Intratumoral injection of interleukin-12 plasmid DNA, either naked or in complex with cationic lipid, resultsin similar tumor regression in a murine model

Molecular Cancer Therapeutics

Volumn 1, Issue 11, 2002, Pages 949-957

  Shi, Fushun ^a,c   Rakhmilevich, Alexander L ^b   Heise, Chuck P ^a   Oshikawa, Katsuhisa ^a,d   Sondel, Paul M ^b   Yang, Ning Sun ^b,e   Mahvi, David M ^a  

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

^b UNIVERSITY OF WISCONSIN   (United States)

^c Purecyn Inc   (United States)

^d JICHI MEDICAL UNIVERSITY   (Japan)

^e AGRICULTURAL BIOTECHNOLOGY RESEARCH CENTER   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CATION; CD4 ANTIGEN; CD8 ANTIGEN; COMPLEMENTARY DNA; CYTOKINE; DNA; GAMMA INTERFERON; INTERLEUKIN 12;

ANIMAL; ARTICLE; BAGG ALBINO MOUSE; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; GENE THERAPY; GENE TRANSFER; GENE VECTOR; KINETICS; LIPID METABOLISM; LYMPHATIC SYSTEM DISEASE; METABOLISM; MOUSE; NEOPLASM; PHENOTYPE; PLASMID; SPLEEN; SPLENOMEGALY; TIME; TRANSGENE;

ANIMALS; ANTIGENS, CD4; ANTIGENS, CD8; CATIONS; CYTOKINES; DNA; DNA, COMPLEMENTARY; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; INTERFERON TYPE II; INTERLEUKIN-12; KINETICS; LIPID METABOLISM; LYMPHATIC DISEASES; MICE; MICE, INBRED BALB C; NEOPLASMS; PHENOTYPE; PLASMIDS; SPLEEN; SPLENOMEGALY; TIME FACTORS; TRANSGENES; TUMOR CELLS, CULTURED;

EID: 0036726133     PISSN: 15357163     EISSN: 15388514     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Leroy, P., Slos, P., Homann, H., Erbs, P., Poitevin, Y., Regulier, E., Colonna, F. Q., Devauchelle, P., Roth, C., Pavirani, A., and Mehtali, M. Cancer immunotherapy by direct in vivo transfer of immunomodulatory genes. Res. Immunol., 49: 681-684, 1998. (Pubitemid 29487162)
2. Rakhmilevich, A. L., Janssen, K., Turner, J., Culp, J., and Yang, N-S. Cytokine gene therapy of cancer using gene gun technology: superior antitumor activity of interleukin-12. Hum. Gene Ther., 8: 1303-1311, 1997. (Pubitemid 27445411)
3. Cavallo, F., Signorelli, P., Giovarelli, M., Musiani, P., Modesti, A., Brunda, M. J., Colombo, M. P., and Forni, G. Antitumor efficacy of adenocarcinoma cells engineered to produce interleukin 12 (IL-12) or other cytokines compared with exogenous IL-12. J. Natl. Cancer Inst., 89: 1049-1058, 1997. (Pubitemid 27327870)
4. 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. T. Recombinant IL-12 administration induces tumor regression in associated with IFN-γ production. J. Immunol., 153: 1697-1706, 1994. (Pubitemid 24251114)
5. Rakhmilevich, A. L., Turner, J., Ford, M. J., McCabe, D., Sun, W. H., Sondel, P. M., Grota, K., and Yang, N-S. 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, 1996. (Pubitemid 26230298)
6. Saffran, D. C., Horton, H. M., Yankauchas, M. A., Anderson, D., Barnhart, K. M., Abai, A. M., Hobart, P., Manthorpe, M., Norman, J. A., and Parker, S. E. Immunotherapy of established tumors in mice by intratumoral injection of interleukin-2 plasmid DNA: Induction of CD8+ T-cell immunity. Cancer Gene Ther., 5: 321-330, 1998. (Pubitemid 128640019)
7. + T cells in the tumor and blood is associated with efficient local IL-12 gene therapy of cancer. J. Immunol., 162: 609-617, 1999.
8. Lode, H. N., Dreier, T., Xiang, R., Varki, N. M., Kang, A. S., and Reisfeld, R. A. Gene therapy with a single chain interleukin 12 fusion protein induces T cell-dependent protective immunity in a syngeneic model of murine neuroblastoma. Proc. Natl. Acad. Sci. USA, 95: 2475-2480, 1998. (Pubitemid 28145966)
9. Yao, L., Sgadari, C., Furuke, K., Bloom, E. T., Teruya-Feldstein, J., and Tosato, G. Contribution of natural killer cells to inhibition of angiogenesis by interleukin-12. Blood, 93: 1612-1621, 1999. (Pubitemid 29102489)
10. Pham-Nguyen, K. B., Yang, W., Saxena, R., Thung, S. N., Woo, S. L. C., and Chen, S. H. Role of NK and T cells in IL-12-induced anti-tumor response against hepatic colon carcinoma. Int. J. Cancer, 81: 813-819, 1999. (Pubitemid 29214395)
11. Kodama, T., Takeda, K., Shimozato, O., Hayakawa, Y., Atsuta, M., Kobayashi, K., Ito, M., Yagita, H., and Okumura, K. Perforin-dependent NK cell cytotoxicity is sufficient for anti-metastatic effect of IL-12. Eur. J. Immunol., 29: 1390-1396, 1999. (Pubitemid 29164186)
12. Watanabe, M., Fenton, R. G., Wigginton, J. M., McCormick, K. L., Volker, K. F., Fogler, W. E., Roessler, P. G., and Wiltrout, R. H. Intradermal delivery of IL-12 naked DNA induces systemic NK cell activation and Th1 response in vivo that is independent of endogenous IL-12 production. J. Immunol., 163: 1943-1950, 1999. (Pubitemid 29382196)
13. Rakhmilevich, A. L., Janssen, K., Hao, Z., Sondel, P. M., and Yang, N-S. Interleukin 12 gene therapy of a weakly immunogenic mouse mammary carcinoma results in reduction of spontaneous lung metastases via a T cell-independent mechanism. Cancer Gene Ther., 7: 826-838, 2000. (Pubitemid 30437282)
14. Cui, J., Shin, T., Kawano, T., Sato, H., Kondo, E., Toura, I., Kaneko, Y., Koseki, H., Kanno, M., and Taniguchi, M. Requirement for Vα14 NKT cells in IL-12-mediated rejection of tumors. Science (Wash. DC), 278: 1623-1626, 1997. (Pubitemid 27516281)
15. Brunda, M. J., Luistro, L., Hendrzak, J. A., Fountoulakis, M., Garotta, G., and Gately, M. K. Role of interferon-γ in mediating the antitumor efficacy of interleukin-12. J. Immunother. Emphasis Tumor Immunol., 17: 71-75, 1995.
16. Manetti, R., Gerosa, F., Giudizi, M. G., Biagiotti, R., Parronchi, P., Piccinni, M. P., Sampognaro, S., Maggi, E., Romagnani, S., and Trinchieri, G. Interleukin 12 induces stable priming for interferon γ (IFN-γ) producing during differentiation of human T helper (Th) cells and transient IFN-γ production in established Th2 cells clones. J. Exp. Med., 179: 1273-1283, 1994.
17. 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. 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, 1994. (Pubitemid 24040344)
18. Tannenbaum, C. S., Wicker, N., Armstrong, D., Tubbs, R., Finke, J., Bukowski, R. M., and Hamilton, T. A. Cytokine and chemokine expression in tumors of mice receiving systemic therapy with IL-12. J. Immunol., 156: 693-699, 1996. (Pubitemid 26029621)
19. Tannenbaum, C. S., Tubbs, R., Armstrong, D., Finke, J. H., Bukowski, R. M., and Hamilton, T. A. The CXC chemokines IP-10 and Mig are necessary for IL-12-mediated regression of the mouse RENCA tumor. J. Immunol., 161: 927-932, 1998. (Pubitemid 28323558)
20. Voest, E. E., Kenyon, B. M., O'Reilly, M. S., Truitt, G., D'Amato, R. J., and Folkman, J. Inhibition of angiogenesis in vivo by interleukin 12. J. Natl. Cancer Inst., 87: 581-586, 1995.
21. Tahara, H., Zitvogel, L., Storkus, W. J., Robbins, P. D., and Lotze, M. T. Murine models of cancer cytokine gene therapy using interleukin-12. Ann. NY Acad. Sci., 795: 275-283, 1996. (Pubitemid 27029576)
22. Golab, J., and Zagozdzon, R. Antitumor effects of interleukin-12 in pre-clinical and early clinical studies. Int. J. Mol. Med., 3: 537-544, 1999.
23. Rook, A. H., Wood, G. S., Yoo, E. K., Elenitsas, R., Kao, D. M., Sherman, M. L., Witmer, W. K., Rockwell, K. A., Shane, R. B., Lessin, S. R., and Vonderheid, E. C. Interleukin-12 therapy of cutaneous T-cell lymphoma induces lesion regression and cytotoxic T-cell responses. Blood, 94: 902-908, 1999. (Pubitemid 29361820)
24. Marshall, E. Cancer trial of interleukin-12 halted. Science (Wash. DC), 268: 1555, 1995.
25. Car, B. D., Eng, V. M., Lipman, J. M., and Anderson, T. D. The toxicology of interleukin-12: a review. Toxicol. Pathol., 27: 58-63, 1999. (Pubitemid 29075746)
26. Colombo, M. P., Vagliani, M., Spreafico, F., Parenza, M., Chiodoni, C., Melani, C., and Stoppacciaro, A. Amount of interleukin 12 available at the tumor site is critical for tumor regression. Cancer Res., 56: 2531-2534, 1996. (Pubitemid 26170689)
27. Rakhmilevich, A. L., Timmins, J. G., Janssen, K., Pohlmann, E. L., Sheehy, M. J., and Yang, N-S. Gene gun-mediated IL-12 gene therapy induces antitumor effects in the absence of toxicity: a direct comparison with systemic IL-12 protein therapy. J. Immunother., 22: 135-144, 1999. (Pubitemid 29135898)
28. Weber, S. M., Shi, F. S., Heise, C., Warner, T., and Mahvi, D. M. Interleukin-12 gene transfer results in CD8-dependent regression of murine CT26 liver tumors. Ann. Surg. Oncol., 6: 186-194, 1998. (Pubitemid 29114283)
29. Oshikawa, K., Shi, F-S., Rakhmilevich, A. L., Sondel, P. M., Mahvi, D. M., and Yang, N-S. Synergistic inhibition of tumor growth in a murine mammary adenocarcinoma model by combinational gene therapy using IL-12, pro-IL-18, and IL-1β converting enzyme cDNA. Proc. Natl. Acad. Sci. USA, 96: 13351-13356, 1999.
30. Tahara, H., Zitvogel, L., Storkus, W. J., Zeh, H. J., III, McKinney, T. G., Schreiber, R. D., Gubler, U., Robbins, P. D., and Lotze, M. T. Effective eradication of established murine tumors with IL-12 gene therapy using a polycistronic retroviral vector. J. Immunol., 154: 6466-6474, 1995.
31. Zitvogel, L., Tahara, H., Robbins, P. D., Storkus, W. J., Clarke, M. R., Nalesnik, M. A., and Lotze, M. T. Cancer immunotherapy of established tumors with IL-12. Effective delivery by genetically engineered fibroblasts. J. Immunol., 155: 1393-1403, 1995.
32. Miller, D. G., Adam, M. A., and Miller, A. D. Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection. Mol. Cell. Biol., 10: 4239-4242, 1990.
33. Hurley, M. J., Bradford, H. F., O'Hare, K., Stern, G. M., and Uchida, K. Neural toxicity of retroviruses. Neurosci. Lett., 220: 66-68, 1996. (Pubitemid 26423052)
34. Bramson, J. L., Hitt, M., Addison, C. L., Muller, W. J., Gauldie, J., and Graham, F. L. Direct intratumoral injection of an adenovirus expressing interleukin-12 induces regression and long-lasting immunity that is associated with highly localized expression of interleukin-12. Hum. Gene Ther., 7: 1995-2002, 1996. (Pubitemid 26390239)
35. Nomura, T., Nakajima, S., Kawabata, K., Yamashita, F., Takakura, Y., and Hashida, M. Intratumoral pharmacokinetics and in vivo gene expression of naked plasmid DNA and its cationic liposome complexes after direct gene transfer. Cancer Res., 57: 2681-2686, 1997. (Pubitemid 27283780)
36. Addison, C. L., Bramso, J. L., Hitt, M. M., Muller, W. J., Gauldie, J., and Graham, F. L. Intratumoral coinjection of adenoviral vectors expression IL-2 and IL-12 results in enhanced frequency of regression of injected and untreated distal tumors. Gene. Ther., 5: 1400-1409, 1998. (Pubitemid 28482668)
37. Lehrman, S. Virus treatment questioned after gene therapy death. Nature (Lond.), 40: 517-518, 1999.
38. Missol, E., Sochanik, A., and Szala, S. Introduction of murine IL-4 gene into B16 (F10) melanoma tumors by direct gene transfer with DNA-liposome complexes. Cancer Lett., 97: 189-193, 1995. (Pubitemid 3005767)
39. Parker, S. E., Ducharme, S., Norman, J., and Wheeler, C. J. Tissue distribution of the cytofectin component of a plasmid-DNA/cationic lipid complex following intravenous administration in mice. Hum. Gene Ther., 8: 393-401, 1997. (Pubitemid 27140542)
40. Stephan, D. J., Yang, Z. Y., San, H., Simari, R. D., Wheeler, C. J., Felgner, P. L., Gordon, D., Nabel, G. J., and Nabel, E. G. A new cationic liposome DNA complex enhances the efficiency of arterial gene transfer in vivo. Hum. Gene Ther., 7: 1803-1812, 1996. (Pubitemid 26364589)
41. Blezinger, P., Freimark, B. D., Matar, M., Wilson, E., Singhal, A., Jeffrey, W. M., Nordstrom, J. L., and Pericle, F. Intratracheal administration of interleukin 12 plasmid-cationic lipid complexes inhibits murine lung metastases. Hum. Gene Ther., 10: 723-731, 1999. (Pubitemid 29168157)
42. Horton, H. M., Anderson, D., Hernandez, P., Barnhart, K. M., Norman, J. A., and Parker, S. E. A gene therapy for cancer using intramuscular injection of plasmid DNA encoding interferon α. Proc. Natl. Acad. Sci. USA, 96: 1553-1558, 1999. (Pubitemid 29098489)
43. Mendiratta, S. K., Quezada, A., Matar, M., Wang, J., Hebel, H. L., Long, S., Nordstrom, J. L., and Pericle, F. Intratumoral delivery of IL-12 gene by polyvinyl polymeric vector system to murine renal and colon carcinoma results in potent antitumor immunity. Gene Ther., 6: 833-839, 1999. (Pubitemid 29243657)
44. Chamberlain, R. S., Carroll, M. W., Bronte, V., Hwu, P., Warren, S., Yang, J. C., Nishimura, M., Moss, B., Rosenberg, S. A., and Restifo, N. P. Costimulation enhances the active immunotherapy effect of recombinant anticancer vaccines. Cancer Res., 56: 2832-2836, 1996. (Pubitemid 26175744)
45. Mahvi, D. M., Burkholder, J. K., Turner, J., Culp, J., Malter, J. S., Sondel, P. M., and Yang, N-S. Particle-mediated gene transfer of granulocyte-macrophage colony-stimulating factor cDNA to tumor cells: implications for a clinically relevant tumor vaccine. Hum. Gene Ther., 7: 1535-1543, 1996. (Pubitemid 26302208)
46. Schultz, J., Pavlovic, J., Strack, B., Nawrath, M., and Moelling, K. Long-lasting anti-metastatic efficiency of interleukin 12-encoding plasmid DNA. Hum. Gene Ther., 10: 407-417, 1999. (Pubitemid 29097319)
47. Popovic, D., El-Shami, K. M., Vadai, E., Feldman, M., Tzehoval, E., and Eisenbach, L. Antimetastatic vaccination against Lewis lung carcinoma with autologous tumor cells modified to express murine interleukin 12. Clin. Exp. Metastasis, 7: 623-632, 1998. (Pubitemid 29044585)
48. Puisieux, I., Odin, L., Poujol, D., Moingeon, P., Tartaglia, J., and Cox, W. Canarypox virus-mediated interleukin 12 gene transfer into murine mammary adenocarcinoma induces tumor suppression and long-term antitumoral immunity. Hum. Gene Ther., 9: 2481-2492, 1998. (Pubitemid 29004621)
49. Yahata, T., Watanabe, K., Ohta, A., Ohmi, Y., Sato, N., Santa, K., Abe, N., Iwakabe, K., Kaneko, S., Suzuki, N., Habu, S., Yasuda, S., and Nishimura, T. Accumulation of IL-12-activated antitumor effector cells into lymph nodes of tumor-bearing mice. Immunol. Lett., 61: 127-133, 1998. (Pubitemid 28260987)
50. Tare, N. S., Bowen, S., Warrier, R. R., Carvajal, D. M., Benjamin, W. R., Riley, J. H., Anderson, T. D., and Gately, M. K. Administration of recombinant interleukin-12 to mice suppresses hematopoiesis in the bone marrow but enhances hematopoiesis in the spleen. J. Interferon Cytokine Res., 15: 377-383, 1995.