Electroporation driven delivery of both an IL-12 expressing plasmid and cisplatin synergizes to inhibit B16 melanoma tumor growth through an NK cell mediated tumor killing mechanism

Human Vaccines and Immunotherapeutics

Volumn 8, Issue 11, 2012, Pages 1714-1721

  Kim, Ha ^a   Sin, Jeong Im ^a  

^a Kangwon National University   (South Korea)

Author keywords

Antitumor immunity; Cisplatin; Electroporation; IL 12; Melanoma; NK cells

Indexed keywords

CISPLATIN; COMPLEMENTARY DNA; DOPACHROME TAUTOMERASE; GAMMA INTERFERON; INTERLEUKIN 12;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; DRUG POTENTIATION; ELECTROPORATION; FEMALE; INTERFERON INDUCTION; INTERFERON PRODUCTION; LYMPHOCYTE DEPLETION; MELANOMA B16; MOUSE; NATURAL KILLER CELL; NONHUMAN; SPLEEN CELL;

ANTITUMOR IMMUNITY; CISPLATIN; ELECTROPORATION; IL-12; MELANOMA; NK CELLS;

ANIMALS; CISPLATIN; ELECTROPORATION; FEMALE; INTERFERON-GAMMA; INTERLEUKIN-12; KILLER CELLS, NATURAL; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C;

EID: 84869797481     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.22346     Document Type: Article

References (31)

1. Li Y, McClay EF. Systemic chemotherapy for the treatment of metastatic melanoma. Semin Oncol 2002; 29:413-26; PMID:12407507; http://dx.doi.org/10.1053/ sonc.2002.35237.
2. Bajetta E, Del Vecchio M, Bernard-Marty C, Vitali M, Buzzoni R, Rixe O, et al. Metastatic melanoma: chemotherapy. Semin Oncol 2002; 29:427-45; PMID:12407508; http://dx.doi.org/10.1053/sonc.2002.35238.
3. Rosenberg SA, Spiess P, Lafreniere R. A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science 1986; 233:1318-21; PMID:3489291; http://dx.doi.org/10.1126/science. 3489291.
4. Dudley ME, Rosenberg SA. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nat Rev Cancer 2003; 3:666-75; PMID:12951585; http://dx.doi.org/10.1038/nrc1167.
5. Kobayashi M, Fitz L, Ryan M, Hewick RM, Clark SC, Chan S, et al. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J Exp Med 1989; 170:827-45; PMID:2504877; http://dx.doi.org/10.1084/jem.170.3.827.
6. Robertson MJ, Soiffer RJ, Wolf SF, Manley TJ, Donahue C, Young D, et al. Response of human natural killer (NK) cells to NK cell stimulatory factor (NKSF): cytolytic activity and proliferation of NK cells are differentially regulated by NKSF. J Exp Med 1992; 175:779-88; PMID:1346796; http://dx.doi.org/10.1084/jem.175.3.779.
7. Germann T, Gately MK, Schoenhaut DS, Lohoff M, Mattner F, Fischer S, et al. Interleukin-12/T cell stimulating factor, a cytokine with multiple effects on T helper type 1 (Th1) but not on Th2 cells. Eur J Immunol 1993; 23:1762-70; PMID:8102100; http://dx.doi.org/10.1002/eji.1830230805.
8. Rakhmilevich AL, Turner J, Ford MJ, McCabe D, Sun WH, Sondel PM, et al. Gene gun-mediated skin transfection with interleukin 12 gene results in regression of established primary and metastatic murine tumors. Proc Natl Acad Sci U S A 1996; 93:6291-6; PMID:8692808; http://dx.doi.org/10.1073/ pnas.93.13.6291.
9. Yu WG, Ogawa M, Mu J, Umehara K, Tsujimura T, Fujiwara H, et al. IL-12-induced tumor regression correlates with in situ activity of IFN-gamma produced by tumor-infiltrating cells and its secondary induction of anti-tumor pathways. J Leukoc Biol 1997; 62:450-7;PMID:9335314.
10. Dias S, Thomas H, Balkwill F. Multiple molecular and cellular changes associated with tumour stasis and regression during IL-12 therapy of a murine breast cancer model. Int J Cancer 1998; 75:151-7; PMID:9426704; http://dx.doi.org/10.1002/ (SICI)1097-0215(19980105)75:1〈151:: AIDIJC23〉 3.0.CO;2-I.
11. Gambotto A, Tüting T, McVey DL, Kovesdi I, Tahara H, Lotze MT, et al. Induction of antitumor immunity by direct intratumoral injection of a recombinant adenovirus vector expressing interleukin-12. Cancer Gene Ther 1999; 6:45-53; PMID:10078963; http://dx.doi.org/10.1038/sj.cgt.7700013.
12. Mazzolini G, Qian C, Xie X, Sun Y, Lasarte JJ, Drozdzik M, et al. Regression of colon cancer and induction of antitumor immunity by intratumoral injection of adenovirus expressing interleukin-12. Cancer Gene Ther 1999; 6:514-22; PMID:10608348; http://dx.doi.org/10.1038/sj.cgt.7700072.
13. Narvaiza I, Mazzolini G, Barajas M, Duarte M, Zaratiegui M, Qian C, et al. Intratumoral coinjection of two adenoviruses, one encoding the chemokine IFN-gamma-inducible protein-10 and another encoding IL-12, results in marked antitumoral synergy. J Immunol 2000; 164:3112-22; PMID:10706701.
14. Ahn WS, Bae SM, Kim TY, Kim TG, Lee JM, Namkoong SE, 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 2003; 14:1389-99; PMID:14577920; http://dx.doi.org/10.1089/104303403769211619.
15. 180-188 peptides. Cancer Immunol Immunother 2012; 61:1671-82; PMID:22382361; http://dx.doi.org/10. 1007/s00262-012-1214-8.
16. Bronte V, Apolloni E, Ronca R, Zamboni P, Overwijk WW, Surman DR, et al. Genetic vaccination with "self " tyrosinase-related protein 2 causes melanoma eradication but not vitiligo. Cancer Res 2000; 60:253-8; PMID:10667570.
17. Lladser A, Mougiakakos D, Tufvesson H, Ligtenberg MA, Quest AF, Kiessling R, et al. DAI (DLM-1/ ZBP1) as a genetic adjuvant for DNA vaccines that promotes effective antitumor CTL immunity. Mol Ther 2011; 19:594-601; PMID:21157438; http://dx.doi.org/10.1038/mt.2010.268.
18. Cho HI, Celis E. Optimized peptide vaccines eliciting extensive CD8 T-cell responses with therapeutic antitumor effects. Cancer Res 2009; 69:9012-9; PMID:19903852; http://dx.doi.org/10.1158/0008-5472.CAN-09-2019.
19. Suzuki E, Kapoor V, Jassar AS, Kaiser LR, Albelda SM, Albelda SM. Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin Cancer Res 2005; 11:6713-21; PMID:16166452; http://dx.doi.org/10.1158/1078-0432.CCR-05- 0883.
20. Bae SH, Park YJ, Park JB, Choi YS, 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 2007; 13:341-9; PMID:17200373; http://dx.doi.org/10.1158/1078-0432.CCR-06-1838.
21. Ramakrishnan R, Assudani D, Nagaraj S, Hunter T, Cho HI, Antonia S, et al. Chemotherapy enhances tumor cell susceptibility to CTL-mediated killing during cancer immunotherapy in mice. J Clin Invest 2010; 120:1111-24; PMID:20234093; http://dx.doi.org/10.1172/JCI40269.
22. Hong M, Puaux AL, Huang C, Loumagne L, Tow C, Mackay C, et al. Chemotherapy induces intratumoral expression of chemokines in cutaneous melanoma, favoring T-cell infiltration and tumor control. Cancer Res 2011; 71:6997-7009; PMID:21948969; http://dx.doi.org/10.1158/0008-5472.CAN-11-1466.
23. Jaroszeski MJ, Gilbert R, Perrott R, Heller R. Enhanced effects of multiple treatment electrochemotherapy. Melanoma Res 1996; 6:427-33; PMID:9013480; http://dx.doi.org/10.1097/00008390-199612000-00004.
24. 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 2007; 15:1564-70; PMID:17505485; http://dx.doi.org/10.1038/sj.mt.6300149.
25. Lee IH, Park JB, Cheong M, Choi YS, Park D, Sin JI. Antitumor therapeutic and antimetastatic activity of electroporation-delivered human papillomavirus 16 E7 DNA vaccines: a possible mechanism for enhanced tumor control. DNA Cell Biol 2011; 30:975-85; PMID:21649506; http://dx.doi.org/10.1089/dna.2011.1266.
26. Li S, Zhang L, Torrero M, Cannon M, Barret R. Administration route- and immune cell activation-dependent tumor eradication by IL12 electrotransfer. Mol Ther 2005; 12:942-9; PMID:15953768; http://dx.doi.org/10.1016/j.ymthe.2005.03. 037.
27. Kim JH, Ajaz M, Lokshin A, Lee YJ. Role of antiapoptotic proteins in tumor necrosis factor-related apoptosis-inducing ligand and cisplatin-augmented apoptosis. Clin Cancer Res 2003; 9:3134-41; PMID:12912965.
28. Keane MM, Ettenberg SA, Nau MM, Russell EK, Lipkowitz S. Chemotherapy augments TRAIL-induced apoptosis in breast cell lines. Cancer Res 1999; 59:734-41; PMID:9973225.
29. Zisman A, Ng CP, Pantuck AJ, Bonavida B, Belldegrun AS. Actinomycin D and gemcitabine synergistically sensitize androgen-independent prostate cancer cells to Apo2L/TRAIL-mediated apoptosis. J Immunother 2001; 24:459-71; PMID:11759069; http://dx.doi.org/10.1097/00002371-200111000-00003.
30. Yang S, Haluska FG. Treatment of melanoma with 5-fluorouracil or dacarbazine in vitro sensitizes cells to antigen-specific CTL lysis through perforin/granzyme- and Fas-mediated pathways. J Immunol 2004; 172:4599-608; PMID:15034078.
31. Leonard JP, Sherman ML, Fisher GL, Buchanan LJ, Larsen G, Atkins MB, et al. Effects of single-dose interleukin-12 exposure on interleukin-12-associated toxicity and interferon-gamma production. Blood 1997; 90:2541-8; PMID:9326219.