Promises and challenges of human papillomavirus vaccines for cervical cancer

References

• Munger K, Phelps WC, Bubb V, Howley PM, Schlegel R. The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J. Virol.63, 4417–4421 (1989).
   PubMed Web of Science ®Google Scholar
• Dyson N, Howley PM, Munger K, Harlow E. The human papillomavirus-16 E7 oncoprotein is able to bind the retinoblastoma gene product. Science243, 934–937 (1989).
   PubMed Web of Science ®Google Scholar
• Scheffner M, Munger K, Bryne JC, Howley PM. The state of the p53 and retinoblastoma genes in human cervical carcinoma cell lines. Proc. Natl Acad. Sci. USA88, 5523–5527 (1991).
   PubMed Web of Science ®Google Scholar
• Werness BA, Levine AJ, Howley PM. Association of HPV type 16 and 18 E6 protein with p53. Science248, 76–79 (1990).
   PubMed Web of Science ®Google Scholar
• Rose P, Bundy BN, Watkins EB et al. Concurrent cisplatin-based radiotherapy and chemotherapy for locally advanced cervical cancer. N. Engl. J. Med.340, 1144–1153 (1999).
   PubMed Web of Science ®Google Scholar
• Green JA, Kirwan JM, Tierney JF et al. Survival and recurrence after concomitant chemotherapy and radiotherapy for cancer of the uterine cervix: a systematic review and meta-analysis. Lancet358, 781–786 (2001).
   PubMed Web of Science ®Google Scholar
• Nakagawa M, Stites DP, Farhat S et al. Cytotoxic T lymphocyte responses to E6 and E7 proteins of human papillomavirus type 16: relationship to cervical intraepithelial neoplasia. J. Infect. Dis.175, 927–931 (1997).
   PubMed Web of Science ®Google Scholar
• Nakagawa M, Stites DP, Patel S et al. 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).
   PubMed Web of Science ®Google Scholar
• Sarkar AK, Tortolero-Luna G, Follen M, Sastry KJ. Inverse correlation of cellular immune responses specific to synthetic peptides from the E6 and E7 oncoproteins of HPV-16 with recurrence of cervical intraepithelial neoplasia in a cross-sectional study. Gynecol. Oncol.99, S251–S261 (2005).
   PubMed Web of Science ®Google Scholar
• Piersma SJ, Jordanova ES, van Poelgeest MI et al. High number of intraepithelial CD8+ tumor-infiltrating lymphocytes is associated with the absence of lymph node metastases in patients with large early-stage cervical cancer. Cancer Res.67, 354–361 (2007).
   PubMed Web of Science ®Google Scholar
• Cheng WF, Hung CF, Hsu KF et al. Cancer immunotherapy using Sindbis virus replicon particles encoding a VP22-antigen fusion. Hum. Gene Ther.13, 553–568 (2002).
   PubMed Web of Science ®Google Scholar
• Kim TY, Myoung HJ, Kim JH et al. Both E7 and CpG-ODN are required for protective immunity against challenge with human papillomavirus 16 (E6/E7)-immortalized tumor cells: involvement of CD4+ and CD8+ T cells in protection. Cancer Res.62, 7234–7240 (2002).
   PubMed Web of Science ®Google Scholar
• Ahn WS, Bae SM, Kim TY et al. A therapy modality using recombinant IL-12 adenovirus plus E7 protein in a human papillomavirus 16 E6/E7-associated cervical cancer animal model. Hum. Gene Ther.14, 1389–1399 (2003).
   PubMed Web of Science ®Google Scholar
• Zhang L, Tang Y, Akbulut H, Zelterman D, Linton PJ, Deisseroth AB. An adenoviral vector cancer vaccine that delivers a tumor-associated antigen/CD40-ligand fusion protein to dendritic cells. Proc. Natl Acad. Sci. USA100, 15101–15106 (2003).
   PubMed Web of Science ®Google Scholar
• Kim TW, Hung CF, Boyd DA et al. Enhancement of DNA vaccine potency by coadministration of a tumor antigen gene and DNA encoding serine protease inhibitor-6. Cancer Res.64, 400–405 (2004).
   PubMed Web of Science ®Google Scholar
• Kim TW, Hung CF, Kim JW et al. Vaccination with a DNA vaccine encoding herpes simplex virus type 1 VP22 linked to antigen generates long-term antigen-specific CD8-positive memory T cells and protective immunity. Hum. Gene Ther.15, 167–177 (2004).
   PubMed Web of Science ®Google Scholar
• Kim MS, Sin JI. Both antigen optimization and lysosomal targeting are required for enhanced anti-tumour protective immunity in a human papillomavirus E7-expressing animal tumour model. Immunol.116, 255–266 (2005).
   PubMed Web of Science ®Google Scholar
• Sin JI, Hong SH, Park YJ, Park JB, Choi YS, Kim, MS. Anti-tumor therapeutic effects of E7 subunit and DNA vaccines in an animal cervical cancer model: anti-tumor efficacy of E7 therapeutic vaccines is dependent on tumor sizes, vaccine doses, and vaccine delivery routes. DNA Cell Biol.25, 277–286 (2006).
   PubMed Web of Science ®Google Scholar
• Bae SH, Park YJ, Choi YS, Park JB, Kim MS, Sin JI. Therapeutic synergy of human papillomavirus E7 subunit vaccines plus cisplatin in an animal tumor model: causal involvement of increased sensitivity of cisplatin-treated tumors to CTL-mediated killing in therapeutic synergy. Clin. Cancer Res.13, 341–349 (2007).
   PubMed Web of Science ®Google Scholar
• Fernando GJP, Murray B, Zhou J, Frazer IH. Expression, purification and immunological characterization of the transforming protein E7, from cervical cancer-associated human papillomavirus type 16. Clin. Exp. Immunol.115, 397–403 (1999).
   PubMed Web of Science ®Google Scholar
• Cui Z, Huang L. Liposome-polycation-DNA (LPD) particle as a carrier and adjuvant for protein-based vaccines: therapeutic effect against cervical cancer. Cancer Immunol. Immunother.54, 1180–1190 (2005).
   PubMed Web of Science ®Google Scholar
• Zwaveling S, Ferreira Mota SC, Nouta J et al. Established human papillomavirus type 16-expressing tumors are effectively eradicated following vaccination with long peptides. J. Immunol.169, 350–358 (2002).
   PubMed Web of Science ®Google Scholar
• Cui Z, Qiu F, Synthetic double-stranded RNA poly(I:C) as a potent peptide vaccine adjuvant: therapeutic activity against human cervical cancer in a rodent model. Cancer Immunol. Immunother.54, 1180–1190 (2005).
   PubMed Web of Science ®Google Scholar
• Livingston BD, Crimi C, Grey H et al. The hepatitis B virus-specific CTL responses induced in humans by lipopeptide vaccination are comparable to those elicited by acute viral infection. J. Immunol.159, 1383–1392 (1997).
   PubMed Web of Science ®Google Scholar
• Gahery-Segard H, Pialoux G, Charmeteau B et al. Multiepitopic B- and T-cell responses induced in humans by a human immunodeficiency virus type 1 lipopeptide vaccine. J. Virol.74, 1694–1703 (2000).
   PubMed Web of Science ®Google Scholar
• Mortara L, Gras-Masse H, Rommens C, Venet A, Guillet JG, Bourgault-Villada I. Type 1 CD4+ T-cell help is required for induction of antipeptide multispecific cytotoxic T lymphocytes by a lipopeptidic vaccine in rhesus macaques. J. Virol.73, 4447–4451 (1999).
   PubMed Web of Science ®Google Scholar
• Preville X, Ladant D, Timmerman B, Leclerc C. Eradication of established tumors by vaccination with recombinant Bordetella pertussis adenylate cyclase carrying the human papillomavirus 16 E7 oncoprotein. Cancer Res.65, 641–649 (2005).
   PubMed Web of Science ®Google Scholar
• Ji H, Wang TL, Chen CH et al. Targeting human papillomavirus type 16 E7 to the endosomal/lysosomal compartment enhances the anti-tumor immunity of DNA vaccines against murine human papillomavirus type 16 E7-expressing tumors. Hum. Gene Ther.10, 2727–2740 (1999).
   PubMed Web of Science ®Google Scholar
• Hung CF, Cheng WF, Hsu KF et al. Cancer immunotherapy using a DNA vaccine encoding the translocation domain of a bacterial toxin linked to a tumor antigen. Cancer Res.61, 3698–3703 (2001).
   PubMed Web of Science ®Google Scholar
• Cheng WF, Hung CF, Chai CY et al. Tumor-specific immunity and anti-angiogenesis generated by a DNA vaccine encoding calreticulin linked to a tumor antigen. J. Clin. Invest.108, 669–678 (2001).
   PubMed Web of Science ®Google Scholar
• Hung CF, He L, Juang J, Lin TJ, Ling M, Wu TC. Improving DNA vaccine potency by linking Marek’s disease virus type 1 VP22 to an antigen. J. Virol.76, 2676–2682 (2002).
   PubMed Web of Science ®Google Scholar
• Hung CF, Cheng WF, He L et al. Enhancing major histocompatibility complex class I antigen presentation by targeting antigen to centrosomes. Cancer Res.63, 2393–2398 (2003).
   PubMed Web of Science ®Google Scholar
• Kim TW, Hung CF, Ling M et al. Enhancing DNA vaccine potency by coadministration of DNA encoding anti-apoptotic proteins. J. Clin. Invest.112, 109–117 (2003).
   PubMed Web of Science ®Google Scholar
• Tang Y, Zhang L, Yuan J et al. Multistep process through which adenoviral vector vaccine overcomes anergy to tumor-associated antigens. Blood104, 2704–2713 (2004).
   Google Scholar
• Kim TG, Kim CH, Won EH et al. CpG-ODN-stimulated dendritic cells act as a potent adjuvant for E7 protein delivery to induce antigen-specific anti-tumor immunity in a HPV 16 (E6/E7)-associated tumor animal model. Immunology112, 117–125 (2004).
   PubMed Web of Science ®Google Scholar
• Bermudez-Humaran LG, Cortes-Perez NG, Lefevre F et al. A novel mucosal vaccine based on live Lactococci expressing E7 antigen and IL-12 induces systemic and mucosal immune responses and protects mice against human papillomavirus type 16-induced tumors. J. Immunol.175, 7297–7302 (2005).
   PubMed Web of Science ®Google Scholar
• Roychowdhury S, May KF Jr, Tzou KS et al. Failed adoptive immunotherapy with tumor-specific T cells: reversal with low-dose interleukin 15 but not low-dose interleukin 2. Cancer Res.64, 8062–8067 (2004).
   PubMed Web of Science ®Google Scholar
• Klebanoff CA, Finkelstein SE, Surman DR et al. IL-15 enhances the in vivo antitumor activity of tumor-reactive CD8+ T cells. Proc. Natl Acad. Sci. USA101, 1969–1974 (2004).
   PubMed Web of Science ®Google Scholar
• Comes A, Rosso O, Orengo AM et al. CD25+ Regulatory T cell depletion augments immunotherapy of micrometastases by an IL-21-secreting cellular vaccine. J. Immunol.176, 1750–1758 (2006).
   PubMed Web of Science ®Google Scholar
• Viehl CT, Moore TT, Liyanage UK et al. Depletion of CD4+CD25+ regulatory T cells promotes a tumor-specific immune response in pancreas cancer-bearing mice. Ann. Surg. Oncol.13, 1252–1258 (2006).
   PubMed Web of Science ®Google Scholar
• Prasad SJ, Farrand KJ, Matthews SA, Chang JH, McHugh RS, Ronchese F. Dendritic cells loaded with stressed tumor cells elicit long-lasting protective tumor immunity in mice depleted of CD4+CD25+ regulatory T cells. J. Immunol.174, 90–98 (2005).
   PubMed Web of Science ®Google Scholar
• van Elsas A, Hurwitz AA, Allison JP. Combination immunotherapy of B16 melanoma using anti-cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) and granulocyte/macrophage colony-stimulating factor (GM-CSF)-producing vaccines induces rejection of subcutaneous and metastatic tumors accompanied by autoimmune depigmentation. J. Exp. Med.190, 355–366 (1999).
   PubMed Web of Science ®Google Scholar
• Quezada SA, Peggs KS, Curran MA, Allison JP. CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J. Clin. Invest.116, 1935–1945 (2006).
   PubMed Web of Science ®Google Scholar
• Muderspach L, Wilczynski S, Roman L et al. A Phase I trial of a human papillomavirus (HPV) peptide vaccine for women with high-grade cervical and vulvar intraepithelial neoplasia who are HPV 16 positive. Clin. Cancer Res.6, 3406–3416 (2000).
   PubMed Web of Science ®Google Scholar
• Garcia-Hernandez E, Gonzalez-Sanchez JL, Andrade-Manzano A et al. Regression of papilloma high-grade lesions (CIN 2 and CIN 3) is stimulated by therapeutic vaccination with MVA E2 recombinant vaccine. Cancer Gene Ther.13, 592–597 (2006).
   PubMed Web of Science ®Google Scholar
• Roman L, Wilczynski S, Muderspach LI et al. A Phase II study of hsp-7 (SGN-00101) in women with high-grade cervical intraepithelial neoplasia. Gynecol. Oncol.106, 558–566 (2007).
   PubMed Web of Science ®Google Scholar
• Kaufmann, A., Nieland, JD, Jochmus I et al. Vaccination trial with HPV16 L1E7 chimeric virus-like particles in women suffering from high grade cervical intraepithelial neoplasia (CIN 2/3). Int. J. Cancer121, 2794–2800 (2007).
   PubMed Web of Science ®Google Scholar
• van Driel WJ, Ressing ME, Kenter GG et al. Vaccination with HPV 16 peptides of patients with advanced cervical carcinoma: clinical evaluation of a Phase I–II trial. Eur. J. Cancer35, 946–952 (1999).
   PubMed Web of Science ®Google Scholar
• Ferrara A, Nonn M, Sehr P et al. Dendritic cell-based tumor vaccine for cervical cancer II: results of a clinical pilot study in 15 individual patients. J. Cancer Res. Clin. Oncol.129, 521–530 (2003).
   PubMed Web of Science ®Google Scholar
• Santin AD, Bellone S, Palmieri M et al. HPV 16/18 E7-pulsed dendritic cell vaccination in cervical cancer patients with recurrent disease refractory to standard treatment modalities. Gynecol. Oncol.100, 469–478 (2006).
   PubMed Web of Science ®Google Scholar
• Borysiewicz LK, Fiander A, Nimako M et al. A recombinant vaccinia virus encoding human papillomavirus types 16 and 18, E6 and E7 proteins as immunotherapy for cervical cancer. Lancet347, 1523–1527 (1996).
   PubMed Web of Science ®Google Scholar
• Kaufmann AM, Stern PL, Rankin EM et al. Safety and immunogenicity of TA-HPV, a recombinant vaccinia virus expressing modified human papillomavirus (HPV)-16 and HPV-18 E6 and E7 genes, in women with progressive cervical cancer. Clin. Cancer Res.8, 3676–3685 (2002).
   PubMed Web of Science ®Google Scholar
• Ye GW, Park JB, Park YJ, Choi YS, Sin JI. Increased sensitivity of radiated murine cervical cancer tumors to E7 subunit vaccine-driven CTL-mediated killing induces synergistic anti-tumor activity. Mol. Ther.15, 1564–1570 (2007).
   PubMed Web of Science ®Google Scholar
• Tseng C, Monie A, Wu CY et al. Treatment with proteasome inhibitor bortezomib enhances antigen-specific CD8+ T-cell-mediated anti-tumor immunity induced by DNA vaccination. J. Mol. Med.86, 899–908 (2008).
   PubMed Web of Science ®Google Scholar