Glioma immunotherapy by IL-21 gene-modified cells or by recombinant IL-21 involves antibody responses

International Journal of Cancer

Volumn 121, Issue 8, 2007, Pages 1756-1763

  Daga, Antonio ^a   Orengo, Anna Maria ^a   Gangemi, Rosaria Maria Rita ^a   Marubbi, Daniela ^a,b   Perera, Marzia ^a   Comes, Alberto ^a   Ferrini, Silvano ^a   Corte, Giorgio ^a,b  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

Author keywords

Antibodies; Glioma; Immunotherapy; NK; rIL21

Indexed keywords

CANCER ANTIBODY; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 21; RECOMBINANT INTERLEUKIN 21; RETROVIRUS VECTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; BYSTANDER EFFECT; CANCER GRAFT; CANCER IMMUNOTHERAPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENETIC TRANSDUCTION; GLIOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR REJECTION;

ANIMALS; ANTIBODIES, NEOPLASM; BLOTTING, WESTERN; BRAIN NEOPLASMS; BYSTANDER EFFECT; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GERM-FREE LIFE; GLIOMA; HUMANS; INTERLEUKIN-12; INTERLEUKIN-2; INTERLEUKINS; KAPLAN-MEIERS ESTIMATE; MICE; MICE, INBRED C57BL; TRANSDUCTION, GENETIC;

EID: 34548681848     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.22901     Document Type: Article

References (44)

1. Behin A, Hoang-Xuan K, Carpentier AF, Delattre JY. Primary brain tumors in adults. Lancet 2003;361:323-31 (review).
2. Grossman SA, Batara JF. Current management of glioblastoma multiforme. Semin Oncol 2004;31:635-44 (review).
3. Murphy A, Westwood JA, Teng MW, Moeller M, Darcy PK, Kershaw MH. Gene modification strategies to induce tumor immunity. Immunity 2005;22:403-14 (review).
4. Yamanaka R. Novel immunotherapeutic approaches to glioma. Curr Opin Mol Ther 2006;8:46-51 (review).
5. Curtin JF, King GD, Candolfi M, Greeno RB, Kroeger KM, Lowenstein PR, Castro MG. Combining cytotoxic and immune-mediated gene therapy to treat brain tumors. Curr Top Med Chem 2005;5:1151-70 (review).
6. Giezeman-Smits KM, Okada H, Brissette-Storkus CS, Villa LA, Attanucci J, Lotze MT, Pollack IF, Bozik ME, Chambers WH. Cytokine gene therapy of gliomas: induction of reactive CD4+ T cells by interleukin-4-transfected 9L gliosarcoma is essential for protective immunity. Cancer Res 2000;60:2449-57.
7. Yuan X, Hu J, Belladonna ML, Black KL, Yu JS. Interleukin-23-expressing bone marrow-derived neural stem-like cells exhibit antitumor activity against intracranial glioma. Cancer Res 2006;66:2630-8.
8. Tahara H, Lotze MT. Antitumor effects of interleukin-12 (IL-12): applications for the immunotherapy and gene therapy of cancer. Gene Ther 1995;2:96-106.
9. Figlin RA, Parker SE, Horton HM Technology evaluation: interleukin-2 gene therapy for the treatment of renal cell carcinoma. Curr Opin Mol Ther 1999;1:271-8 (review).
10. Melero I, Mazzolini G, Narvaiza I, Qian C, Chen L, Prieto J. IL-12 gene therapy for cancer: in synergy with other immunotherapies. Trends Immunol 2001;22:113-5.
11. Wigginton JM, Wiltrout RH IL-12/IL-2 combination cytokine therapy for solid tumors: translation from bench to bedside. Expert Opin Biol Ther 2002;2:513-24 (review).
12. Parrish-Novak J, Dillon SR, Nelson A, Hammond A, Sprecher C, Gross JA, Johnston J, Madden K, Xu W, West J, Schrader S, Burkhead S, et al. Interleukin-21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature 2000;408:57-63.
13. Leonard WJ, Spolski R. Interleukin-21: a modulator of lymphoid proliferation, apoptosis and differentiation. Nat Rev Immunol 2005;5:688-98 (review).
14. Asao H, Okuyama C, Kumaki S, Ishii N, Tsuchiya S, Foster D, Sugamura K. Cutting edge: the common γ-chain is an indispensable subunit of the IL-21 receptor complex. J Immunol 2001;167:1-5.
15. Di Carlo E, Comes A, Orengo AM, Rosso O, Meazza R, Musiani P, Colombo MP, Ferrini S. IL-21 induces tumor rejection by specific CTL and IFN-γ-dependent CXC chemokines in syngeneic mice. J Immunol 2004;172:1540-7.
16. van Leeuwen EM, Gamadia LE, Baars PA, Remmerswaal EB, ten Berge IJ, van Lier RA. Proliferation requirements of cytomegalovirus-specific, effector-type human CD8+ T cells. J Immunol 2002;169:5838-9.
17. Kasaian MT, Whitters MJ, Carter LL, Lowe LD, Jussif JM, Deng B, Johnson KA, Witek JS, Senices M, Konz RF, Wurster AL, Donaldson DD, et al. IL-21 limits NK cell responses and promotes antigen-specific T cell activation: a mediator of the transition from innate to adaptive immunity. Immunity 2002;16:559-69.
18. Wang G, Tschoi M, Spolski R, Lou Y, Ozaki K, Feng C, Kim G, Leonard WJ, Hwu P. In vivo antitumor activity of interleukin 21 mediated by natural killer cells. Cancer Res 2003;63:9016-22.
19. Brady J, Hayakawa Y, Smyth MJ, Nutt SL. IL-21 induces the functional maturation of murine NK cells. J Immunol 2004;172:2048-58.
20. Moroz A, Eppolito C, Li Q, Tao J, Clegg CH, Shrikant PA. IL-21 enhances and sustains CD8+ T cell responses to achieve durable tumor immunity: comparative evaluation of IL-2, IL-15, and IL-21. J Immunol 2004;173:900-9.
21. Comes A, Rosso O, Orengo AM, Di Carlo E, Sorrentino C, Meazza R, Piazza T, Valzasina B, Nanni P, Colombo MP, Ferrini S. CD25+ regulatory T cell depletion augments immunotherapy of micrometastases by an IL-21-secreting cellular vaccine. J Immunol 2006;176:1750-8.
22. Ma HL, Whitters MJ, Konz RF, Senices M, Young DA, Grusby MJ, Collins M, Dunussi-Joannopoulos K. IL-21 activates both innate and adaptive immunity to generate potent antitumor responses that require perforin but are independent of IFN-γ. J Immunol 2003;171:608-15.
23. Ozaki K, Spolski R, Feng CG, Qi CF, Cheng J, Sher A, Morse HC 3rd, Liu C, Schwartzberg PL, Leonard WJ. A critical role for IL-21 in regulating immunoglobulin production. Science 2002;298:1630-4.
24. Jarnicki AG, Lysaght J, Todryk S, Mills KH. Suppression of antitumor immunity by IL-10 and TGF-β-producing T cells infiltrating the growing tumor: influence of tumor environment on the induction of CD4+ and CD8+ regulatory T cells. J Immunol 2006;177:896-904.
25. Menoret A, Myers LM, Lee SJ, Mittler RS, Rossi RJ, Vella AT. TGFβ protein processing and activity through TCR triggering of primary CD8+ T regulatory cells. J Immunol 2006;177:6091-7.
26. Meloni F, Morosini M, Solari N, Passadore I, Nascimbene C, Novo M, Ferrari M, Cosentino M, Marino F, Pozzi E, Fietta AM. Foxp3 expressing CD4+ CD25+ and CD8+CD28- T regulatory cells in the peripheral blood of patients with lung cancer and pleural mesothelioma. Hum Immunol 2006;67:1-12.
27. Kitamura D, Roes J, Kuhn R, Rajewsky K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 1991;350:423-6.
28. Ransohoff RM, Kivisakk P, Kidd G. Three or more routes for leukocyte migration into the central nervous system. Nat Rev Immunol 2003;3:569-81 (review).
29. Walker PR, Calzascia T, Dietrich PY. All in the head: obstacles for immune rejection of brain tumours. Immunology 2002;107:28-38 (review).
30. Kikuchi T, Joki T, Akasaki Y, Abe T, Ohno T. Induction of antitumor immunity using intercellular adhesion molecule 1 (ICAM-1) transfection in mouse glioma cells. Cancer Lett 1999;142:201-6.
31. Sadlack B, Lohler J, Schorle H, Klebb G, Haber H, Sickel E, Noelle RJ, Horak I. Generalized autoimmune disease in interleukin-2-deficient mice is triggered by an uncontrolled activation and proliferation of CD4+ T cells. Eur J Immunol 1995;25:3053-9.
32. Willerford DM, Chen J, Ferry JA, Davidson L, Ma A, Alt FW. Interleukin-2 receptor α chain regulates the size and content of the peripheral lymphoid compartment. Immunity 1995;3:521-30.
33. Schwartz RH. Natural regulatory T cells and self tolerance. Nat Immunol 2005;6:327-30.
34. Shimizu J, Yamazaki S, Sakaguchi S. Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity. J Immunol 1999;163:5211-8.
35. Wang HY, Lee DA, Peng G, Guo Z, Li Y, Kiniwa Y, Shevach EM, Wang RF. Tumor-specific human CD4+ regulatory T cells and their ligands: implications for immunotherapy. Immunity 2004;20:107-18.
36. Adams GP, Weiner LM. Monoclonal antibody therapy of cancer. Nat Biotechnol 2005;23:1147-57 (review).
37. Gelderman KA, Tomlinson S, Ross GD, Gorter A. Complement function in mAb-mediated cancer immunotherapy. Trends Immunol 2004;25:158-64 (review).
38. Iannello A, Ahmad A. Role of antibody-dependent cell-mediated cytotoxicity in the efficacy of therapeutic anti-cancer monoclonal antibodies. Cancer Metastasis Rev 2005;24:487-99 (review).
39. Orengo AM, Di Carlo E, Comes A, Fabbi M, Piazza T, Cilli M, Musiani P, Ferrini S. Tumor cells engineered with IL-12 and IL-15 genes induce protective antibody responses in nude mice. J Immunol 2003;171:569-75.
40. Croci S, Nicoletti G, Landuzzi L, De Giovanni C, Astolfi A, Marini C, Di Carlo E, Musiani P, Forni G, Nanni P, Lollini PL. Immunoprevention of HER-2/neu transgenic mammary carcinoma through an interleukin 12-engineered allogeneic cell vaccine. Cancer Res 2004;64:4001-9.
41. Ettinger R, Sims GP, Fairhurst AM, Robbins R, da Silva YS, Spolski R, Leonard WJ, Lipsky PE. IL-21 induces differentiation of human naive and memory B cells into antibody-secreting plasma cells. J Immunol 2005;175:7867-79.
42. Strengell M, Matikainen S, Siren J, Lehtonen A, Foster D, Julkunen I, Sareneva T. IL-21 in synergy with IL-15 or IL-18 enhances IFN-γ production in human NK and T cells. J Immunol 2003;170:5464-9.
43. Roda JM, Parihar R, Lehman A, Mani A, Tridandapani S, Carson WE 3rd. Interleukin-21 enhances NK cell activation in response to antibody-coated targets. J Immunol 2006;177:120-9.
44. Ulvestad E, Williams K, Matre R, Nyland H, Olivier A, Antel J. Fc receptors for IgG on cultured human microglia mediate cytotoxicity and phagocytosis of antibody-coated targets. J Neuropathol Exp Neurol 1994;53:27-36.