Immunological and clinical responses in women with vulval intraepithelial neoplasia vaccinated with a vaccinia virus encoding human papillomavirus 16/18 oncoproteins

Cancer Research

Volumn 63, Issue 18, 2003, Pages 6032-6041

  Davidson, Emma J ^a,b   Boswell, Christopher M ^c   Sehr, Peter ^d   Pawlita, Michael ^d   Tomlinson, Anne E ^b   McVey, Rhona J ^b   Dobson, Jennifer ^c   Roberts, John St C ^c   Hickling, Julian ^c   Kitchener, Henry C ^b   Stern, Peter L ^a  

^a CHRISTIE HOSPITAL   (United Kingdom)

^b ST MARY S HOSPITAL   (United Kingdom)

^c Cantab Pharmaceuticals Ltd   (United Kingdom)

^d GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD68 ANTIGEN; CD8 ANTIGEN; GLUTATHIONE TRANSFERASE; HLA A2 ANTIGEN; HYBRID PROTEIN; ONCOPROTEIN; T6 ANTIGEN; UNCLASSIFIED DRUG; VIRUS E6 PROTEIN; VIRUS E7 PROTEIN;

ANTIBODY RESPONSE; ARTICLE; CANCER IMMUNOTHERAPY; CELL LYSATE; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; DRUG RESPONSE; DRUG SAFETY; DRUG TOLERABILITY; EDEMA; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLU LIKE SYNDROME; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE PROLIFERATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SKIN MANIFESTATION; SORE THROAT; T LYMPHOCYTE; UTERINE CERVIX CARCINOMA IN SITU; VACCINATION; VACCINATION REACTION; VACCINIA VIRUS; VIRUS LOAD; VIRUS RECOMBINANT; VIRUS STRAIN; VULVA CARCINOMA; VULVA CARCINOMA IN SITU; WART VIRUS;

CANCER VACCINES; CARCINOMA IN SITU; DNA-BINDING PROTEINS; FEMALE; HLA-A2 ANTIGEN; HUMANS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; REPRESSOR PROTEINS; TUMOR VIRUS INFECTIONS; VACCINIA VIRUS; VIRAL VACCINES; VULVAR NEOPLASMS;

EID: 0141619282     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (63)

1. van Beurden, M., ten Kate, F. J., Smits, H. L., Berkhout, R. J., de Craen, A. J., van der Vange, N., Lammes, F. B., and ter Schegget, J. Multifocal vulvar intraepithelial neoplasia grade III and multicentric lower genital tract neoplasia is associated with transcriptionally active human papillomavirus. Cancer (Phila.), 75: 2879-2884, 1995.
2. Kagie, M. J., Kenter, G. G., Zomerdijk-Nooijen, Y., Hermans, J., Schuuring, E., Timmers, P. J., Trimbos, J. B., and Fleuren, G. J. Human papillomavirus infection in squamous cell carcinoma of the vulva, in various synchronous epithelial changes and in normal vulvar skin. Gynecol. Oncol., 67: 178-183, 1997.
3. Abdel-Hady, E. S., Martin-Hirsch, P., Duggan-Keen, M., Stern, P. L., Moore, J. V., Corbitt, G., Kitchener, H. C., and Hampson, I. N. Immunological and viral factors associated with the response of vulval intraepithelial neoplasia to photodynamic therapy. Cancer Res., 61: 192-196, 2001.
4. Sturgeon, S. R., Brinton, L. A., Devesa, S. S., and Kurman, R. J. In situ and invasive vulvar cancer incidence trends (1973-1987). Am. J. Obstet. Gynecol., 166: 1482-1485, 1992.
5. Jones, R. W., Baranyai, J., and Stables, S. Trends in squamous cell carcinoma of the vulva: the influence of vulvar intraepithelial neoplasia. Obstet. Gynecol., 90: 448-455, 1997.
6. Jones, R. W., and Rowan, D. M. Vulvar intraepithelial neoplasia III: a clinical study of the outcome in 113 cases with relation to the later development of invasive vulvar carcinoma. Obstet. Gynecol., 84: 741-745, 1994.
7. Herod, J. J. O., Shafi, M. I., Rollason, T. P., Jordan, J. A., and Luesley, D. M. Vulvar intraepithelial neoplasia: long term follow up of treated and untreated women. Br. J. Obstet. Gynaecol., 103: 446-452, 1996.
8. Modesitt, S. C., Waters, A. B., Walton, L., Fowler, W. C., and Van Le, L. Vulvar intraepithelial neoplasia III: occult cancer and the impact of margin status on recurrence. Obstet. Gynecol., 92: 962-966, 1998.
9. Jones, R. W. The natural history of vulvar intraepithelial neoplasia. Br. J. Obstet. Gynaecol., 102: 764-766, 1995.
10. Shaft, M. I., Luesley, D. M., Byme, P., Samra, J. S., Redman, C. W., Jordan, J. A., and Rollason, T. P. Vulval intraepithelial neoplasia: management and outcome. Br. J. Obstet. Gynaecol., 96: 1339-1344, 1989.
11. Stanley, M. A. Human papillomavirus and cervical carcinogenesis. Best Pract. Res. Clin. Obstet. Gynaecol., 15: 663-676, 2001.
12. Feltkamp, M. C. W., Smits, H. L., Vierboom, M. P. M., Minnaar, R. P., de Jongh, B. M., Drijfhout, J. W., ter Schegget, J., Melief, C. J. M., and Kast, W. M. Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumour induced by human papillomavirus type 16-transformed cells. Eur. J. Immunol., 23: 2242-2249, 1993.
13. De Bruijn, M. L. H., Schuurhuis, D. H., Vierboom, M. P. M., Vermeulen, H., de Cock, K. A. J., Ooms, M. E., Ressing, M. E., Toebes, M., Franken, K. L. M. C., Drijfhout, J. W., Ottenhoff, T. H. M., Offringa, R., and Melief, C. J. M. Immunisation with human papillomavrius type 16 (HPV16) oncoprotein-loaded dendritic cells as well as protein in adjuvant induces MHC class I-restricted protection to HPV16-induced tumor cells. Cancer Res., 58: 724-731, 1998.
14. Boursnell, M. E., Rutherford, E., Hickling, J. K., Rollinson, E. A., Munro, A. J., Rolley, N., McLean, C. S., Borysiewicz, L. K., Vousden, K., and Inglis, S. C. Construction and characterisation of a recombinant vaccinia virus expressing human papillomavirus proteins for immunotherapy of cervical cancer. Vaccine, 14: 1485-1494, 1996.
15. Borysiewicz, L. K., Fiander, A., Nimako, M., Man, S., Wilkinson, G. W. G., Westmorland, D., Evans, A. S., Adams, M., Stacey, S. N., Boursall, M. E. G., Rutherford, E., Hickling, J. K., and Inglis, S. C. A recombinant vaccinia virus encoding human papillomavirus types 16 and 18, E6 and E7 proteins as immunotherapy for cervical cancer. Lancet, 347: 1523-1527, 1996.
16. Kaufman, A., Stern, P. L., Rankin, E. M., Sommer, H., Schneider, A., Adams, M., Kitchener, H. C., Bauknecht, T., Wagner, U., Kroon, K., Hickling, J., Stacey, S., Onon, T., Gillard, J., Wanders, J., Roberts, J., and Zwierzina, H. Safety and immunogenicity of TA-HPV™, a recombinant vaccinia virus expressing modified HPV16 and 18 E6 and E7 genes, in women with progressive cervical cancer. Clin. Cancer Res., 8: 3676-3685, 2002.
17. Buckley, C. H., Butler, E. B., and Fox, H. Vulvar intraepithelial neoplasia and microinvasive carcinoma of the vulva. J. Clin. Pathol., 37: 1201-1211, 1984.
18. Bauer, H. M., Greer, C. E., and Manos, M. M. Determination of genital human papillomavirus infection by consensus PCR amplification. In: C. S. Herrington and J. O. D. McGee (eds.), Diagnostic Molecular Pathology: a Practical Approach, Vol. 2, pp. 131-152. Cambridge, United Kingdom: Oxford University Press, 1992.
19. De Roda Husman, A. M., Walboomers, J. M. M., van den Brule, A. J. C., Meijer, C. J. L. M., and Snijders, P. J. F. The use of general primers Gp5 and Gp6 elongated at their 3′ ends with adjacent highly conserved sequences improves papillomavirus detection by PCR. J. Gen. Virol., 76: 1057-1062, 1995.
20. Soler, C., Allibert, P., Chardonnet, Y., Cros, P., Mandrand, B., and Thivolet, J. Detection of human papillomavirus types 6, 11, 16 and 18 in mucosal and cutaneous lesions by the multiplex polymerase chain reaction. J. Virol. Methods, 35: 143-157, 1991.
21. Van den Brule, A. J. C., Meijer, C. J. L. M., Bakels, V., Kenemans, P., and Walboomers, J. M. M. Rapid human papillomavirus detection in cervical scrapes by combined general primers mediated and type specific polymerase chain reaction. J. Clin. Microbiol., 28: 2739-2743, 1990.
22. Vandenvelde, C., Scheen, R., Van Pachterbeke, C., Loriaux, C., Decelle, J., Hubert, T., Delhaye, C., Cattor, J. P., Duys, M., and Van Beers, D. Prevalence of high risk genital papillomaviruses in the Belgian female population determined by fast multiplex polymerase chain reaction. J. Med. Virol., 36: 279-282, 1992.
23. Heid, C. A., Stevens, J., Livak, K. J., and Williams, P. M. Real time quantitative PCR. Genome Res., 6: 986-994, 1996.
24. van Duin, M., Snijders, P. J. F., Schrijnemakers, H. F. J., Voorhorst, F. J., Rozendaal, L., Nobbenhuis, M. A. E., van den Brule, A. J. C., Verheijen, R. H. M., Helmerhorst, T. J., and Meijer, C. J. L. M. Human papillomavirus load in normal and abnormal cervical scrapes: an indicator of CIN II/III and viral clearance. Int. J. Cancer, 98: 590-595, 2002.
25. Sehr, P., Zumbach, K., and Pawlita, M. A generic capture ELISA for recombinant proteins fused to glutathione S-transferase: validation for HPV serology. J. Immunol. Methods, 253: 153-162, 2001.
26. Davidson, E. J., Sehr, P., Faulkner, R. L., Parish, J. L., Gaston, K., Moore, R. A., Pawlita, M., Kitchener, H. C., and Stern, P. L. Human papillomavirus type 16 E2- and L1-specific serological and T-cell responses in women with vulval intraepithelial neoplasia. J. Gen. Virol., 84: 2089-2097, 2003.
27. Reid, R. Superficial laser vulvectomy. III. A new surgical technique for appendage-conserving ablation of refractory condylomas and vulvar intraepithelial neoplasia. Am. J. Obstet. Gynecol., 152: 504-509, 1985.
28. Reid, R., Greenberg, M. D., Lorincz, A. T., Daoud, Y., Pizzuti, D., and Stoler, M. Superficial laser vulvectomy. IV. Extended laser vaporization and adjunctive 5-fluorouracil therapy of human papillomavirus-associated vulvar disease. Obstet. Gynecol., 76: 439-448, 1990.
29. Martin-Hirsch, P. L., Whitehurst, C., Buckley, C. H., Moore, J. V., and Kitchener, H. C. Photodynamic treatment for lower genital tract neoplasia. Lancet, 351: 1403, 1998.
30. Friedrich, E. G. Reversible vulvar atypia. Obstet. Gynecol., 39: 173-181, 1972.
31. Skinner, M. S., Sternberg, W. H., Ichinose, H., and Collins, J. Spontaneous regression of Bowenoid atypia of the vulva. Obstet. Gynecol., 42: 40-46, 1973.
32. Jones, R. W., and Rowan, D. M. Spontaneous regression of vulvar intraepithelial neoplasia 2-3. Obstet. Gynecol., 96: 470-472, 2000.
33. Thuis, Y. N., Campion, M., Fox, H., and Hacker, N. F. Contemporary experience with the management of vulvar intraepithaliel neoplasia. Int. J. Gynecol. Cancer, 10: 223-227, 2000.
34. van Beurden, M., van der Vange, N., ten Kate, F. J. W., de Craen, A. J., Schilthuis, M. S., and Lammes, F. B. Restricted surgical management of vulvar intraepithelial neoplasia 3: focus on exclusion of invasion and on relief of symptoms. Int. J. Gynecol. Cancer, 8: 73-77, 1998.
35. McCutcheon, M., Wehner, N., Wensky, A., Kushner, M., Doan, S., Hsiao, L., Calabresi, P., Ha, T., Tran, T. V., Tate, K. M., Winkelhake, J., and Spack, E. G. A sensitive ELISPOT assay to detect low-frequency human T lymphocytes. J. Immunol. Methods, 210: 149-166, 1997.
36. Schmittel, A., Keilholz, U., and Scheibenbogen, C. Evaluation of the interferon-γ ELISPOT-assay for quantification of peptide specific T lymphocytes from peripheral blood. J. Immunol. Methods, 210: 167-174, 1997.
37. Davidson, E. J., Davidson, J. A., Sterling, J. C., Baldwin, P. J. W., Kitchener, H. C., and Stern, P. L. Association between human leukocyte antigen polymorphism and human papillomavirus 16-positive vulval intraepithelial neoplasia in British women. Cancer Res., 63: 400-403, 2003.
38. Nakagawa, M., Stites, D. P., Patel, S., Farhat, S., Scott, M., Hills, N. K., Palefsky, J. M., and Moscicki, A. B. Persistence of human papillomavirus type 16 infection is associated with lack of cytotoxic T lymphocyte response to the E6 antigens. J. Infect. Dis., 182: 595-598, 2000.
39. Okabayashi, M., Angell, M. G., Christensen, N. D., and Kreider, J. W. Morphometric analysis and identification of infiltrating leucocytes in regressing and progressing Shope rabbit papillomas. Int. J. Cancer, 49: 919-923, 1991.
40. Coleman, N., Birley, H. D. L., Renton, A. M., Hanna, N. F., Ryait, B. K., Byrne, M., Taylor Robinson, D., and Stanley, M. A. Immunological events in regressing genital warts. Am. J. Clin. Pathol., 102: 768-774, 1994.
41. Vardy, D. A., Baadsgaard, O., Hansen, E. R., Lisby, S., and Vejlsgaard, G. L. The cellular immune response to human papillomavirus infection. Int. J. Derrnatol., 29: 603-610, 1990.
42. Frazer, I. H. Immunology of papillomavirus infection. Curr. Opin. Immunol., 8: 484-491, 1996.
43. Stern, P. L., Brown, M., Stacey, S. N., Kitchener, H. C., Hampson, I., Abdel-Hady, E.-S., and Moore, J. V. Natural HPV immunity and vaccination strategies. J. Clin. Virol., 19: 57-66, 2000.
44. Becker, C., Pohla, H., Frankenberger, B., Schuler, T., Assenmacher, M., Schendel, D. J., and Blankenstein, T. Adoptive tumor therapy with T lymphocytes enriched through an IFN-γ capture assay. Nat. Med., 7: 1159-1162, 2001.
45. de Gruiji, T. D., Bontkes, H. J., Walboomers, J. M., Stukart, M. J., Doekhie, F. S., Remmink, A. J., Helmerhorst, T. J., Verheijen, R. H., Duggan Keen, M. F., Stern, P. L., Meijer, C. J., and Scheper, R. J. Differential T helper cell responses to human papillomavirus type 16 E7 related to viral clearance or persistence in patients with cervical neoplasia: a longitudinal study. Cancer Res., 58: 1700-1706, 1998.
46. Bontkes, H. J., de Gruijl, T. D., van den Muysenberg, A. J., Verheijen, R. H., Stukart, M. J., Meijer, C. J., Scheper, R. J., Stacey, S. N., Duggan Keen, M. F., Stern, P. L., Man, S., Borysiewicz, L. K., and Walboomers, J. M. Human papillomavirus type 16 E6/E7-specific cytotoxic T lymphocytes in women with cervical neoplasia. Int. J. Cancer, 88: 92-98, 2000.
47. Keene, J. A., and Forman, J. Helper activity is required for the in vivo generation of cytotoxic T lymphocytes. J. Exp. Med., 155: 768-782, 1982.
48. + T-helper and T-killer cell. Nature (Lond.), 393: 474-478, 1998.
49. Connor, J. P., Ferrer, K., Kane, J. P., and Goldberg, J. M. Evaluation of Langerhans' cells in the cervical epithelium of women with cervical intraepithelial neoplasia. Gynecol. Oncol., 75: 130-135, 1999.
50. Nickoloff, B. J., and Turka, L. A. Immunological functions of non-professional antigen-presenting cells: new insights from studies of T-cell interactions with keratinocytes. Immunol. Today, 15: 464-469, 1994.
51. al Saleh, W., Giannini, S. L., Jacobs, N., Moutschen, M., Doyen, J., Boniver, J., and Delvenne, P. Correlation of T-helper secretory differentiation and types of antigen-presenting cells in squamous intraepithelial lesions of the uterine cervix. J. Pathol., 184: 283-290, 1998.
52. Coca, S., Perez-Piqueras, J., Martinez, D., Colmenarejo, A., Saez, M. A., Vallejo, C., Martos, J. A., and Moreno, M. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma. Cancer (Phila.), 79: 2320-2328, 1997.
53. Bontkes, H. J., de Gruijl, T. D., Walboomers, J. M., van den Muysenberg, A. J., Gunther, A. W., Scheper, R. J., Meijer, C. J., and Kummer, J. A. Assessment of cytotoxic T-lymphocyte phenotype using the specific markers granzyme B and TIA-1 in cervical neoplastic lesions. Br. J. Cancer, 76: 1353-1360, 1997.
54. Weinberg, A. D. OX40: targeted immunotherapy-implications for tempering autoimmunity and enhancing vaccines. Trends Immunol., 23: 102-109, 2002.
55. Passmore, J. A., Burch, V. C., Shephard, E. G., Marais, D. J., Allan, B., Kay, P., Rose, R. C., and Williamson, A. L. Single-cell cytokine analysis allows detection of cervical T-cell responses against human papillomavirus type 16 L1 in women infected with genital HPV. J. Med. Virol., 67: 234-240, 2002.
56. de Gruijl, T. D., Bontkes, H. J., van den Muysenberg, A. J., van Oostveen, J. W., Stukart, M. J., Verheijen, R. H., van der Vange, N., Snijders, P. J., Meijer, C. J., Walboomers, J. M., and Scheper, R. J. Differences in cytokine mRNA profiles between premalignant and malignant lesions of the uterine cervix. Eur. J. Cancer, 35: 490-497, 1999.
57. El-Sherif, A. M., Seth, R., Tighe, P. J., and Jenkins, D. Quantitative analysis of IL-10 and IFN-γ mRNA levels in normal cervix and human papillomavirus type 16 associated cervical precancer. J. Pathol., 195: 179-185, 2001.
58. Peitsaro, P., Johansson, B., and Syrjanen, S. Integrated human papillomavirus type 16 is frequently found in cervical cancer precursors as demonstrated by a novel quantitative real-time PCR technique. J. Clin. Microbiol., 40: 886-891, 2002.
59. Gjerdrum, L. M., Lielpetere, I., Rasmussen, L. M., Bendix, K., and Hamilton-Dutoit, S. Laser-assisted microdissection of membrane-mounted paraffin section for polymerase chain reaction analysis: identification of cell populations using immunohistochemistry and in situ hybridisation. J. Mol. Diagn., 3: 105-110, 2001.
60. Lehmann, U., and Kreipe, H. Real-time PCR analysis of DNA and RNA extracted from formalin-fixed and paraffin-embedded biopsies. Methods, 25: 409-418, 2001.
61. Hu, X., Pang, T., Asplund, A., Pontén, J., and Nistér, M. Clonality analysis of synchronous lesions of cervical carcinoma based on X chromosome inactivation polymorphism, human papillomavirus type 16 genome mutations, and loss of heterozygosity. J. Exp. Med., 195: 845-854, 2002.
62. Stern, P. L., Faulkner, R., Veranes, E. C., and Davidson, E. J. The role of human papillomavirus vaccines in cervical neoplasia. Best Practice & Research Obstet. Gynaecol., 15: 783-799, 2001.
63. van der Burg, S. H., Kwappenberg, K. M., O'Neill, T., Brandt, R. M., Melief, C. J., Hickling, J. K., and Offringa, R. Pre-clinical safety and efficacy of TA-CIN, a recombinant HPV16 L2E6E7 fusion protein vaccine, in homologous and heterologous prime-boost regimens. Vaccine, 19: 3652-3660, 2001.