R., Durst, M., Gissmann, L., Lowy, D. R. & Schiller, J. T.(1993). Efficient self-assembly of human papillomavirus type 16 L1 and L1-L2 into virus-like particles.Journal of Virology 67, 6929-6936. [Google Scholar]
  23. 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] [Google Scholar]
  24. Lowy, D. R. & Schiller, J. T. (1998). Papillomaviruses and cervical cancer: pathogenesis and vaccine development. Journal of the National Cancer Institute Monographs, 27–30.
  25. McMillan, N. A., Payne, E., Frazer, I. H. & Evander, M.(1999). Expression of the alpha6 integrin confers papillomavirus binding upon receptor-negative B-cells.Virology 261, 271-279.[CrossRef] [Google Scholar]
  26. Miquel, C., Gagnoux-Palacios, L., Durand-Clement, M., Marinkovich, P., Ortonne, J. P. & Meneguzzi, G.(1996). Establishment and characterization of cell line LSV5 that retains the altered adhesive properties of human junctional epidermolysis bullosa keratinocytes.Experimental Cell Research 224, 279-290.[CrossRef] [Google Scholar]
  27. Montgomery, R. I., Warner, M. S., Lum, B. J. & Spear, P. G.(1996). Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family.Cell 87, 427-436.[CrossRef] [Google Scholar]
  28. Morgan, I. M., Grindlay, G. J. & Campo, M. S.(1999). The bovine papillomavirus type 4 long control region contains an epithelial specific enhancer.Journal of General Virology 80, 23-27. [Google Scholar]
  29. Muller, M., Gissmann, L., Cristiano, R. J., Sun, X. Y., Frazer, I. H., Jenson, A. B., Alonso, A., Zentgraf, H. & Zhou, J.(1995). Papillomavirus capsid binding and uptake by cells from different tissues and species.Journal of Virology 69, 948-954. [Google Scholar]
  30. O’Brien, P. M., Aitken, R., O’Neil, B. W. & Campo, M. S.(1999). Generation of native bovine mAbs by phage display.Proceedings of the National Academy of Sciences, USA 96, 640-645.[CrossRef] [Google Scholar]
  31. Ohrui, T., Yamaya, M., Sekizawa, K., Terajima, M., Yamada, N., Suzuki, T., Okinaga, S., Hoshi, H., Suzuki, H. & Sasaki, H. (1996). [Rhinovirus infection and expression of adhesion molecules in human tracheal epithelium]. Nihon Kyobu Shikkan Gakkai Zasshi(Japanese Journal of Thoracic Diseases) 34, 121–125 (in Japanese).
  32. Qi, Y. M., Peng, S. W., Hengst, K., Evander, M., Park, D. S., Zhou, J. & Frazer, I. H.(1996). Epithelial cells display separate receptors for papillomavirus VLPs and for soluble L1 capsid protein.Virology 216, 35-45.[CrossRef] [Google Scholar]
  33. Roden, R. B., Kirnbauer, R., Jenson, A. B., Lowy, D. R. & Schiller, J. T.(1994). Interaction of papillomaviruses with the cell surface.Journal of Virology 68, 7260-7266. [Google Scholar]
  34. Rose, R. C., Reichman, R. C. & Bonnez, W.(1994). Human papillomavirus (HPV) type 11 recombinant virus-like particles induce the formation of neutralizing antibodies and detect HPV-specific antibodies in human sera.Journal of General Virology 75, 2075-2079.[CrossRef] [Google Scholar]
  35. Ruzzi, L., Gagnoux-Palacios, L., Pinola, M., Belli, S., Meneguzzi, G., D’Alessio, M. & Zambruno, G.(1997). A homozygous mutation in the integrin alpha6 gene in junctional epidermolysis bullosa with pyloric atresia.Journal of Clinical Investigation 99, 2826-2831.[CrossRef] [Google Scholar]
  36. Schiller, J. T. & Lowy, D. R.(1996). Papillomavirus-like particles and HPV vaccine development.Seminars in Cancer Biology 7, 373-382.[CrossRef] [Google Scholar]
  37. Shafren, D. R., Dorahy, D. J., Ingham, R. A., Burns, G. F. & Barry, R. D.(1997). Coxsackievirus A21 binds to decay-accelerating factor but requires intercellular adhesion molecule 1 for cell entry.Journal of Virology 71, 4736-4743. [Google Scholar]
  38. Sibbet, G. J., Cuthill, S. & Campo, M. S.(1995). The enhancer in the long control region of human papillomavirus type 16 is up-regulated by PEF-1 and down-regulated by Oct-1.Journal of Virology 69, 4006-4011. [Google Scholar]
  39. Smith, L. H., Foster, C., Hitchcock, M. E. & Isseroff, R.(1993). In vitro HPV-11 infection of human foreskin.Journal of Investigative Dermatology 101, 292-295.[CrossRef] [Google Scholar]
  40. Sonnenberg, A., Janssen, H., Hogervorst, F., Calafat, J. & Hilgers, J.(1987). A complex of platelet glycoproteins Ic and IIa identified by a rat monoclonal antibody.Journal of Biological Chemistry 262, 10376-10383. [Google Scholar]
  41. Suzuki, Y. (1997). [Host range of influenza viruses and their receptor binding specificities]. Nippon Rinsho (Japanese Journal of Clinical Medicine) 55, 2640–2647 (in Japanese).
  42. Terpe, H. J., Stark, H., Ruiz, P. & Imhof, B. A.(1994). Alpha 6 integrin distribution in human embryonic and adult tissues.Histochemistry 101, 41-49.[CrossRef] [Google Scholar]
  43. Vidal, F., Aberdam, D., Miquel, C., Christiano, A. M., Pulkkinen, L., Uitto, J., Ortonne, J. P. & Meneguzzi, G.(1995). Integrin beta-4 mutation associated with junctional epidermolysis bullosa with pyloric atresia.Nature Genetics 10, 229-234.[CrossRef] [Google Scholar]
  44. Volpers, C., Unckell, F., Schirmacher, P., Streeck, R. E. & Sapp, M.(1995). Binding and internalization of human papillomavirus type 33 virus-like particles by eukaryotic cells.Journal of Virology 69, 3258-3264. [Google Scholar]
  45. Whitbeck, J. C., Peng, C., Lou, H., Xu, R., Willis, S. H., Ponce de Leon, M., Peng, T., Nicola, A. V., Montgomery, R. I., Warner, M. S., Soulika, A. M., Spruce, L. A., Moore, W. T., Lambris, J. D., Spear, P. G., Cohen, G. H. & Eisenberg, R. J.(1997). Glycoprotein D of herpes simplex virus (HSV) binds directly to HVEM, a member of the tumor necrosis factor receptor superfamily and a mediator of HSV entry.Journal of Virology 71, 6083-6093. [Google Scholar]
  46. White, W. I., Wilson, S. D., Bonnez, W., Rose, R. C., Koenig, S. & Suzich, J. A.(1998). In vitro infection and type-restricted antibody-mediated neutralization of authentic human papillomavirus type 16.Journal of Virology 72, 959-964. [Google Scholar]
  47. Wickham, T. J., Mathias, P., Cheresh, D. A. & Nemerow, G. R.(1993). Integrins alpha v beta 3 and alpha v beta 5 promote adenovirus internalization but not virus attachment.Cell 73, 309-319.[CrossRef] [Google Scholar]
  48. Wu, L., Gerard, N. P., Wyatt, R., Choe, H., Parolin, C., Ruffing, N., Borsetti, A., Cardoso, A. A., Desjardin, E., Newman, W., Gerard, C. & Sodroski, J.(1996). CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5.Nature 384, 179-183.[CrossRef] [Google Scholar]
  49. Zhou, J., Sun, X. Y., Davies, H., Crawford, L., Park, D. & Frazer, I. H.(1992). Definition of linear antigenic regions of the HPV16 L1 capsid protein using synthetic virion-like particles.Virology 189, 592-599.[CrossRef] [Google Scholar]
  50. Zhou, J., Stenzel, D. J., Sun, X.-Y. & Frazer, I. H.(1993). Synthesis and assembly of infectious bovine papillomavirus particles in vitro.Journal of General Virology 74, 763-768.[CrossRef] [Google Scholar]
  51. Zur Hausen, H. & Rosl, F.(1994). Pathogenesis of cancer of the cervix.Cold Spring Harbor Symposia on Quantitative Biology 59, 623-628.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-2-327
Loading
α6 integrin is not the obligatory cell receptor for bovine papillomavirus type 4
J. Gen. Virol. 81, 327 (2000); https://doi.org/10.1099/0022-1317-81-2-327
/content/journal/jgv/10.1099/0022-1317-81-2-327
/content/journal/jgv/10.1099/0022-1317-81-2-327
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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