Cytokine gene therapy of cancer using gene gun technology: Superior antitumor activity of interleukin-12

Human Gene Therapy

Volumn 8, Issue 11, 1997, Pages 1303-1311

  Rakhmilevich, Alexander L ^a,d,e   Janssen, Karen ^b,d   Turner, Joel ^c,d   Culp, Jerilyn ^d   Yang, Ning Sun ^d  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b Agracetus   (United States)

^c H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^d Geniva   (United States)

^e UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; COMPLEMENTARY DNA; CYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOLISTIC TRANSFORMATION; FEMALE; GENE THERAPY; MOUSE; NONHUMAN; T LYMPHOCYTE; TUMOR IMMUNITY; TUMOR REGRESSION;

ANIMALIA; MURINAE;

EID: 0030879639     PISSN: 10430342     EISSN: None     Source Type: Journal    
DOI: 10.1089/hum.1997.8.11-1303     Document Type: Article

References (47)

1. AWWAD, M., and NORTH, R.J. (1988). Cyclophosphamide (Cy)-facilitated adoptive immunotherapy of a Cy-resistant tumour. Evidence that Cy permits the expression of adoptive T-cell mediated immunity by removing suppressor T cells rather than by reducing tumour burden. Immunology 65, 87-92.
2. BANNERJI, R., ARROYO, C.D., CORDON-CARDO, C., and GILBOA, E. (1994). The role of IL-2 secreted from genetically modified tumor cells in the establishment of antitumor immunity. J. Immunol. 152, 2324-2332.
3. BRUNDA, M.J., LUISTRO, L., WARRIER, R.R., WRIGHT, R.B., HUBBARD, B.R., MURPHY, M., WOLF, S.F., and GATELY, M.K. (1993). Antitumor and antimetastatic activity of interleukin 12 against murine tumors. J. Exp. Med. 178, 1223-1230.
4. BRUNDA, M.J., LUISTRO, J., HENDRZAK, J.A., FOUNTOULAKIS, M., GAROTTA, G., and GATELY, M.K. (1995). Role of interferon-γ in mediating the antitumor efficacy of interleukin-12. J. Immunother. 17, 71-77.
5. COHEN, J. (1995). IL-12 deaths: Explanation and a puzzle. Science 270, 908.
6. COLOMBO, M.P., and FORNI, G. (1994). Cytokine gene transfer in tumor inhibition and tumor therapy: Where are we now? Immunol. Today 15, 48-51.
7. COLOMBO, M.P., VAGLIANI, M., SPREAFICO, F., PARENZA, M., CHIODONI, C., MELANI, C., and STOPPACCIARO, A. (1996). Amount of interleukin 12 available at the tumor site is critical for tumor regression. Cancer Res 56, 2531-2534.
8. COUGHLIN, C.M., WYSOCKA, M., KURZAWA, H.L., LEE, W.M., TRINCHIERI, G., and ECK, S.L. (1995). B7-1 and interleukin 12 synergistically induce effective antitumor immunity. Cancer Res 55, 4980-4987.
9. DRANOFF, G., JAFFEE, E., LAZENBY, A., GOLUMBEK, P., LEVITSKY, H., BROSE, K., JACKSON, V., HAMADA, H., PARDOLL, D., and MULLIGAN, R.C. (1993). Vaccination with irradiated tumor cells engineered to secrete murine granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc. Natl. Acad. Sci. USA 90, 3539-3543.
10. + effector T cells temporarily causes the destruction of already disseminated tumor cells. J. Immunol. 136, 1510-1515.
11. GANSBACHER, B., ZIER, K., DANIELS, B., CRONIN, K., BANNERJI, R., and GILBOA, E. (1990). Interleukin 2 gene transfer into tumor cells abrogates tumorigenicity and induces protective immunity. J. Exp. Med. 172, 1217-1224.
12. GATELY, M.K., WARRIER, R.R., HONASOGE, S., CARVAJAL, D.M., FAHERTY, D.A., CONNAUGHTON, S.E., ANDERSON, T.D., SARMIENTO, U., HUBBARD, B.R., and MURPHY, M. (1994). Administration of recombinant IL-12 to normal mice enhances cytolytic lymphocyte activity and induces production of IFN-γ in vivo. Int. Immunol. 6, 157-167.
13. GOLUMBEK, P.T., LAZENBY, A.J., LEVITSKY, H.I., JAFFEE, L.M., KARASUYAMA, H., BAKER, M., and PARDOLL, D.M. (1991). Treatment of established renal cancer by tumor cells engineered to secrete interleukin-4. Science 254, 713-716.
14. GREENBERG, P.D. (1991). Adoptive T cell therapy of tumors: mechanisms operative in the recognition and elimination of tumor cells, Adv. Immunol. 49, 281-355.
15. IOANNIDES, C.G., and WHITESIDE, T.L. (1993). T cell recognition of human tumors: implications for molecular immunotherapy of cancer. Clin. Immunol. Immunopath. 66, 91-106.
16. JENKS, S. (1996). After initial setback, IL-12 regaining popularity. J. Natl. Cancer Inst. 88, 576-577.
17. KOSHITA, Y., LU, Y., FUJII, S., NEDA, H., MATSUYAMA, T., SATOH, Y., ITOH, Y., TAKAHASHI, M., KATO, J., SAKAMAKI, S., WATANABE, N., KOHGO, Y., and NIITSU, Y. (1995). Efficacy of the TNF-α gene-transduced tumor cells in treatment of established in vivo tumor. Int. J. Cancer 63, 130-135.
18. MAHVI, D.M., BURKHOLDER, J.K., TURNER, J., CULP, J., MALTER, J.S., SONDEL, P.M., and YANG, N.S. (1996). Particle-mediated gene transfer of GM-CSF cDNA to tumor cells: Implications for a clinically relevant tumor vaccine. Hum. Gene Ther. 7, 1535-1543.
19. MARSHALL, E. (1995). Cancer trial of interleukin-12 halted. Science 268, 1555.
20. MEKO, J.B., YIM, J.H., TSUNG, K., and NORTON, J.A. (1995). High cytokine production and effective antitumor activity of a recombinant vaccinia virus encoding murine interleukin 12. Cancer Res. 55, 4765-4770.
21. MILLER, A.R., McBRIDE, W.H., HUNT, K., and ECONOMOU, J.S. (1994). Cytokine-mediated gene therapy for cancer. Ann. Surg. Oncol. 1, 436-450.
22. MU, J., ZOU, J.P., YAMAMOTO, N., TSUTSUI, T., TAI, X.G., KOBAYASHI, M., HERRMANN, S., FUJIWARA, H., and HAMAOKA, T. (1995). Administration of recombinant interleukin 12 prevents outgrowth of tumor cells metastasizing spontaneously to lung and lymph nodes. Cancer Res 55, 4404-4408.
23. MULLEN, C.A., COALE, M.M., LEVY, A.T., STETLER-STEVENSON, W.G., LIOTTA, L.A., BRANDT, S., and BLAESE, R.M. (1992). Fibrosarcoma cells transduced with the IL-6 gene exhibit reduced turmorigenicity, increased immunogenicity, and decreased metastatic potential. Cancer Res 52, 6020-6024.
24. NASTALA, C.L., EDINGTON, H.D., McKINNEY, T.G., TAHARA, H., NALESNIK, M.A., BRUNDA, M.J., GATELY, M.K., WOLF, S.F., SCHREIBER, R.D., STORKUS, W.J., and LOTZE, M. (1994). Recombinant IL-12 administration induces tumor regression in association with IFN-γ production. J. Immunol. 153, 1697-1706.
25. National Institutes of Health. (1985). Guide for the Care and Use of Laboratory Animals, publication 86-23. (National Institutes of Health, Bethesda, MD).
26. + T cells. Proc. Natl. Acad. Sci. USA 91, 3171-3175.
27. NOGUCHI, Y., RICHARDS, E.C., CHEN, Y.-T., and OLD, L.J. (1995). Influence of interleukin 12 on p53 peptide vaccination against established Meth A sarcoma. Proc. Natl. Acad. Sci. USA 92, 2219-2223.
28. NORTH, R.J., and BURSUKER, I. (1984). T cell-mediated suppression of the concomitant antitumor immune response as an example of transplantation tolerance. Transplantation Proc. 16, 463-469.
29. + effector T cells during progressive growth of the P815 mastocytoma. Immunology 54, 47-56.
30. ORANGE, J.S., SALAZAR-MATHER, T.P., OPAL, S.M., SPENCER, R.L., MILLER, A.H., McEWEN, B.S., and BIRON, C.A. (1995). Mechanism of interleukin 12-mediated toxicities during experimental viral infections: role of tumor necrosis factor and glucocorticoids. J. Exp. Med. 181, 901-914.
31. PAPPO, I., TAHARA, H., ROBBINS, P.D., GATELY, M.K., WOLF, S.F., BARNEA, A., and LOTZE, M.T. (1995). Administration of systemic or local interleukin-2 enhances the anti-tumor effects of interleukin-12 gene therapy. J. Surgical Res. 58, 218-226.
32. PORGADOR, A., TZEHOVAL, E., KATZ, A., VADAI, E., REVEL, M., FELDMAN, M., and EISENBACH, L. (1992). Interleukin 6 gene transfection into Lewis Lung carcinoma tumor cells suppresses the malignant phenotype and confers immunotherapeutic competence against parental metastatic cells. Cancer Res. 52, 3679-3686.
33. RAKHMILEVICH, A.L. (1994). Failure of anti-T cell monoclonal antibodies to prevent acute tumor allograft rejection is associated with their inability to deplete or inactive T cells at the site of rejection. Transplantation 58, 72-80.
34. RAKHMILEVICH, A.L., TURNER, J., FORD, M.J., McCABE, D., SUN, W.H., SONDEL, P.M., GROTA, K., and YANG, N.S. (1996). Gene gun-mediated skin transfection with interleukin 12 gene results in regression of established primary and metastatic murine tumors. Proc. Natl. Acad. Sci. USA 93, 6291-6296.
35. ROSENBERG, S.A., MULE, J.J., SPIESS, P.J., REICHERT, C.M., and SCHWARZ, S.L. (1985). Regression of established pulmonary metastases and subcutaneous tumor mediated by the systemic administration of high-dose recombinant interleukin 2. J. Exp. Med. 161, 1169-1188.
36. ROSENBERG, S.A., LOTZE, M.T., MUUL, L.M., CHANG, A.E., AVIS, F.P., LEITMON, S., LINEHAN, W.M., ROBERTSON, C.N., LEE, R.E., ROBIN, J.T., et al. (1987). A progress report on the treatment of 157 patients with advanced cancer using lymphokine-activated killer cells and interleukin-2 or high dose interleukin-2 alone. N. Engl. J. Med. 316, 889-897.
37. STERN, L.L., TARBY, C.M., TAMBORINI, B., and TRUITT, G.A. (1994). Preclinical development of IL-12 as an anticancer drug: comparison to IL-2. Proc. Am. Assoc. Cancer Res. 35, 520.
38. SUN, W.H., BURKHOLDER, J.K., SUN, J., CULP, J., TURNER, J., LU, X.G., PUGH, T.D., ERSHLER, W.G., and YANG, N.-S. (1995). In vivo cytokine gene transfer by gene gun reduces tumor growth in mice. Proc. Natl. Acad. Sci. USA 92, 2889-2893.
39. TAHARA, H., ZEH, H.J., STORKUS, W.J., PAPPO, I., WATKINS, S.C., GUBLER, U., WOLF, S.F., ROBBINS, P.D., and LOTZE, M.T. (1994). Fibroblasts genetically engineered to secrete interleukin 12 can suppress tumor growth and induce antitumor immunity to a murine melanoma in vivo. Cancer Res. 54, 182-189.
40. TAHARA, H., ZITVOGEL, L., STORKUS, W.J., ZEH, H.J., McKINNEY, T.G., SCHREIBER, R.D., GUBLER, U., ROBBINS, P.D., and LOTZE, M.T. (1995). Effective eradication of established murine tumors with IL-12 gene therapy using a polycistronic retroviral vector. J. Immunol. 154, 6466-6474.
41. TEPPER, R.I., PATTENGALE, P.K., and LEDER, P. (1989). Murine interleukin-4 displays potent anti-tumor activity in vivo. Cell 57, 503-512.
42. WATANABE, Y., KURIBAYASHI, K., MIYATAKE, S., NISHIHARA, K., NAKAYAMA, E., TANIYAMA, T., and SAKATA, T. (1989). Exogenous expression of mouse interferon γcDNA in mouse neuroblastoma C1300 cells results in reduced tumorigenicity by augmented anti-tumor immunity. Proc. Natl. Acad. Sci. USA 86, 9456-9460.
43. YANG, N.S., and ZIEGLEHOFFER, P.R. (1994). The particle bombardment system for gene transfer. In Particle Bombardment Technology for Gene Transfer. N.S. Yang and P. Christou, eds. (Oxford University Press, New York) pp. 117-142.
44. YANG, N.S., BURKHOLDER, J., ROBERTS, B., MARTINELL, B., and McCABE, D. (1990). In vivo and in vitro gene transfer to mammalian somatic cells by particle bombardment. Proc. Natl. Acad. Sci. USA 87, 9568-9572.
45. YU, J.S., WEI, M.X., CHIOCCA, E.A., MARTUZA, R.L., and TEPPER, R.I. (1993). Treatment of glioma by engineered interleukin 4-secreting cells. Cancer Res 53, 3125-3128.
46. ZITVOGEL, L., TAHARA, H., ROBBINS, P.D., STORKUS, W.J., CLARKE, M.R., NALESNIK, M.A., and LOTZE, M.T. (1995). Cancer immunotherapy of established tumors with IL-12: Effective delivery of genetically engineered fibroblasts. J. Immunol. 155, 1393-1403.
47. ZOU, J.-P., YAMAMOTO, N., FUJII, T., TAKENAKA, H., KOBAYASHI, M., HERRMANN, S.H., WOLF, S.F., FUJIWARA, H., and HAMAOKA, T. (1995). Systemic administration of rIL-12 induces complete tumor regression and protective immunity: response is correlated with a striking reversal of suppressed IFN-γ production by anti-tumor T cells. Int. Immunol. 7, 1135-1145.