Intratumoral IL-12 gene therapy results in the crosspriming of tc1 cells reactive against tumor-associated stromal antigens

Molecular Therapy

Volumn 19, Issue 4, 2011, Pages 805-814

  Zhao, Xi ^a   Bose, Anamika ^a   Komita, Hideo ^a   Taylor, Jennifer L ^a   Kawabe, Mayumi ^a   Chi, Nina ^a   Spokas, Laima ^a   Lowe, Devin B ^a   Goldbach, Christina ^a   Alber, Sean ^a   Watkins, Simon C ^a   Butterfield, Lisa H ^a,b   Kalinski, Pawel ^a   Kirkwood, John M ^a,b   Storkus, Walter J ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; GAMMA INTERFERON; HLA A2 ANTIGEN; INTERLEUKIN 12; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; TUMOR ANTIGEN; TUMOR ASSOCIATED STROMAL ANTIGEN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN RECOGNITION; ARTICLE; CD8+ T LYMPHOCYTE; CELL ISOLATION; CELL SURFACE; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE RELEASE; DENDRITIC CELL; EFFECTOR CELL; ENDOTHELIUM CELL; FEMALE; GENE THERAPY; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; MELANOMA; MELANOMA B16; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PERICYTE; PROTEIN EXPRESSION; STROMA CELL; TARGET CELL; TRANSGENIC MOUSE; TUMOR CELL; VASCULAR ENDOTHELIUM;

MUS; MUS MUSCULUS;

EID: 79953322613     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2010.295     Document Type: Article

References (50)

1. Ostrand-Rosenberg, S (2008). Immune surveillance: a balance between pro-tumor and anti-tumor immunity. Curr Opin Genet Dev 18: 11-18. (Pubitemid 351694442)
2. Reiman, JM, Kmieciak, M, Manjili, MH and Knutson, KL (2007). Tumor immunoediting and immunosculpting pathways to cancer progression. Semin Cancer Biol 17: 275-287. (Pubitemid 47211962)
3. Bui, JD and Schreiber, RD (2007). Cancer immunosurveillance, immunoediting and inflammation: independent or interdependent processes? Curr Opin Immunol 19: 203-208. (Pubitemid 46356963)
4. Slingluff, CL Jr, Chianese-Bullock, KA, Bullock, TN, Grosh, WW, Mullins, DW, Nichols, L et al. (2006). Immunity to melanoma antigens: from self-tolerance to immunotherapy. Adv Immunol 90: 243-295. (Pubitemid 43786236)
5. Yu, Z and Restifo, NP (2002). Cancer vaccines: progress reveals new complexities. J Clin Invest 110: 289-294. (Pubitemid 34847958)
6. Bellone, S, Pecorelli, S, Cannon, MJ and Santin, AD (2007). Advances in dendriticcell- based therapeutic vaccines for cervical cancer. Expert Rev Anticancer Ther 7: 1473-1486. (Pubitemid 351835155)
7. Singh, R and Paterson, Y (2007). Immunoediting sculpts tumor epitopes during immunotherapy. Cancer Res 67: 1887-1892. (Pubitemid 46424202)
8. Gajewski, TF, Fallarino, F, Ashikari, A and Sherman, M (2001). Immunization of HLA-A2+ melanoma patients with MAGE-3 or MelanA peptide-pulsed autologous peripheral blood mononuclear cells plus recombinant human interleukin 12. Clin Cancer Res 7(3 Suppl): 895s-901s. (Pubitemid 33600943)
9. Feltkamp, MC, Smits, HL, Vierboom, MP, Minnaar, RP, de Jongh, BM, Drijfhout, JW et al. (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)
10. Hofmeister, V, Schrama, D and Becker, JC (2008). Anti-cancer therapies targeting the tumor stroma. Cancer Immunol Immunother 57: 1-17. (Pubitemid 350043655)
11. Zhang, B, Bowerman, NA, Salama, JK, Schmidt, H, Spiotto, MT, Schietinger, A et al. (2007). Induced sensitization of tumor stroma leads to eradication of established cancer by T cells. J Exp Med 204: 49-55. (Pubitemid 46148755)
12. Loberg, RD, Gayed, BA, Olson, KB and Pienta, KJ (2005). A paradigm for the treatment of prostate cancer bone metastases based on an understanding of tumor cell-microenvironment interactions. J Cell Biochem 96: 439-446. (Pubitemid 41504643)
13. Komita, H, Zhao, X, Taylor, JL, Sparvero, LJ, Amoscato, AA, Alber, S et al. (2008). CD8+ T-cell responses against hemoglobin-prevent solid tumor growth. Cancer Res 68: 8076-8084.
14. Hatano, M, Kuwashima, N, Tatsumi, T, Dusak, JE, Nishimura, F, Reilly, KM et al. (2004). Vaccination with EphA2-derived T cell-epitopes promotes immunity against both EphA2-expressing and EphA2-negative tumors. J Transl Med 2: 40.
15. Maciag, PC, Seavey, MM, Pan, ZK, Ferrone, S and Paterson, Y (2008). Cancer immunotherapy targeting the high molecular weight melanoma-associated antigen protein results in a broad antitumor response and reduction of pericytes in the tumor vasculature. Cancer Res 68: 8066-8075.
16. Ishizaki, H, Tsunoda, T, Wada, S, Yamauchi, M, Shibuya, M and Tahara, H (2006). Inhibition of tumor growth with antiangiogenic cancer vaccine using epitope peptides derived from human vascular endothelial growth factor receptor 1. Clin Cancer Res 12: 5841-5849. (Pubitemid 44629617)
17. Wada, S, Tsunoda, T, Baba, T, Primus, FJ, Kuwano, H, Shibuya, M et al. (2005). Rationale for antiangiogenic cancer therapy with vaccination using epitope peptides derived from human vascular endothelial growth factor receptor 2. Cancer Res 65: 4939-4946. (Pubitemid 40740834)
18. Kaplan, CD, Krüger, JA, Zhou, H, Luo, Y, Xiang, R and Reisfeld, RA (2006). A novel DNA vaccine encoding PDGFRbeta suppresses growth and dissemination of murine colon, lung and breast carcinoma. Vaccine 24: 6994-7002. (Pubitemid 46107180)
19. Liu, W, Parikh, AA, Stoeltzing, O, Fan, F, McCarty, MF, Wey, J et al. (2005). Upregulation of neuropilin-1 by basic fibroblast growth factor enhances vascular smooth muscle cell migration in response to VEGF. Cytokine 32: 206-212. (Pubitemid 43144652)
20. Silver, DA, Pellicer, I, Fair, WR, Heston, WD and Cordon-Cardo, C (1997). Prostatespecific membrane antigen expression in normal and malignant human tissues. Clin Cancer Res 3: 81-85. (Pubitemid 27079448)
21. Harada, M, Matsueda, S, Yao, A, Ogata, R, Noguchi, M and Itoh, K (2004). Prostaterelated antigen-derived new peptides having the capacity of inducing prostate cancerreactive CTLs in HLA-A2+ prostate cancer patients. Oncol Rep 12: 601-607.
22. Bondjers, C, Kalén, M, Hellström, M, Scheidl, SJ, Abramsson, A, Renner, O et al. (2003). Transcription profiling of platelet-derived growth factor-B-deficient mouse embryos identifies RGS5 as a novel marker for pericytes and vascular smooth muscle cells. Am J Pathol 162: 721-729. (Pubitemid 36237480)
23. Boss, CN, Grünebach, F, Brauer, K, Häntschel, M, Mirakaj, V, Weinschenk, T et al. (2007). Identification and characterization of T-cell epitopes deduced from RGS5, a novel broadly expressed tumor antigen. Clin Cancer Res 13: 3347-3355. (Pubitemid 46944922)
24. Christian, S, Winkler, R, Helfrich, I, Boos, AM, Besemfelder, E, Schadendorf, D et al. (2008). Endosialin (Tem1) is a marker of tumor-associated myofibroblasts and tumor vessel-associated mural cells. Am J Pathol 172: 486-494. (Pubitemid 351282034)
25. Kuball, J, Schmitz, FW, Voss, RH, Ferreira, EA, Engel, R, Guillaume, P et al. (2005). Cooperation of human tumor-reactive CD4+ and CD8+ T cells after redirection of their specificity by a high-affinity p53A2.1-specific TCR. Immunity 22: 117-129. (Pubitemid 40143456)
26. Mittendorf, EA, Storrer, CE, Shriver, CD, Ponniah, S and Peoples, GE (2005). Evaluation of the CD107 cytotoxicity assay for the detection of cytolytic CD8+ cells recognizing HER2/neu vaccine peptides. Breast Cancer Res Treat 92: 85-93. (Pubitemid 40875083)
27. Tatsumi, T, Herrem, CJ, Olson, WC, Finke, JH, Bukowski, RM, Kinch, MS et al. (2003). Disease stage variation in CD4+ and CD8+ T-cell reactivity to the receptor tyrosine kinase EphA2 in patients with renal cell carcinoma. Cancer Res 63: 4481-4489. (Pubitemid 36951020)
28. Yuan, J, Gnjatic, S, Li, H, Powel, S, Gallardo, HF, Ritter, E et al. (2008). CTLA-4 blockade enhances polyfunctional NY-ESO-1 specific T cell responses in metastatic melanoma patients with clinical benefit. Proc Natl Acad Sci USA 105: 20410-20415.
29. Woodland, DL and Dutton, RW (2003). Heterogeneity of CD4+ and CD8+ T cells. Curr Opin Immunol 15: 336-342.
30. Fukumura, D and Jain, RK (2007). Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization. Microvasc Res 74: 72-84. (Pubitemid 350051025)
31. Willett, CG, Boucher, Y, di Tomaso, E, Duda, DG, Munn, LL, Tong, RT et al. (2004). Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 10: 145-147. (Pubitemid 38524883)
32. Jain, RK (2005). Antiangiogenic therapy for cancer: current and emerging concepts. Oncology (Williston Park, NY) 19(4 Suppl 3): 7-16.
33. Hamzah, J, Jugold, M, Kiessling, F, Rigby, P, Manzur, M, Marti, HH et al. (2008). Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature 453: 410-414. (Pubitemid 351693122)
34. Manzur, M, Hamzah, J and Ganss, R (2008). Modulation of the "blood-tumor" barrier improves immunotherapy. Cell Cycle 7: 2452-2455.
35. Krupnick, AS, Kreisel, D, Popma, SH, Balsara, KR, Szeto, WY, Krasinskas, AM et al. (2002). Mechanism of T cell-mediated endothelial apoptosis. Transplantation 74: 871-876.
36. Okaji, Y, Tsuno, NH, Kitayama, J, Saito, S, Takahashi, T, Kawai, K et al. (2004). Vaccination with autologous endothelium inhibits angiogenesis and metastasis of colon cancer through autoimmunity. Cancer Sci 95: 85-90. (Pubitemid 38208412)
37. Suidan, GL, Mcdole, JR, Chen, Y, Pirko, I and Johnson, AJ (2008). Induction of blood brain barrier tight junction protein alterations by CD8 T cells. PLoS ONE 3: e3037.
38. Suzuki, H, Shibano, K, Okane, M, Kono, I, Matsui, Y, Yamane, K et al. (1989). Interferon-gamma modulates messenger RNA levels of c-sis (PDGF-B chain), PDGF-A chain, and IL-1 beta genes in human vascular endothelial cells. Am J Pathol 134: 35-43. (Pubitemid 19054976)
39. Molander, C, Kallin, A, Izumi, H, Rönnstrand, L and Funa, K (2000). TNF-suppresses the PDGF beta-receptor kinase. Exp Cell Res 258: 65-71.
40. Strehl, B, Seifert, U, Krüger, E, Heink, S, Kuckelkorn, U and Kloetzel, PM (2005). Interferon-gamma, the functional plasticity of the ubiquitin-proteasome system, and MHC class I antigen processing. Immunol Rev 207: 19-30. (Pubitemid 41415005)
41. Sun, Y, Stevanovic, S, Song, M, Schwantes, A, Kirkpatrick, CJ, Schadendorf, D et al. (2006). The kinase insert domain-containing receptor is an angiogenesis-associated antigen recognized by human cytotoxic T lymphocytes. Blood 107: 1476-1483. (Pubitemid 43242384)
42. Tatsumi, T, Huang, J, Gooding, WE, Gambotto, A, Robbins, PD, Vujanovic, NL et al. (2003). Intratumoral delivery of dendritic cells engineered to secrete both interleukin (IL)-12 and IL-18 effectively treats local and distant disease in association with broadly reactive Tc1-type immunity. Cancer Res 63: 6378-6386. (Pubitemid 37255187)
43. Van der Most, RG, Currie, A, Robinson, BW and Lake, RA (2006). Cranking the immunologic engine with chemotherapy: using context to drive tumor antigen crosspresentation towards useful antitumor immunity. Cancer Res 66: 601-604. (Pubitemid 43165917)
44. Butterfield, LH, Ribas, A, Dissette, VB, Amarnani, SN, Vu, HT, Oseguera, D et al. (2003). Determinant spreading associated with clinical response in dendritic cellbased immunotherapy for malignant melanoma. Clin Cancer Res 9: 998-1008. (Pubitemid 36323703)
45. Ranieri, E, Kierstead, LS, Zarour, H, Kirkwood, JM, Lotze, MT, Whiteside, T et al. (2000). Dendritic cell/peptide cancer vaccines: clinical responsiveness and epitope spreading. Immunol Invest 29: 121-125. (Pubitemid 30316952)
46. Lehmann, PV, Sercarz, EE, Forsthuber, T, Dayan, CM and Gammon, G (1993). Determinant spreading and the dynamics of the autoimmune T-cell repertoire. Immunol Today 14: 203-208. (Pubitemid 23124512)
47. Firat, H, Cochet, M, Rohrlich, PS, Garcia-Pons, F, Darche, S, Danos, O et al. (2002). Comparative analysis of the CD8+ T cell repertoires of H-2 class I wild-type/HLA-A2.1 and H-2 class I knockout/HLA-A2.1 transgenic mice. Int Immunol 14: 925-934.
48. Burg, MA, Pasqualini, R, Arap, W, Ruoslahti, E and Stallcup, WB (1999). NG2 proteoglycan-binding peptides target tumor neovasculature. Cancer Res 59: 2869-2874. (Pubitemid 29283125)
49. Crisan, M, Yap, S, Casteilla, L, Chen, CW, Corselli, M, Park, TS et al. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3: 301-313.
50. Stuber, G, Leder, GH, Storkus, WT, Lotze, MT, Modrow, S, Székely, L et al. (1994). Identification of wild-type and mutant p53 peptides binding to HLA-A2 assessed by a peptide loading-deficient cell line assay and a novel major histocompatibility complex class I peptide binding assay. Eur J Immunol 24: 765-768. (Pubitemid 24076647)