Antitumor and antimetastatic activity of interleukin 12 against murine tumors

doi:10.1084/jem.178.4.1223

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Antitumor and antimetastatic activity of interleukin 12 against murine tumors

MJ Brunda, L Luistro, RR Warrier, RB Wright, BR Hubbard, M Murphy, SF Wolf and MK Gately
Department of Oncology, Hoffmann-La Roche Inc., Nutley, New Jersey 07110.

It has recently been demonstrated that in vivo administration of murine interleukin 12 (IL-12) to mice results in augmentation of cytotoxic natural killer (NK)/lymphocyte-activated killer cell activity, enhancement of cytolytic T cell generation, and induction of interferon gamma secretion. In this study, the in vivo activity of murine IL-12 against a number of murine tumors has been evaluated. Experimental pulmonary metastases or subcutaneous growth of the B16F10 melanoma were markedly reduced in mice treated intraperitoneally with IL-12, resulting in an increase in survival time. The therapeutic effectiveness of IL-12 was dose dependent and treatment of subcutaneous tumors could be initiated up to 14 d after injection of tumor cells. Likewise, established experimental hepatic metastases and established subcutaneous M5076 reticulum cell sarcoma and Renca renal cell adenocarcinoma tumors were effectively treated by IL-12 at doses which resulted in no gross toxicity. Local peritumoral injection of IL-12 into established subcutaneous Renca tumors resulted in regression and complete disappearance of these tumors. IL-12 was as effective in NK cell-deficient beige mice or in mice depleted of NK cell activity by treatment with antiasialo GM1, suggesting that NK cells are not the primary cell type mediating the antitumor effects of this cytokine. However, the efficacy of IL-12 was greatly reduced in nude mice suggesting the involvement of T cells. Furthermore, depletion of CD8+ but not CD4+ T cells significantly reduced the efficacy of IL-12. These results demonstrate that IL-12 has potent in vivo antitumor and antimetastatic effects against murine tumors and demonstrate as well the critical role of CD8+ T cells in mediating the antitumor effects against subcutaneous tumors.
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Ariel, A., Novick, D., Rubinstein, M., Dinarello, C. A., Lider, O., Hershkoviz, R. (2002). IL-12 and IL-18 induce MAP kinase-dependent adhesion of T cells to extracellular matrix components. J. Leukoc. Biol. 72: 192-198 [Abstract] [Full Text]
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Peter, K., Brunda, M. J., Corradin, G. (2002). IL-12 Administration Leads to a Transient Depletion of T Cells, B Cells, and APCs and Concomitant Abrogation of the HLA-A2.1-Restricted CTL Response in Transgenic Mice. J. Immunol. 169: 63-67 [Abstract] [Full Text]
Li, S., Zhang, X., Xia, X. (2002). Regression of Tumor Growth and Induction of Long-Term Antitumor Memory by Interleukin 12 Electro-Gene Therapy. JNCI J Natl Cancer Inst 94: 762-768 [Abstract] [Full Text]
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Lee, J. C., Kim, D. C., Gee, M. S., Saunders, H. M., Sehgal, C. M., Feldman, M. D., Ross, S. R., Lee, W. M. F. (2002). Interleukin-12 Inhibits Angiogenesis and Growth of Transplanted but not in Situ Mouse Mammary Tumor Virus-induced Mammary Carcinomas. Cancer Res. 62: 747-755 [Abstract] [Full Text]
Schmitz, V, Qian, C, Ruiz, J, Sangro, B, Melero, I, Mazzolini, G, Narvaiza, I, Prieto, J (2002). Gene therapy for liver diseases: recent strategies for treatment of viral hepatitis and liver malignancies. Gut 50: 130-135 [Abstract] [Full Text]
Gruber, T. A., Skelton, D. C., Kohn, D. B. (2002). Requirement for NK Cells in CD40 Ligand-Mediated Rejection of Philadelphia Chromosome-Positive Acute Lymphoblastic Leukemia Cells. J. Immunol. 168: 73-80 [Abstract] [Full Text]
Ansell, S. M., Witzig, T. E., Kurtin, P. J., Sloan, J. A., Jelinek, D. F., Howell, K. G., Markovic, S. N., Habermann, T. M., Klee, G. G., Atherton, P. J., Erlichman, C. (2002). Phase 1 study of interleukin-12 in combination with rituximab in patients with B-cell non-Hodgkin lymphoma. Blood 99: 67-74 [Abstract] [Full Text]
Matsumoto, M., Itakura, A., Tanaka, A., Fujisawa, C., Matsuda, H. (2001). Inability of IL-12 to Down-Regulate IgE Synthesis Due to Defective Production of IFN-{gamma} in Atopic NC/Nga Mice. J. Immunol. 167: 5955-5962 [Abstract] [Full Text]
Buckley, C., Newsom-Davis, J., Willcox, N., Vincent, A. (2001). Do titin and cytokine antibodies in MG patients predict thymoma or thymoma recurrence?. Neurology 57: 1579-1582 [Abstract] [Full Text]
Li, D., Shugert, E., Guo, M., Bishop, J. S., O'Malley, B. W. Jr (2001). Combination Nonviral Interleukin 2 and Interleukin 12 Gene Therapy for Head and Neck Squamous Cell Carcinoma. Arch Otolaryngol Head Neck Surg 127: 1319-1324 [Abstract] [Full Text]
Lohr, F., Huang, Q., Hu, K., Dewhirst, M. W., Li, C.-Y. (2001). Systemic Vector Leakage and Transgene Expression by Intratumorally Injected Recombinant Adenovirus Vectors. Clin. Cancer Res. 7: 3625-3628 [Abstract] [Full Text]
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Sharma, S., Stolina, M., Zhu, L., Lin, Y., Batra, R., Huang, M., Strieter, R., Dubinett, S. M. (2001). Secondary Lymphoid Organ Chemokine Reduces Pulmonary Tumor Burden in Spontaneous Murine Bronchoalveolar Cell Carcinoma. Cancer Res. 61: 6406-6412 [Abstract] [Full Text]
Karnbach, C., Daws, M. R., Niemi, E. C., Nakamura, M. C. (2001). Immune Rejection of a Large Sarcoma Following Cyclophosphamide and IL-12 Treatment Requires Both NK and NK T Cells and Is Associated with the Induction of a Novel NK T Cell Population. J. Immunol. 167: 2569-2576 [Abstract] [Full Text]
Ahlers, J. D., Belyakov, I. M., Matsui, S., Berzofsky, J. A. (2001). Mechanisms of cytokine synergy essential for vaccine protection against viral challenge. Int Immunol 13: 897-908 [Abstract] [Full Text]
Khan, W. I., Blennerhassett, P. A., Deng, Y., Gauldie, J., Vallance, B. A., Collins, S. M. (2001). IL-12 gene transfer alters gut physiology and host immunity in nematode-infected mice. Am. J. Physiol. Gastrointest. Liver Physiol. 281: G102-G110 [Abstract] [Full Text]
Golgher, D., Korangy, F., Gao, B., Gorski, K., Jaffee, E., Edidin, M., Pardoll, D. M., Elliott, T. (2001). An Immunodominant MHC Class II-Restricted Tumor Antigen Is Conformation Dependent and Binds to the Endoplasmic Reticulum Chaperone, Calreticulin. J. Immunol. 167: 147-155 [Abstract] [Full Text]
Wang, K. S., Zorn, E., Ritz, J. (2001). Specific down-regulation of interleukin-12 signaling through induction of phospho-STAT4 protein degradation. Blood 97: 3860-3866 [Abstract] [Full Text]
Pertl, U., Luster, A. D., Varki, N. M., Homann, D., Gaedicke, G., Reisfeld, R. A., Lode, H. N. (2001). IFN-{{gamma}}-Inducible Protein-10 Is Essential for the Generation of a Protective Tumor-Specific CD8 T Cell Response Induced by Single-Chain IL-12 Gene Therapy. J. Immunol. 166: 6944-6951 [Abstract] [Full Text]
Kimura, Y., Okuda, H. (2001). Resveratrol Isolated from Polygonum cuspidatum Root Prevents Tumor Growth and Metastasis to Lung and Tumor-Induced Neovascularization in Lewis Lung Carcinoma-Bearing Mice. J. Nutr. 131: 1844-1849 [Abstract] [Full Text]
Lafleur, E. A., Jia, S.-F., Worth, L. L., Zhou, Z., Owen-Schaub, L. B., Kleinerman, E. S. (2001). Interleukin (IL)-12 and IL-12 Gene Transfer Up-Regulate Fas Expression in Human Osteosarcoma and Breast Cancer Cells. Cancer Res. 61: 4066-4071 [Abstract] [Full Text]
Li, W., Lu, L., Wang, Z., Wang, L., Fung, J. J., Thomson, A. W., Qian, S. (2001). IL-12 Antagonism Enhances Apoptotic Death of T Cells Within Hepatic Allografts from Flt3 Ligand-Treated Donors and Promotes Graft Acceptance. J. Immunol. 166: 5619-5628 [Abstract] [Full Text]
Cifaldi, L., Quaglino, E., Di Carlo, E., Musiani, P., Spadaro, M., Lollini, P. L., Wolf, S., Boggio, K., Forni, G., Cavallo, F. (2001). A Light, Nontoxic Interleukin 12 Protocol Inhibits HER-2/neu Mammary Carcinogenesis in BALB/c Transgenic Mice with Established Hyperplasia. Cancer Res. 61: 2809-2812 [Abstract] [Full Text]
Lohr, F., Lo, D. Y., Zaharoff, D. A., Hu, K., Zhang, X., Li, Y., Zhao, Y., Dewhirst, M. W., Yuan, F., Li, C.-Y. (2001). Effective Tumor Therapy with Plasmid-encoded Cytokines Combined with in Vivo Electroporation. Cancer Res. 61: 3281-3284 [Abstract] [Full Text]