The current state of therapeutic and T cell-based vaccines against human papillomaviruses

Virus Research

Volumn 231, Issue , 2017, Pages 148-165

  Yang, Andrew ^a   Farmer, Emily ^a   Lin, John ^a   Wu, T C ^a,b   Hung, Chien Fu ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

HPV E6; HPV E7; Human papillomavirus; Immunotherapy; T cell based vaccine; Therapeutic vaccine

Indexed keywords

BACTERIAL VECTOR; CHIMERIC ANTIGEN RECEPTOR; DENDRITIC CELL VACCINE; DNA VACCINE; LIVE VACCINE; PEPTIDE VACCINE; RNA VACCINE; T LYMPHOCYTE RECEPTOR; TUMOR VACCINE; VIRUS VECTOR; WART VIRUS VACCINE; CANCER VACCINE; SUBUNIT VACCINE;

CELL ENGINEERING; DRUG DESIGN; DRUG EFFICACY; HUMAN; IMMUNIZATION; NONHUMAN; PAPILLOMAVIRUS INFECTION; PHASE 1 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; WART VIRUS; ADOPTIVE TRANSFER; BIOSYNTHESIS; CELLULAR IMMUNITY; CLINICAL TRIAL (TOPIC); DENDRITIC CELL; DRUG EFFECTS; FEMALE; GROWTH, DEVELOPMENT AND AGING; HEAD AND NECK TUMOR; IMMUNOLOGY; PAPILLOMAVIRIDAE; PATHOGENICITY; PATHOLOGY; TRANSPLANTATION; UTERINE CERVIX TUMOR; VACCINATION; VIROLOGY;

ADOPTIVE TRANSFER; CANCER VACCINES; CLINICAL TRIALS AS TOPIC; DENDRITIC CELLS; FEMALE; HEAD AND NECK NEOPLASMS; HUMANS; IMMUNITY, CELLULAR; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PAPILLOMAVIRUS VACCINES; T-LYMPHOCYTES; UTERINE CERVICAL NEOPLASMS; VACCINATION; VACCINES, DNA; VACCINES, SUBUNIT;

EID: 85008195199     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2016.12.002     Document Type: Review

References (97)

1. Adachi, K., Kawana, K., Yokoyama, T., Fujii, T., Tomio, A., Miura, S., Tomio, K., Kojima, S., Oda, K., Sewaki, T., Yasugi, T., Kozuma, S., Taketani, Y., Oral immunization with a Lactobacillus casei vaccine expressing human papillomavirus (HPV) type 16 E7 is an effective strategy to induce mucosal cytotoxic lymphocytes against HPV16 E7. Vaccine 28:16 (2010), 2810–2817.
2. Adams, M., Navabi, H., Jasani, B., Man, S., Fiander, A., Evans, A.S., Donninger, C., Mason, M., Dendritic cell (DC) based therapy for cervical cancer: use of DC pulsed with tumour lysate and matured with a novel synthetic clinically non-toxic double stranded RNA analogue poly [I]:poly [C(12)U] (Ampligen R). Vaccine 21:7–8 (2003), 787–790.
3. Alvarez, R.D., Huh, W.K., Bae, S., Lamb, L.S. Jr., Conner, M.G., Boyer, J., Wang, C., Hung, C.F., Sauter, E., Paradis, M., Adams, E.A., Hester, S., Jackson, B.E., Wu, T.C., Trimble, C.L., A pilot study of pNGVL4a-CRT/E7(detox) for the treatment of patients with HPV16+ cervical intraepithelial neoplasia 2/3 (CIN2/3). Gynecol. Oncol. 140:2 (2016), 245–252.
4. Baez-Astua, A., Herraez-Hernandez, E., Garbi, N., Pasolli, H.A., Juarez, V., Zur Hausen, H., Cid-Arregui, A., Low-dose adenovirus vaccine encoding chimeric hepatitis B virus surface antigen-human papillomavirus type 16 E7 proteins induces enhanced E7-specific antibody and cytotoxic T-cell responses. J. Virol. 79:20 (2005), 12807–12817.
5. Bagarazzi, M.L., Yan, J., Morrow, M.P., Shen, X., Parker, R.L., Lee, J.C., Giffear, M., Pankhong, P., Khan, A.S., Broderick, K.E., Knott, C., Lin, F., Boyer, J.D., Draghia-Akli, R., White, C.J., Kim, J.J., Weiner, D.B., Sardesai, N.Y., Immunotherapy against HPV16/18 generates potent TH1 and cytotoxic cellular immune responses. Sci. Transl. Med., 4(155), 2012, 155ra138.
6. Baldwin, P.J., van der Burg, S.H., Boswell, C.M., Offringa, R., Hickling, J.K., Dobson, J., Roberts, J.S., Latimer, J.A., Moseley, R.P., Coleman, N., Stanley, M.A., Sterling, J.C., Vaccinia-expressed human papillomavirus 16 and 18 e6 and e7 as a therapeutic vaccination for vulval and vaginal intraepithelial neoplasia. Clin. Cancer Res. 9:14 (2003), 5205–5213.
7. Benencia, F., Courreges, M.C., Coukos, G., Whole tumor antigen vaccination using dendritic cells: comparison of RNA electroporation and pulsing with UV-irradiated tumor cells. J. Transl. Med., 6, 2008, 21.
8. Berglund, P., Quesada-Rolander, M., Putkonen, P., Biberfeld, G., Thorstensson, R., Liljestrom, P., Outcome of immunization of cynomolgus monkeys with recombinant Semliki Forest virus encoding human immunodeficiency virus type 1 envelope protein and challenge with a high dose of SHIV-4 virus. AIDS Res. Hum. Retroviruses 13:17 (1997), 1487–1495.
9. Bermudez-Humaran, L.G., Cortes-Perez, N.G., Le Loir, Y., Alcocer-Gonzalez, J.M., Tamez-Guerra, R.S., de Oca-Luna, R.M., Langella, P., An inducible surface presentation system improves cellular immunity against human papillomavirus type 16 E7 antigen in mice after nasal administration with recombinant lactococci. J. Med. Microbiol. 53:Pt 5 (2004), 427–433.
10. Borysiewicz, L.K., Fiander, A., Nimako, M., Man, S., Wilkinson, G.W., Westmoreland, D., Evans, A.S., Adams, M., Stacey, S.N., Boursnell, M.E., Rutherford, E., Hickling, J.K., Inglis, S.C., A recombinant vaccinia virus encoding human papillomavirus types 16 and 18, E6 and E7 proteins as immunotherapy for cervical cancer. Lancet 347:9014 (1996), 1523–1527.
11. Brun, J.L., Dalstein, V., Leveque, J., Mathevet, P., Raulic, P., Baldauf, J.J., Scholl, S., Huynh, B., Douvier, S., Riethmuller, D., Clavel, C., Birembaut, P., Calenda, V., Baudin, M., Bory, J.P., Regression of high-grade cervical intraepithelial neoplasia with TG4001 targeted immunotherapy. Am. J. Obstet. Gynecol. 204:2 (2011), e161–168.
12. Cassetti, M.C., McElhiney, S.P., Shahabi, V., Pullen, J.K., Le Poole, I.C., Eiben, G.L., Smith, L.R., Kast, W.M., Antitumor efficacy of Venezuelan equine encephalitis virus replicon particles encoding mutated HPV16 E6 and E7 genes. Vaccine 22:3–4 (2004), 520–527.
13. Chang, E.Y., Chen, C.H., Ji, H., Wang, T.L., Hung, K., Lee, B.P., Huang, A.Y., Kurman, R.J., Pardoll, D.M., Wu, T., Antigen-specific cancer immunotherapy using a GM-CSF secreting allogeneic tumor cell-based vaccine. International journal of cancer. J. Int. Cancer 86:5 (2000), 725–730.
14. Chattergoon, M.A., Robinson, T.M., Boyer, J.D., Weiner, D.B., Specific immune induction following DNA-based immunization through in vivo transfection and activation of macrophages/antigen-presenting cells. J. Immunol. 160:12 (1998), 5707–5718.
15. Chen, Z., Ozbun, L., Chong, N., Wallecha, A., Berzofsky, J.A., Khleif, S.N., Episomal expression of truncated listeriolysin O in LmddA-LLO-E7 vaccine enhances antitumor efficacy by preferentially inducing expansions of CD4 + FoxP3- and CD8+ T cells. Cancer Immunol. Res. 2:9 (2014), 911–922.
16. Cheng, W.F., Hung, C.F., Hsu, K.F., Chai, C.Y., He, L., Polo, J.M., Slater, L.A., Ling, M., Wu, T.C., Cancer immunotherapy using Sindbis virus replicon particles encoding a VP22-antigen fusion. Hum. Gene Ther. 13:4 (2002), 553–568.
17. Coleman, H.N., Greenfield, W.W., Stratton, S.L., Vaughn, R., Kieber, A., Moerman-Herzog, A.M., Spencer, H.J., Hitt, W.C., Quick, C.M., Hutchins, L.F., Mackintosh, S.G., Edmondson, R.D., Erickson, S.W., Nakagawa, M., Human papillomavirus type 16 viral load is decreased following a therapeutic vaccination. Cancer Immunol. Immunother.: CII 65:5 (2016), 563–573.
18. Cortes-Perez, N.G., Azevedo, V., Alcocer-Gonzalez, J.M., Rodriguez-Padilla, C., Tamez-Guerra, R.S., Corthier, G., Gruss, A., Langella, P., Bermudez-Humaran, L.G., Cell-surface display of E7 antigen from human papillomavirus type-16 in Lactococcus lactis and in Lactobacillus plantarum using a new cell-wall anchor from lactobacilli. J. Drug Targeting 13:2 (2005), 89–98.
19. Daayana, S., Elkord, E., Winters, U., Pawlita, M., Roden, R., Stern, P.L., Kitchener, H.C., Phase II trial of imiquimod and HPV therapeutic vaccination in patients with vulval intraepithelial neoplasia. Br. J. Cancer 102:7 (2010), 1129–1136.
20. Dai, H., Wang, Y., Lu, X., Han, W., Chimeric antigen receptors modified T-Cells for cancer therapy. J. Natl. Cancer Inst., 108(7), 2016.
21. Davidson, E.J., Faulkner, R.L., Sehr, P., Pawlita, M., Smyth, L.J., Burt, D.J., Tomlinson, A.E., Hickling, J., Kitchener, H.C., Stern, P.L., Effect of TA-CIN (HPV 16 L2E6E7) booster immunisation in vulval intraepithelial neoplasia patients previously vaccinated with TA-HPV (vaccinia virus encoding HPV 16/18 E6E7). Vaccine 22:21–22 (2004), 2722–2729.
22. Doorbar, J., Model systems of human papillomavirus-associated disease. J. Pathol. 238:2 (2016), 166–179.
23. Draper, L.M., Kwong, M.L., Gros, A., Stevanovic, S., Tran, E., Kerkar, S., Raffeld, M., Rosenberg, S.A., Hinrichs, C.S., Targeting of HPV-16+ epithelial cancer cells by TCR gene engineered t cells directed against E6. Clin. Cancer Res. 21:19 (2015), 4431–4439.
24. Dupuis, M., Denis-Mize, K., Woo, C., Goldbeck, C., Selby, M.J., Chen, M., Otten, G.R., Ulmer, J.B., Donnelly, J.J., Ott, G., McDonald, D.M., Distribution of DNA vaccines determines their immunogenicity after intramuscular injection in mice. J. Immunol. 165:5 (2000), 2850–2858.
25. Egawa, N., Egawa, K., Griffin, H., Doorbar, J., Human papillomaviruses; epithelial tropisms, and the development of neoplasia. Viruses 7:7 (2015), 3863–3890.
26. Feltkamp, M.C., Smits, H.L., Vierboom, M.P., Minnaar, R.P., de Jongh, B.M., Drijfhout, J.W., ter Schegget, J., Melief, C.J., Kast, W.M., Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur. J. Immunol. 23:9 (1993), 2242–2249.
27. Forman, D., de Martel, C., Lacey, C.J., Soerjomataram, I., Lortet-Tieulent, J., Bruni, L., Vignat, J., Ferlay, J., Bray, F., Plummer, M., Franceschi, S., Global burden of human papillomavirus and related diseases. Vaccine 30:Suppl. 5 (2012), F12–23.
28. Fu, T.M., Ulmer, J.B., Caulfield, M.J., Deck, R.R., Friedman, A., Wang, S., Liu, X., Donnelly, J.J., Liu, M.A., Priming of cytotoxic T lymphocytes by DNA vaccines: requirement for professional antigen presenting cells and evidence for antigen transfer from myocytes. Mol. Med. 3:6 (1997), 362–371.
29. Ghittoni, R., Accardi, R., Chiocca, S., Tommasino, M., Role of human papillomaviruses in carcinogenesis. Ecancermedicalscience, 9, 2015, 526.
30. Ginaldi, L., Loreto, M.F., Corsi, M.P., Modesti, M., De Martinis, M., Immunosenescence and infectious diseases. Microbes Infect. 3:10 (2001), 851–857.
31. Gomez-Gutierrez, J.G., Elpek, K.G., Montes de Oca-Luna, R., Shirwan, H., Sam Zhou, H., McMasters, K.M., Vaccination with an adenoviral vector expressing calreticulin-human papillomavirus 16 E7 fusion protein eradicates E7 expressing established tumors in mice. Cancer Immunol. Immunother.: CII 56:7 (2007), 997–1007.
32. Gunn, G.R., Zubair, A., Peters, C., Pan, Z.K., Wu, T.C., Paterson, Y., Two Listeria monocytogenes vaccine vectors that express different molecular forms of human papilloma virus-16 (HPV-16) E7 induce qualitatively different T cell immunity that correlates with their ability to induce regression of established tumors immortalized by HPV-16. J. Immunol. 167:11 (2001), 6471–6479.
33. Haji-Fatahaliha, M., Hosseini, M., Akbarian, A., Sadreddini, S., Jadidi-Niaragh, F., Yousefi, M., CAR-modified T-cell therapy for cancer: an updated review. Artif. Cells Nanomed. Biotechnol. 44:6 (2016), 1339–1349.
34. Harper, D.M., Williams, K.B., Prophylactic HPV vaccines: current knowledge of impact on gynecologic premalignancies. Discov. Med. 10:50 (2010), 7–17.
35. Harper, D.M., Currently approved prophylactic HPV vaccines. Expert Rev. Vaccines 8:12 (2009), 1663–1679.
36. Hossain, N.M., Chapuis, A.G., Walter, R.B., T-Cell receptor-engineered cells for the treatment of hematologic malignancies. Curr. Hematol. Malig. Rep. 11:4 (2016), 311–317.
37. Hsieh, C.J., Kim, T.W., Hung, C.F., Juang, J., Moniz, M., Boyd, D.A., He, L., Chen, P.J., Chen, C.H., Wu, T.C., Enhancement of vaccinia vaccine potency by linkage of tumor antigen gene to gene encoding calreticulin. Vaccine 22:29–30 (2004), 3993–4001.
38. Hsu, K.F., Hung, C.F., Cheng, W.F., He, L., Slater, L.A., Ling, M., Wu, T.C., Enhancement of suicidal DNA vaccine potency by linking Mycobacterium tuberculosis heat shock protein 70 to an antigen. Gene Ther. 8:5 (2001), 376–383.
39. Hung, C.F., Ma, B., Monie, A., Tsen, S.W., Wu, T.C., Therapeutic human papillomavirus vaccines: current clinical trials and future directions. Expert Opin. Biol. Ther. 8:4 (2008), 421–439.
40. Ip, P.P., Boerma, A., Walczak, M., Oosterhuis, K., Haanen, J.B., Schumacher, T.N., Nijman, H.W., Daemen, T., Antigen design enhances the immunogenicity of Semliki Forest virus-based therapeutic human papillomavirus vaccines. Gene Ther. 22:7 (2015), 560–567.
41. Jeanbart, L., Swartz, M.A., Engineering opportunities in cancer immunotherapy. Proc. Natl. Acad. Sci. U. S. A. 112:47 (2015), 14467–14472.
42. Kash, N., Lee, M.A., Kollipara, R., Downing, C., Guidry, J., Tyring, S.K., Safety and efficacy data on vaccines and immunization to human papillomavirus. J. Clin. Med. 4:4 (2015), 614–633.
43. Kaufmann, A.M., Stern, P.L., Rankin, E.M., Sommer, H., Nuessler, V., Schneider, A., Adams, M., Onon, T.S., Bauknecht, T., Wagner, U., Kroon, K., Hickling, J., Boswell, C.M., Stacey, S.N., Kitchener, H.C., Gillard, J., Wanders, J., Roberts, J.S., Zwierzina, H., 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. 8:12 (2002), 3676–3685.
44. Kawana, K., Adachi, K., Kojima, S., Taguchi, A., Tomio, K., Yamashita, A., Nishida, H., Nagasaka, K., Arimoto, T., Yokoyama, T., Wada-Hiraike, O., Oda, K., Sewaki, T., Osuga, Y., Fujii, T., Oral vaccination against HPV E7 for treatment of cervical intraepithelial neoplasia grade 3 (CIN3) elicits E7-specific mucosal immunity in the cervix of CIN3 patients. Vaccine 32:47 (2014), 6233–6239.
45. Kelderman, S., Heemskerk, B., Fanchi, L., Philips, D., Toebes, M., Kvistborg, P., van Buuren, M.M., van Rooij, N., Michels, S., Germeroth, L., Haanen, J.B., Schumacher, N.M., Antigen-specific TIL therapy for melanoma: a flexible platform for personalized cancer immunotherapy. Eur. J. Immunol. 46:6 (2016), 1351–1360.
46. Kenter, G.G., Welters, M.J., Valentijn, A.R., Lowik, M.J., Berends-van der Meer, D.M., Vloon, A.P., Essahsah, F., Fathers, L.M., Offringa, R., Drijfhout, J.W., Wafelman, A.R., Oostendorp, J., Fleuren, G.J., van der Burg, S.H., Melief, C.J., Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N. Engl. J. Med. 361:19 (2009), 1838–1847.
47. Kim, J.W., Hung, C.F., Juang, J., He, L., Kim, T.W., Armstrong, D.K., Pai, S.I., Chen, P.J., Lin, C.T., Boyd, D.A., Wu, T.C., Comparison of HPV DNA vaccines employing intracellular targeting strategies. Gene Ther. 11:12 (2004), 1011–1018.
48. Kim, J.H., Kang, T.H., Noh, K.H., Bae, H.C., Kim, S.H., Yoo, Y.D., Seong, S.Y., Kim, T.W., Enhancement of dendritic cell-based vaccine potency by anti-apoptotic siRNAs targeting key pro-apoptotic proteins in cytotoxic CD8(+) T cell-mediated cell death. Immunol. Lett. 122:1 (2009), 58–67.
49. Kim, T.J., Jin, H.T., Hur, S.Y., Yang, H.G., Seo, Y.B., Hong, S.R., Lee, C.W., Kim, S., Woo, J.W., Park, K.S., Hwang, Y.Y., Park, J., Lee, I.H., Lim, K.T., Lee, K.H., Jeong, M.S., Surh, C.D., Suh, Y.S., Park, J.S., Sung, Y.C., Clearance of persistent HPV infection and cervical lesion by therapeutic DNA vaccine in CIN3 patients. Nat. Commun., 5, 2014, 5317.
50. Klaes, R., Woerner, S.M., Ridder, R., Wentzensen, N., Duerst, M., Schneider, A., Lotz, B., Melsheimer, P., von Knebel Doeberitz, M., Detection of high-risk cervical intraepithelial neoplasia and cervical cancer by amplification of transcripts derived from integrated papillomavirus oncogenes. Cancer Res. 59:24 (1999), 6132–6136.
51. Klebanoff, C.A., Rosenberg, S.A., Restifo, N.P., Prospects for gene-engineered T cell immunotherapy for solid cancers. Nat. Med. 22:1 (2016), 26–36.
52. Kumar, A., Hussain, S., Yadav, I.S., Gissmann, L., Natarajan, K., Das, B.C., Bharadwaj, M., Identification of human papillomavirus-16 E6 variation in cervical cancer and their impact on T and B cell epitopes. J. Virol. Methods 218 (2015), 51–58.
53. Lamikanra, A., Pan, Z.K., Isaacs, S.N., Wu, T.C., Paterson, Y., Regression of established human papillomavirus type 16 (HPV-16) immortalized tumors in vivo by vaccinia viruses expressing different forms of HPV-16 E7 correlates with enhanced CD8(+) T-cell responses that home to the tumor site. J. Virol. 75:20 (2001), 9654–9664.
54. Lee, S.J., Yang, A., Wu, T.C., Hung, C.F., Immunotherapy for human papillomavirus-associated disease and cervical cancer: review of clinical and translational research. J. Gynecol. Oncol., 27(5), 2016, e51.
55. Lin, K., Doolan, K., Hung, C.F., Wu, T.C., Perspectives for preventive and therapeutic HPV vaccines. J. Formos. Med. Assoc. 109:1 (2010), 4–24.
56. Liu, D.W., Tsao, Y.P., Kung, J.T., Ding, Y.A., Sytwu, H.K., Xiao, X., Chen, S.L., Recombinant adeno-associated virus expressing human papillomavirus type 16 E7 peptide DNA fused with heat shock protein DNA as a potential vaccine for cervical cancer. J. Virol. 74:6 (2000), 2888–2894.
57. Ma, B., Maraj, B., Tran, N.P., Knoff, J., Chen, A., Alvarez, R.D., Hung, C.F., Wu, T.C., Emerging human papillomavirus vaccines. Expert Opin. Emerg. Drugs 17:4 (2012), 469–492.
58. Maciag, P.C., Radulovic, S., Rothman, J., The first clinical use of a live-attenuated Listeria monocytogenes vaccine: a Phase I safety study of Lm-LLO-E7 in patients with advanced carcinoma of the cervix. Vaccine 27:30 (2009), 3975–3983.
59. Mackova, J., Kutinova, L., Hainz, P., Krystofova, J., Sroller, V., Otahal, P., Gabriel, P., Nemeckova, S., Adjuvant effect of dendritic cells transduced with recombinant vaccinia virus expressing HPV16-E7 is inhibited by co-expression of IL12. Int. J. Oncol. 24:6 (2004), 1581–1588.
60. Maxwell, J.H., Grandis, J.R., Ferris, R.L., HPV-associated head and neck cancer: unique features of epidemiology and clinical management. Annu. Rev. Med., 2015.
61. Mehanna, H., Beech, T., Nicholson, T., El-Hariry, I., McConkey, C., Paleri, V., Roberts, S., Prevalence of human papillomavirus in oropharyngeal and nonoropharyngeal head and neck cancer?systematic review and meta-analysis of trends by time and region. Head Neck 35:5 (2013), 747–755.
62. Mikyskova, R., Indrova, M., Simova, J., Jandlova, T., Bieblova, J., Jinoch, P., Bubenik, J., Vonka, V., Treatment of minimal residual disease after surgery or chemotherapy in mice carrying HPV16-associated tumours: cytokine and gene therapy with IL-2 and GM-CSF. Int. J. Oncol. 24:1 (2004), 161–167.
63. Murakami, M., Gurski, K.J., Marincola, F.M., Ackland, J., Steller, M.A., Induction of specific CD8+ T-lymphocyte responses using a human papillomavirus-16 E6/E7 fusion protein and autologous dendritic cells. Cancer Res. 59:6 (1999), 1184–1187.
64. Ostor, A.G., Natural history of cervical intraepithelial neoplasia: a critical review. Int. J. Gynecol. Pathol. 12:2 (1993), 186–192.
65. Peng, S., Kim, T.W., Lee, J.H., Yang, M., He, L., Hung, C.F., Wu, T.C., Vaccination with dendritic cells transfected with BAK and BAX siRNA enhances antigen-specific immune responses by prolonging dendritic cell life. Hum. Gene Ther. 16:5 (2005), 584–593.
66. Peters, C., Paterson, Y., Enhancing the immunogenicity of bioengineered Listeria monocytogenes by passaging through live animal hosts. Vaccine 21:11–12 (2003), 1187–1194.
67. Porgador, A., Irvine, K.R., Iwasaki, A., Barber, B.H., Restifo, N.P., Germain, R.N., Predominant role for directly transfected dendritic cells in antigen presentation to CD8+ T cells after gene gun immunization. J. Exp. Med. 188:6 (1998), 1075–1082.
68. Ramanathan, P., Ganeshrajah, S., Raghanvan, R.K., Singh, S.S., Thangarajan, R., Development and clinical evaluation of dendritic cell vaccines for HPV related cervical cancer–a feasibility study. Asian Pacific J. Cancer Prev.: APJCP 15:14 (2014), 5909–5916.
69. Riemer, A.B., Keskin, D.B., Zhang, G., Handley, M., Anderson, K.S., Brusic, V., Reinhold, B., Reinherz, E.L., A conserved E7-derived cytotoxic T lymphocyte epitope expressed on human papillomavirus 16-transformed HLA-A2+ epithelial cancers. J. Biol. Chem. 285:38 (2010), 29608–29622.
70. Rosales, C., Graham, V.V., Rosas, G.A., Merchant, H., Rosales, R., A recombinant vaccinia virus containing the papilloma E2 protein promotes tumor regression by stimulating macrophage antibody-dependent cytotoxicity. Cancer Immunol. Immunother.: CII 49:7 (2000), 347–360.
71. Rosales, R., Lopez-Contreras, M., Rosales, C., Magallanes-Molina, J.R., Gonzalez-Vergara, R., Arroyo-Cazarez, J.M., Ricardez-Arenas, A., Del Follo-Valencia, A., Padilla-Arriaga, S., Guerrero, M.V., Pirez, M.A., Arellano-Fiore, C., Villarreal, F., Regression of human papillomavirus intraepithelial lesions is induced by MVA E2 therapeutic vaccine. Hum. Gene Ther. 25:12 (2014), 1035–1049.
72. Santin, A.D., Bellone, S., Roman, J.J., Burnett, A., Cannon, M.J., Pecorelli, S., Therapeutic vaccines for cervical cancer: dendritic cell-based immunotherapy. Curr. Pharm. Des. 11:27 (2005), 3485–3500.
73. Santin, A.D., Bellone, S., Palmieri, M., Zanolini, A., Ravaggi, A., Siegel, E.R., Roman, J.J., Pecorelli, S., Cannon, M.J., Human papillomavirus type 16 and 18 E7-pulsed dendritic cell vaccination of stage IB or IIA cervical cancer patients: a phase I escalating-dose trial. J. Virol. 82:4 (2008), 1968–1979.
74. Schnupf, P., Portnoy, D.A., Listeriolysin O: a phagosome-specific lysin. Microbes Infect. 9:10 (2007), 1176–1187.
75. Schober, K., Busch, D.H., TIL 2.0: More effective and predictive T-cell products by enrichment for defined antigen specificities. Eur. J. Immunol. 46:6 (2016), 1335–1339.
76. Sewell, D.A., Pan, Z.K., Paterson, Y., Listeria-based HPV-16 E7 vaccines limit autochthonous tumor growth in a transgenic mouse model for HPV-16 transformed tumors. Vaccine 26:41 (2008), 5315–5320.
77. Smyth, L.J., Van Poelgeest, M.I., Davidson, E.J., Kwappenberg, K.M., Burt, D., Sehr, P., Pawlita, M., Man, S., Hickling, J.K., Fiander, A.N., Tristram, A., Kitchener, H.C., Offringa, R., Stern, P.L., Van Der Burg, S.H., Immunological responses in women with human papillomavirus type 16 (HPV-16)-associated anogenital intraepithelial neoplasia induced by heterologous prime-boost HPV-16 oncogene vaccination. Clin. Cancer Res. 10:9 (2004), 2954–2961.
78. Stevanovic, S., Draper, L.M., Langhan, M.M., Campbell, T.E., Kwong, M.L., Wunderlich, J.R., Dudley, M.E., Yang, J.C., Sherry, R.M., Kammula, U.S., Restifo, N.P., Rosenberg, S.A., Hinrichs, C.S., Complete regression of metastatic cervical cancer after treatment with human papillomavirus-targeted tumor-infiltrating T cells. J. Clin. Oncol. 33:14 (2015), 1543–1550.
79. Su, J.H., Wu, A., Scotney, E., Ma, B., Monie, A., Hung, C.F., Wu, T.C., Immunotherapy for cervical cancer: research status and clinical potential. BioDrugs 24:2 (2010), 109–129.
80. Subramaniam, D.S., Liu, S.V., Giaccone, G., Novel approaches in cancer immunotherapy. Discov. Med. 21:116 (2016), 267–274.
81. Trimble, C.L., Morrow, M.P., Kraynyak, K.A., Shen, X., Dallas, M., Yan, J., Edwards, L., Parker, R.L., Denny, L., Giffear, M., Brown, A.S., Marcozzi-Pierce, K., Shah, D., Slager, A.M., Sylvester, A.J., Khan, A., Broderick, K.E., Juba, R.J., Herring, T.A., Boyer, J., Lee, J., Sardesai, N.Y., Weiner, D.B., Bagarazzi, M.L., Safety, efficacy, and immunogenicity of VGX-3100, a therapeutic synthetic DNA vaccine targeting human papillomavirus 16 and 18 E6 and E7 proteins for cervical intraepithelial neoplasia 2/3: a randomised, double-blind, placebo-controlled phase 2b trial. Lancet, 18, 2015.
82. Van Damme, P., Bouillette-Marussig, M., Hens, A., De Coster, I., Depuydt, C., Goubier, A., Van Tendeloo, V., Cools, N., Goossens, H., Hercend, T., Timmerman, B., Bissery, M.C., GTL001, a therapeutic vaccine for women infected with human papillomavirus 16 or 18 and normal cervical cytology: results of a phase I clinical trial. Clin. Cancer Res. 22:13 (2016), 3238–3248.
83. Wakeham, K., Kavanagh, K., The burden of HPV-associated anogenital cancers. Curr. Oncol. Rep., 16(9), 2014, 402.
84. Walboomers, J.M., Jacobs, M.V., Manos, M.M., Bosch, F.X., Kummer, J.A., Shah, K.V., Snijders, P.J., Peto, J., Meijer, C.J., Munoz, N., Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J. Pathol. 189:1 (1999), 12–19.
85. Walczak, M., Regts, J., van Oosterhout, A.J., Boon, L., Wilschut, J., Nijman, H.W., Daemen, T., Role of regulatory T-cells in immunization strategies involving a recombinant alphavirus vector system. Antivir. Ther. 16:2 (2011), 207–218.
86. Wang, T.L., Ling, M., Shih, I.M., Pham, T., Pai, S.I., Lu, Z., Kurman, R.J., Pardoll, D.M., Wu, T.C., Intramuscular administration of E7-transfected dendritic cells generates the most potent E7-specific anti-tumor immunity. Gene Ther. 7:9 (2000), 726–733.
87. Welters, M.J., van der Sluis, T.C., van Meir, H., Loof, N.M., van Ham, V.J., van Duikeren, S., Santegoets, S.J., Arens, R., de Kam, M.L., Cohen, A.F., van Poelgeest, M.I., Kenter, G.G., Kroep, J.R., Burggraaf, J., Melief, C.J., van der Burg, S.H., Vaccination during myeloid cell depletion by cancer chemotherapy fosters robust T cell responses. Sci. Transl. Med., 8(334), 2016, 334ra352.
88. Yan, J., Harris, K., Khan, A.S., Draghia-Akli, R., Sewell, D., Weiner, D.B., Cellular immunity induced by a novel HPV18 DNA vaccine encoding an E6/E7 fusion consensus protein in mice and rhesus macaques. Vaccine 26:40 (2008), 5210–5215.
89. Yan, J., Reichenbach, D.K., Corbitt, N., Hokey, D.A., Ramanathan, M.P., McKinney, K.A., Weiner, D.B., Sewell, D., Induction of antitumor immunity in vivo following delivery of a novel HPV-16 DNA vaccine encoding an E6/E7 fusion antigen. Vaccine 27:3 (2009), 431–440.
90. Yang, A., Jeang, J., Cheng, K., Cheng, T., Yang, B., Wu, T.C., Hung, C.F., Current state in the development of candidate therapeutic HPV vaccines. Expert Rev. Vaccines 15:8 (2016), 989–1007.
91. Yao, Y., Huang, W., Yang, X., Sun, W., Liu, X., Cun, W., Ma, Y., HPV-16 E6 and E7 protein T cell epitopes prediction analysis based on distributions of HLA-A loci across populations: an in silico approach. Vaccine 31:18 (2013), 2289–2294.
92. Zhang, H., Ye, Z.L., Yuan, Z.G., Luo, Z.Q., Jin, H.J., Qian, Q.J., New strategies for the treatment of solid tumors with CAR-T cells. Int. J. Biol. Sci. 12:6 (2016), 718–729.
93. de Jong, A., O'Neill, T., Khan, A.Y., Kwappenberg, K.M., Chisholm, S.E., Whittle, N.R., Dobson, J.A., Jack, L.C., St Clair Roberts, J.A., Offringa, R., van der Burg, S.H., Hickling, J.K., Enhancement of human papillomavirus (HPV) type 16 E6 and E7-specific T-cell immunity in healthy volunteers through vaccination with TA-CIN, an HPV16 L2E7E6 fusion protein vaccine. Vaccine 20:29–30 (2002), 3456–3464.
94. de Vos van Steenwijk, P.J., Ramwadhdoebe, T.H., Lowik, M.J., van der Minne, C.E., Berends-van der Meer, D.M., Fathers, L.M., Valentijn, A.R., Oostendorp, J., Fleuren, G.J., Hellebrekers, B.W., Welters, M.J., van Poelgeest, M.I., Melief, C.J., Kenter, G.G., van der Burg, S.H., A placebo-controlled randomized HPV16 synthetic long-peptide vaccination study in women with high-grade cervical squamous intraepithelial lesions. Cancer Immunol. Immunother.: CII 9 (2012), 1485–1492.
95. van Poelgeest, M.I., Welters, M.J., van Esch, E.M., Stynenbosch, L.F., Kerpershoek, G., van Persijn van Meerten, E.L., van den Hende, M., Lowik, M.J., Berends-van der Meer, D.M., Fathers, L.M., Valentijn, A.R., Oostendorp, J., Fleuren, G.J., Melief, C.J., Kenter, G.G., van der Burg, S.H., HPV16 synthetic long peptide (HPV16-SLP) vaccination therapy of patients with advanced or recurrent HPV16-induced gynecological carcinoma, a phase II trial. J. Transl. Med., 11, 2013, 88.
96. van der Burg, S.H., Kwappenberg, K.M., O'Neill, T., Brandt, R.M., Melief, C.J., Hickling, J.K., 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 19:27 (2001), 3652–3660.
97. zur Hausen, H., Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer 2:5 (2002), 342–350.