Antitumor therapeutic and antimetastatic activity of electroporation- delivered human papillomavirus 16 E7 DNA vaccines: A possible mechanism for enhanced tumor control

DNA and Cell Biology

Volumn 30, Issue 12, 2011, Pages 975-985

  Lee, In Hee ^a   Park, Jae Bok ^a   Cheong, Minseon ^a   Choi, Youn Seok ^a   Park, Daehan ^a   Sin, Jeong Im ^b  

^a Catholic University of Daegu   (South Korea)

^b Kangwon National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

DNA VACCINE; IMMUNOGLOBULIN G; WART VIRUS VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER CONTROL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DRUG DELIVERY SYSTEM; ELECTROPORATION; FEMALE; HELPER CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNOCOMPETENT CELL; LONG TERM MEMORY; METASTASIS INHIBITION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR CELL; TUMOR MODEL; UTERINE CERVIX CANCER;

ANIMALS; CANCER VACCINES; CELL LINE, TRANSFORMED; DISEASE MODELS, ANIMAL; DRUG SCREENING ASSAYS, ANTITUMOR; ELECTROPORATION; EPITHELIAL CELLS; FEMALE; HUMAN PAPILLOMAVIRUS 16; HUMANS; IMMUNIZATION SCHEDULE; INJECTIONS, INTRAMUSCULAR; INTERFERON-GAMMA; LUNG; LUNG NEOPLASMS; MICE; MICE, INBRED C57BL; NEOPLASMS, EXPERIMENTAL; PAPILLOMAVIRUS E7 PROTEINS; PAPILLOMAVIRUS VACCINES; SUBCUTANEOUS TISSUE; UTERINE CERVICAL NEOPLASMS; VACCINES, DNA;

EID: 79956122546     PISSN: 10445498     EISSN: 15577430     Source Type: Journal    
DOI: 10.1089/dna.2011.1266     Document Type: Article

References (54)

1. Ahlén, G., Söderholm, J., Tjelle, T., Kjeken, R., Frelin, L., Hö-glund, U., Blomberg, P., Fons, M., Mathiesen, I., and Sällberg, M. (2007). In vivo electroporation enhances the immunoge-nicity of hepatitis C virus nonstructural 3/4A DNA by increased local DNA uptake, protein expression, inflammation, and infiltration of CD3+ T cells. J Immunol 179, 4741-4753.
2. Ahn, W.S., Bae, S.M., Kim, T.Y., Kim, T.G., Lee, J.M., Namkoong, S.E., Kim, C.K., and Sin, J.I. (2003). 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. (Pubitemid 37268218)
3. Aihara, H., and Miyazaki, J. (1998). Gene transfer into muscle by electroporation in vivo. Nat Biotechnol 16, 867-870. (Pubitemid 28405859)
4. Bae, S.H., Park, Y.J., Choi, Y.S., Park, J.B., Kim, M.S., and Sin, J.I. (2007). 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. (Pubitemid 46121888)
5. Barouch, D.H. (2006). Rational design of gene-based vaccines. J Pathol 208, 283-289. (Pubitemid 43126120)
6. Barouch, D.H., Santra, S., Tenner-Racz, K., Racz, P., Kuroda, M.J., Schmitz, J.E., Jackson, S.S., Lifton, M.A., Freed, D.C., Perry, H.C., Davies, M.E., Shiver, J.W., and Letvin, N.L. (2002). Potent CD4 + T-cell responses elicited by a bicistronic HIV-1 DNA vaccine expressing gp120 and GM-CSF. J Immunol 168, 562-568. (Pubitemid 34049554)
7. Bodles-Brakhop, A.M., Heller, R., and Draghia-Akli, R. (2009). Electroporation for the delivery of DNA-based vaccines and immunotherapeutics: current clinical developments. Mol Ther 17, 585-592.
8. 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., and Inglis, S.C. (1996). A recombinant vaccinia virus encoding human papil-lomavirus types 16 and 18, E6 and E7 proteins as immuno-therapy for cervical cancer. Lancet 347, 1523-1527. (Pubitemid 26162644)
9. Chakraborty, M., Abrams, S.I., Coleman, C.N., Camphausen, K., Schlom, J., and Hodge, J.W. (2004). External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res 64, 4328-4337. (Pubitemid 38802440)
10. Chattergoon, M.A., Robinson, T.M., Boyer, J.D., and Weiner, D.B. (1998). Specific immune induction following DNA-based immunization through in vivo transfection and activation of macrophages. J Immunol 160, 5707-5718. (Pubitemid 28298026)
11. Cheng, W.F., Hung, C.F., Chai, C.Y., Hsu, K.F., He, L., Ling, M., and Wu, T.C. (2001). Tumor-specific immunity and anti-angiogenesis generated by a DNA vaccine encoding calreti-culin linked to a tumor antigen. J Clin Invest 108, 669-678. (Pubitemid 32906195)
12. Cheng, W.F., Hung, C.F., Hsu, K.F., Chai, C.Y., He, L., Polo, J.M., Slater, L.A., Ling, M., and Wu, T.C. (2002). Cancer immuno-therapy using Sindbis virus replicon particles encoding a VP22-antigen fusion. Hum Gene Ther 13, 553-568. (Pubitemid 34253156)
13. 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., and Kast, W.M. (1993). Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur J Immunol 23, 2242-2249. (Pubitemid 23265889)
14. Ferrara, A., Nonn, M., Sehr, P., Schreckenberger, C., Pawlita, M., Durst, M., Schneider, A., and Kaufmann, A.M. (2003). 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. (Pubitemid 37211193)
15. Garcia-Hernandez, E., Gonzalez-Sanchez, J.L., Andrade-Man-zano, A., Contreras, M.L., Padilla, S., Guzman, C.C., Jimenez, R., Reyes, L., Morosoli, G., Verde, M.L., and Rosales, R. (2006). Regression of papilloma high-grade lesions (CIN 2 and CIN 3) is stimulated by therapeutic vaccination with MVA E2 re-combinant vaccine. Cancer Gene Ther 13, 592-597.
16. Gronevik, E., von Steyern, F.V., Kalhovde, J.M., Tjelle, T.E., and Mathiesen, I. (2005). Gene expression and immune response kinetics using electroporation-mediated DNA delivery to muscle. J Gene Med 7, 218-227. (Pubitemid 40348026)
17. Han, D.J., Weiner, D.B., and Sin, J.I. (2010). DNA vaccines against infectious diseases and cancer. Biomol Ther 18, 1-15.
18. Hsu, K.F., Hung, C.F., Cheng, W.F., He, L., Slater, L.A., Ling, M., and Wu, T.C. (2001). Enhancement of suicidal DNA vaccine potency by linking Mycobacterium tuberculosis heat shock protein 70 to an antigen. Gene Ther 8, 376-383. (Pubitemid 32241937)
19. Huang, S., Apasov, S, Koshiba, M, and Sitkovsky, M. (1997). Role of A2a extracellular adenosine receptor-mediated signaling in adenosine-mediated inhibition of T-cell activation and expansion. Blood 90, 1600-1610. (Pubitemid 27355433)
20. Hung, C.F., Cheng, W.F., Hsu, K.F., Chai, C.Y., He, L., Ling, M., and Wu, T.C. (2001). Cancer immunotherapy using a DNA vaccine encoding the translocation domain of a bacterial toxin linked to a tumor antigen. Cancer Res 61, 3698-3703. (Pubitemid 32694982)
21. Hung, C.F., He, L., Juang, J., Lin, T.J., Ling, M., and Wu, T.C. (2002). Improving DNA vaccine potency by linking Marek's disease virus type 1 VP22 to an antigen. J Virol 76, 2676-2682. (Pubitemid 34184853)
22. Ji, H., Wang, T.L., Chen, C.H., Pai, S.I., Hung, C.F., Lin, K.Y., Kurman, R.J., Pardoll, D.M., and Wu, T.C. (1999). Targeting human papillomavirus type 16 E7 to the endosomal/lyso-somal compartment enhances the antitumor immunity of DNA vaccines against murine human papillomavirus type 16 E7-expressing tumors. Hum Gene Ther 10, 2727-2740.
23. Jin, D., Fan, J., Wang, L., Thompson, L.F., Liu, A., Daniel, B.J., Shin, T., Curiel, T.J., and Zhang, B. (2010). CD73 on tumor cells impairs antitumor T-cell responses: a novel mechanism of tumor-induced immune suppression. Cancer Res 70, 2245-2255.
24. Kaufmann, A., Nieland, J.D., Jochmus, I., Baur, S., Friese, K., Gabelsberger, J., Gieseking, F., Gissmann, L., Glasschröder, B., Grubert, T., Hillemanns, P., Hö pfl, R., Ikenberg, H., Schwarz, J., Karrasch, M., Knoll, A., Kü ppers, V., Lechmann, M., Lelle, R.J., Meissner, H., Mü ller, R.T., Pawlita, M., Petry, K.U., Pilch, H., Walek, E., and Schneider, A. (2007). Vaccination trial with HPV16 L1E7 chimeric virus-like particles in women suffering from high grade cervical intraepithelial neoplasia (CIN 2/3). Int J Cancer 121, 2794-2800. (Pubitemid 350136429)
25. Kaufmann, A.M., Stern, P.L., Rankin, E.M., Sommer, H., Nuessler, V., Schneider, A., Adams, M., Onon, T.S., Bau-knecht, T., Wagner, U., Kroon, K., Hickling, J., Boswell, C.M., Stacey, S.N., Kitchener, H.C., Gillard, J., Wanders, J., Roberts, J.S, and Zwierzina, H. (2002). 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. (Pubitemid 35424757)
26. Kim, M.S., and Sin, J.I. (2005). Both antigen optimization and lysosomal targeting are required for enhanced anti-tumour protective immunity in a human papillomavirus E7-expressing animal tumour model. Immunology 116, 255-266. (Pubitemid 41368667)
27. Kim, T.W., Hung, C.F., Boyd, D.A., He, L., Lin, C.T., Kaiserman, D., Bird, P.I., and Wu, T.C. (2004a). Enhancement of DNA vaccine potency by coadministration of a tumor antigen gene and DNA encoding serine protease inhibitor-6. Cancer Res 64, 400-405. (Pubitemid 38114124)
28. Kim, T.W., Hung, C.F., Kim, J.W., Juang, J., Chen, P.J., He, L., Boyd, D.A., and Wu, T.C. (2004b). 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. (Pubitemid 38210532)
29. Kim, T.Y., Myoung, H.J., Kim, J.H., Moon, I.S., Kim, T.G., Ahn W.S., and Sin, J.I. (2002). Both E7 and CpG-ODN are required for protective immunity against challenge with human pap-illomavirus 16 (E6/E7)-immortalized tumor cells: Involvement of CD4+ and CD8+ T cells in protection. Cancer Res 62, 7234-7240.
30. Liu, J., Kjeken, R., Mathiesen, I., and Barouch, D.H. (2008). Recruitment of antigen-presenting cells to the site of inoculation and augmentation of human immunodeficiency virus type 1 DNA vaccine immunogenicity by in vivo electroporation. J Virol 82, 5643-5649. (Pubitemid 351705271)
31. Luxembourg, A., Evans, C.F., and Hannaman, D. (2007). Elec-troporation based DNA immunization: translation to the clinic. Expert Opin Biol Ther 7, 1647-1664. (Pubitemid 350161649)
32. MacGregor, R.R., Boyer, J.D., Ugen, K.E., Lacy, K.E., Gluckman, S.J., Bagarazzi, M.L., Chattergoon, M.A., Baine, Y., Higgins, T.J., Ciccarelli, R.B., Coney, L.R., Ginsberg, R.S., and Weiner, D.B. (1998). First clinical trial of a DNA-based vaccine for treatment of HIV-1 infection: safety and host response. J Infect Dis 178, 92-100. (Pubitemid 28328080)
33. McKay, P.F., Barouch, D.H., Santra, S., Sumida, S.M., Jackson, S.S., Gorgone, D.A., Lifton, M.A., and Letvin, N.L. (2004). Recruitment of different subsets of antigen-presenting cells selectively modulates DNA vaccine-elicited CD4 and CD8 T lymphocyte responses. Eur J Immunol 34, 1011-1020. (Pubitemid 39255979)
34. Muderspach, L., Wilczynski, S., Roman, L., Bade, L., Felix, J., Small, L.A., Kast, W.M., Fascio, G., Marty, V., and Weber, J. (2000). 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.
35. Reinstein, E., Scheffner, M., Oren, M., Ciechanover, A., and Schwartz, A. (2000). Degradation of the E7 human papillo-mavirus oncoprotein by the ubiquitin-proteasome system: targeting via ubiquitination of the N-terminal residue. Onco-gene 19, 5944-5950. (Pubitemid 32005376)
36. Reits, E.A., Hodge, J.W., Herberts, C.A., Groothuis, T.A., Chakraborty, M., Wansley, E.K., Camphausen, K., Luiten, R.M., de Ru, A.H., Neijssen, J., Griekspoor, A., Mesman, E., Verreck, F.A., Spits, H., Schlom, J., van Veelen, P., and Neefjes, J.J. (2006). Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful anti-tumor immunotherapy. J Exp Med 203, 1259-1271. (Pubitemid 43736595)
37. Rizzuto, G., Cappelletti, M., Maione, D., Savino, R., Lazzaro, D., Costa, P., Mathiesen, I., Cortese, R., Ciliberto, G., Laufer, R., La Monica, N., and Fattori, E. (1999). Efficient and regulated erythropoietin production by naked DNA injection and muscle electroporation. Proc Natl Acad Sci USA 96, 6417-6422. (Pubitemid 29256680)
38. Roman, L., Wilczynski, S., Muderspach, L.I., Burnett, A.F., O'Meara, A., Brinkman, J.A., Kast, W.M., Facio, G., Felix, J.C., Aldana, M., and Weber, J.S. (2007). A phase II study of Hsp-7 (SGN-00101) in women with high-grade cervical in-traepithelial neoplasia. Gynecol Oncol 106, 558-566. (Pubitemid 47302472)
39. Santin, A.D., Bellone, S., Palmieri, M., Ravaggi, A., Romani, C., Tassi, R., Roman, J.J., Burnett, A., Pecorelli, S., and Cannon, M.J. (2006). HPV16/18 E7-pulsed dendritic cell vaccination in cervical cancer patients with recurrent disease refractory to standard treatment modalities. Gynecol Oncol 100, 469-478. (Pubitemid 43246861)
40. Sin, J.I. (2006). Human paillomavirus vaccines for the treatment of cervical cancer. Expert Rev Vaccines 5, 783-792.
41. Sin, J.I. (2009a). Promises and challenges of human papilloma-virus vaccines for cervical cancer. Exp Rev Anticancer Ther 9, 1-5.
42. Sin, J.I. (2009b). Suppression of antitumor protective cytotoxic T lymphocyte responses to a human papillomavirus 16 E7 DNA vaccine by coinjection of interleukin-12 cDNA: involvement of nitric oxide in immune suppression. Immunology 128, e707-e717.
43. Sin, J.I., Hong, S.H., Park, Y.J., Park, J.B., Choi, Y.S., and Kim, M.S. (2006). Antitumor therapeutic effects of E7 subunit and DNA vaccines in an animal cervical cancer model: antitumor efficacy of E7 therapeutic vaccines is dependent on tumor sizes, vaccine doses, and vaccine delivery routes. DNA Cell Biol 25, 277-286. (Pubitemid 43830441)
44. Sin, J.I, Kim, J.M., Bae, S.H., Lee, I.H., Park, J.S., and Ryoo, H.M. (2009). Adoptive transfer of human papillomavirus E7-specific CTL enhances tumor chemoresponse through the perforin/granzyme-mediated pathway. Mol Ther 17, 906-913.
45. Smotkin, D., and Wettstein, F.O. (1986). Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein. Proc Natl Acad Sci USA 83, 4680-4684. (Pubitemid 16075465)
46. Stagg, J., Divisekera, U., McLaughlin, N., Sharkey, J., Pommey, S., Denoyer, D., Dwyer, K.M., and Smyth, M.J. (2010). Anti-CD73 antibody therapy inhibits breast tumor growth and metastasis. Proc Natl Acad Sci USA 107, 1547-1552.
47. Stoler, M.H., Rhodes, C.R., Whitbeck, A., Wolinsky, S.M., Chow, L.T., and Broker, T.R. (1992). Human papillomavirus type 16 and 18 gene expression in cervical neoplasias. Hum Pathol 23, 117-128.
48. Sumida, S.M., McKay, P.F., Truitt, D.M., Kishko, M.G., Arthur, J.C., Seaman, M.S., Jackson, S.S., Gorgone, D.A., Lifton, M.A., Letvin, N.L., and Barouch, D.H. (2004). Recruitment and expansion of dendritic cells in vivo potentiate the immunoge-nicity of plasmid DNA vaccines. J Clin Investig 114, 1334-1342. (Pubitemid 40385305)
49. van Driel, W.J., Ressing, M.E., Kenter, G.G., Brandt, R.M., Krul, E.J., van Rossum, A.B., Schuuring, E., Offringa, R., Bauknecht, T., Tamm-Hermelink, A., van Dam, P.A., Fleuren, G.J., Kast, W.M., Melief, C.J., and Trimbos, J.B. (1999). Vaccination with HPV16 peptides of patients with advanced cervical carcinoma: clinical evaluation of a phase I-II trial. Eur J Cancer 35, 946-952. (Pubitemid 29277130)
50. Vannoni, D., Bernini, A., Carlucci, F., Civitelli, S., Di Pietro, M.C., Leoncini, R., Rosi, F., Tabucchi, A., Tanzini, G., and Marinello, E. (2004). Enzyme activities controlling adenosine levels in normal and neoplastic tissues. Med Oncol 21, 187-195. (Pubitemid 39108009)
51. Wang, R., Doolan, D.L., Le, T.P., Hedstrom, R.C., Coonan, K.M., Charoenvit, Y., Jones, T.R., Hobart, P., Margalith, M., Ng, J., Weiss, W.R., Sedegah, M., de Taisne, C., Norman, J.A., and Hoffman, S.L. (1998). Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science 282, 476-480. (Pubitemid 28483675)
52. Widera, G., Austin, M., Rabussay, D., Goldbeck, C., Barnett, S.W., Chen, M., Leung, L., Otten, G.R., Thudium, K., Selby, M.J., and Ulmer, J.B. (2000). Increased DNA vaccine delivery and immunogenicity by electroporation in vivo. J Immunol 164, 4635-4640. (Pubitemid 30238062)
53. Ye, G.W., Park, J.B., Park, Y.J., Choi, Y.S., and Sin, J.I. (2007). Increased sensitivity of radiated murine cervical cancer tumors to E7 subunit vaccine-driven CTL-mediated killing induces synergistic antitumor activity. Mol Ther 15, 1564-1570. (Pubitemid 47099314)
54. Zhang, L., Tang, Y., Akbulut, H., Zelterman, D., Linton, P.J., and Deisseroth, A.B. (2003). An adenoviral vector cancer vaccine that delivers a tumor-associated antigen/CD40-ligand fusion protein to dendritic cells. Proc Natl Acad Sci USA 100, 15101-15106. (Pubitemid 37518023)