Intratumoral IL-12 combined with CTLA-4 blockade elicits T cell-mediated glioma rejection

Journal of Experimental Medicine

Volumn 210, Issue 13, 2013, Pages 2803-2811

  vom Berg, Johannes ^a   Vrohlings, Melissa ^a   Haller, Sergio ^c   Haimovici, Aladin ^d   Kulig, Paulina ^a   Sledzinska, Anna ^a   Weller, Michael ^b   Becher, Burkhard ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d UNIVERSITY OF BERN   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMMUNOGLOBULIN G2B; INTERLEUKIN 12; INTERLEUKIN 23; TRANSCRIPTION FACTOR FOXP3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CONTROL; CD4+ T LYMPHOCYTE; CELL LINE; CONTROLLED STUDY; DRUG EFFECT; EFFECTOR CELL; GLIOBLASTOMA; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNOLOGICAL MEMORY; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE; TUMOR MICROENVIRONMENT; TUMOR REJECTION;

ANIMALS; BRAIN NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; CTLA-4 ANTIGEN; GLIOMA; HEK293 CELLS; HUMANS; IMMUNOLOGIC MEMORY; IMMUNOSUPPRESSION; IMMUNOSUPPRESSIVE AGENTS; INTERLEUKIN-12; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOPLASM TRANSPLANTATION; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 84890846323     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20130678     Document Type: Article

References (32)

1. Agarwalla, P., Z. Barnard, P. Fecci, G. Dranoff, and W.T. Curry Jr. 2012. Sequential immunotherapy by vaccination with GM-CSF-expressing glioma cells and CTLA-4 blockade effectively treats established murine intracranial tumors. J. Immunother. 35:385-389. http://dx.doi.org/10.1097/CJI.0b013e3182562d59
2. Atkins, M.B., M.J. Robertson, M. Gordon, M.T. Lotze, M. DeCoste, J.S. DuBois, J. Ritz, A.B. Sandler, H.D. Edington, P.D. Garzone, et al. 1997. Phase I evaluation of intravenous recombinant human interleukin 12 in patients with advanced malignancies. Clin. Cancer Res. 3:409-417.
3. Becker, J.C., R. Houben, D. Schrama, H. Voigt, S. Ugurel, and R.A. Reisfeld. 2010. Mouse models for melanoma: a personal perspective. Exp. Dermatol. 19:157-164. http://dx.doi.org/10.1111/j.1600-0625.2009.00986.x
4. Colombo, M.P., and G. Trinchieri. 2002. Interleukin-12 in anti-tumor immunity and immunotherapy. Cytokine Growth Factor Rev. 13:155-168. http://dx.doi.org/10.1016/S1359-6101(01)00032-6
5. Cui, J., T. Shin, T. Kawano, H. Sato, E. Kondo, I. Toura, Y. Kaneko, H. Koseki, M. Kanno, and M. Taniguchi. 1997. Requirement for Valpha14 NKT cells in IL-12-mediated rejection of tumors. Science. 278:1623-1626. http://dx.doi.org/10.1126/science.278.5343.1623
6. Daga, A., A.M. Orengo, R.M. Gangemi, D. Marubbi, M. Perera, A. Comes, S. Ferrini, and G. Corte. 2007. Glioma immunotherapy by IL-21 genemodified cells or by recombinant IL-21 involves antibody responses. Int. J. Cancer. 121:1756-1763. http://dx.doi.org/10.1002/ijc.22901
7. Eisenring, M., J. vom Berg, G. Kristiansen, E. Saller, and B. Becher. 2010. IL-12 initiates tumor rejection via lymphoid tissue-inducer cells bearing the natural cytotoxicity receptor NKp46. Nat. Immunol. 11:1030-1038. http://dx.doi.org/10.1038/ni.1947
8. Fecci, P.E., H. Ochiai, D.A. Mitchell, P.M. Grossi, A.E. Sweeney, G.E. Archer, T. Cummings, J.P. Allison, D.D. Bigner, and J.H. Sampson. 2007. Systemic CTLA-4 blockade ameliorates glioma-induced changes to the CD4+ T cell compartment without affecting regulatory T-cell function. Clin. Cancer Res. 13:2158-2167. http://dx.doi.org/10.1158/1078-0432.CCR-06-2070
9. Gordy, L.E., J.S. Bezbradica, A.I. Flyak, C.T. Spencer, A. Dunkle, J. Sun, A.K. Stanic, M.R. Boothby, Y.W. He, Z. Zhao, et al. 2011. IL-15 regulates homeostasis and terminal maturation of NKT cells. J. Immunol. 187:6335-6345. http://dx.doi.org/10.4049/jimmunol.1003965
10. Grauer, O.M., S. Nierkens, E. Bennink, L.W. Toonen, L. Boon, P. Wesseling, R.P. Sutmuller, and G.J. Adema. 2007. CD4+FoxP3+ regulatory T cells gradually accumulate in gliomas during tumor growth and efficiently suppress antiglioma immune responses in vivo. Int. J. Cancer. 121:95-105. http://dx.doi.org/10.1002/ijc.22607
11. Grosso, J.F., and M.N. Jure-Kunkel. 2013. CTLA-4 blockade in tumor models: an overview of preclinical and translational research. Cancer Immun. 13:5.
12. Hodi, F.S., S.J. O'Day, D.F. McDermott, R.W. Weber, J.A. Sosman, J.B. Haanen, R. Gonzalez, C. Robert, D. Schadendorf, J.C. Hassel, et al. 2010. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med. 363:711-723. http://dx.doi.org/10.1056/NEJMoa1003466.
13. Hu, J., X. Yuan, M.L. Belladonna, J.M. Ong, S. Wachsmann-Hogiu, D.L. Farkas, K.L. Black, and J.S. Yu. 2006. Induction of potent antitumor immunity by intratumoral injection of interleukin 23-transduced dendritic cells. Cancer Res. 66:8887-8896. http://dx.doi.org/10.1158/0008-5472.CAN-05-3448
14. Jacobs, J.F., A.J. Idema, K.F. Bol, J.A. Grotenhuis, I.J. de Vries, P. Wesseling, and G.J. Adema. 2010. Prognostic significance and mechanism of Treg infiltration in human brain tumors. J. Neuroimmunol. 225:195-199. http://dx.doi.org/10.1016/j.jneuroim.2010.05.020
15. Joki, T., T. Kikuchi, Y. Akasaki, S. Saitoh, T. Abe, and T. Ohno. 1999. Induction of effective antitumor immunity in a mouse brain tumor model using B7-1 (CD80) and intercellular adhesive molecule 1 (ICAM-1; CD54) transfection and recombinant interleukin 12. Int. J. Cancer. 82:714-720. http://dx.doi.org/10.1002/(SICI)1097-0215(19990827)82:5<714:: AID-IJC15>3.0.CO;2-Q
16. Kodama, T., K. Takeda, O. Shimozato, Y. Hayakawa, M. Atsuta, K. Kobayashi, M. Ito, H. Yagita, and K. Okumura. 1999. Perforin-dependent NK cell cytotoxicity is sufficient for anti-metastatic effect of IL-12. Eur. J. Immunol. 29:1390-1396. http://dx.doi.org/10.1002/(SICI)1521-4141(199904) 29:04<1390::AID-IMMU1390>3.0.CO;2-C
17. Langowski, J.L., X. Zhang, L. Wu, J.D. Mattson, T. Chen, K. Smith, B. Basham, T. McClanahan, R.A. Kastelein, and M. Oft. 2006. IL-23 promotes tumour incidence and growth. Nature. 442:461-465. http://dx.doi.org/10.1038/nature04808
18. Leonard, J.P., M.L. Sherman, G.L. Fisher, L.J. Buchanan, G. Larsen, M.B. Atkins, J.A. Sosman, J.P. Dutcher, N.J. Vogelzang, and J.L. Ryan. 1997. Effects of single-dose interleukin-12 exposure on interleukin-12-associated toxicity and interferon-gamma production. Blood. 90:2541-2548.
19. Liu, Y., M. Ehtesham, K. Samoto, C.J. Wheeler, R.C. Thompson, L.P. Villarreal, K.L. Black, and J.S. Yu. 2002. In situ adenoviral interleukin 12 gene transfer confers potent and long-lasting cytotoxic immunity in glioma. Cancer Gene Ther. 9:9-15. http://dx.doi.org/10.1038/sj.cgt.7700399
20. Lo, C.H., S.C. Lee, P.Y. Wu, W.Y. Pan, J. Su, C.W. Cheng, S.R. Roffler, B.L. Chiang, C.N. Lee, C.W. Wu, and M.H. Tao. 2003. Antitumor and antimetastatic activity of IL-23. J. Immunol. 171:600-607.
21. Ngiow, S.F., M.W. Teng, and M.J. Smyth. 2013. A balance of interleukin-12 and-23 in cancer. Trends Immunol. 34:548-555. http://dx.doi.org/10.1016/j.it.2013.07.004
22. Selby, M.J., J.J. Engelhardt, M. Quigley, K.A. Henning, T. Chen, M. Srinivasan, and A.J. Korman. 2013. Anti-CTLA-4 Antibodies of IgG2a Isotype Enhance Antitumor Activity through Reduction of Intratumoral Regulatory T Cells. Cancer Immunol. Res. doi: 10.1158/2326-6066.CIR-13-0013.
23. Simpson, T.R., F. Li, W. Montalvo-Ortiz, M.A. Sepulveda, K. Bergerhoff, F. Arce, C. Roddie, J.Y. Henry, H. Yagita, J.D. Wolchok, et al. 2013. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti-CTLA-4 therapy against melanoma. J. Exp. Med. 210:1695-1710. http://dx.doi.org/10.1084/jem.20130579
24. Szatmári, T., K. Lumniczky, S. Désaknai, S. Trajcevski, E.J. Hídvégi, H. Hamada, and G. Sáfrány. 2006. Detailed characterization of the mouse glioma 261 tumor model for experimental glioblastoma therapy. Cancer Sci. 97:546-553. http://dx.doi.org/10.1111/j.1349-7006.2006.00208.x
25. Uhl, M., S. Aulwurm, J. Wischhusen, M. Weiler, J.Y. Ma, R. Almirez, R. Mangadu, Y.W. Liu, M. Platten, U. Herrlinger, et al. 2004. SD-208, a novel transforming growth factor beta receptor I kinase inhibitor, inhibits growth and invasiveness and enhances immunogenicity of murine and human glioma cells in vitro and in vivo. Cancer Res. 64:7954-7961. http://dx.doi.org/10.1158/0008-5472.CAN-04-1013
26. Vetter, M., M.J. Hofer, E. Roth, H.P. Pircher, and A. Pagenstecher. 2009. Intracerebral interleukin 12 induces glioma rejection in the brain predominantly by CD8+ T cells and independently of interferon-gamma. J. Neuropathol. Exp. Neurol. 68:525-534. http://dx.doi.org/10.1097/NEN.0b013e3181a2afa0
27. Vom Berg, J., S. Prokop, K.R. Miller, J. Obst, R.E. Kälin, I. Lopategui-Cabezas, A. Wegner, F. Mair, C.G. Schipke, O. Peters, et al. 2012. Inhibition of IL-12/IL-23 signaling reduces Alzheimer's disease-like pathology and cognitive decline. Nat. Med. 18:1812-1819. http://dx.doi.org/10.1038/nm.2965
28. Walker, L.S., and D.M. Sansom. 2011. The emerging role of CTLA4 as a cellextrinsic regulator of T cell responses. Nat. Rev. Immunol. 11:852-863. http://dx.doi.org/10.1038/nri3108
29. Weller, M., T. Cloughesy, J.R. Perry, and W. Wick. 2013. Standards of care for treatment of recurrent glioblastoma-are we there yet? Neuro-oncol. 15:4-27. http://dx.doi.org/10.1093/neuonc/nos273
30. Yamanaka, R., S.A. Zullo, J. Ramsey, N. Yajima, N. Tsuchiya, R. Tanaka, M. Blaese, and K.G. Xanthopoulos. 2002. Marked enhancement of antitumor immune responses in mouse brain tumor models by genetically modified dendritic cells producing Semliki Forest virus-mediated interleukin-12. J. Neurosurg. 97:611-618. http://dx.doi.org/10.3171/jns.2002.97.3.0611
31. Yamanaka, R., N. Tsuchiya, N. Yajima, J. Honma, H. Hasegawa, R. Tanaka, J. Ramsey, R.M. Blaese, and K.G. Xanthopoulos. 2003. Induction of an antitumor immunological response by an intratumoral injection of dendritic cells pulsed with genetically engineered Semliki Forest virus to produce interleukin-18 combined with the systemic administration of interleukin-12. J. Neurosurg. 99:746-753. http://dx.doi.org/10.3171/jns.2003.99.4.0746
32. Yuan, X., J. Hu, M.L. Belladonna, K.L. Black, and J.S. Yu. 2006. Interleukin-23-expressing bone marrow-derived neural stem-like cells exhibit antitumor activity against intracranial glioma. Cancer Res. 66:2630-2638. http://dx.doi.org/10.1158/0008-5472.CAN-05-1682