In vivo tumor transfection with superantigen plus cytokine genes induces tumor regression and prolongs survival in dogs with malignant melanoma

Journal of Clinical Investigation

Volumn 101, Issue 11, 1998, Pages 2406-2414

  Dow, Steven W ^a   Elmslie, Robyn E ^c   Willson, Andrew P ^a   Roche, Lisa ^d,e   Gorman, Cori ^d,f   Potter, Terry A ^a,b  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c Veterinary Referral Center of Colorado   (United States)

^d Megabios Corporation   (United States)

^e GenPharm International   (United States)

^f DNA Bridges Inc   (United States)

Author keywords

Granulocyte macrophage colony stimulating factor; Interleukin 2; Lymphocytes; Melanoma; Staphylococcal enterotoxin B

Indexed keywords

CYTOKINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 2; STAPHYLOCOCCUS ENTEROTOXIN B; SUPERANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER REGRESSION; CANCER SURVIVAL; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DOG; GENE THERAPY; GENETIC TRANSFECTION; IMMUNOSTIMULATION; LYMPHOCYTE PROLIFERATION; LYMPHOCYTIC INFILTRATION; MELANOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TUMOR IMMUNITY; TUMOR REGRESSION;

EID: 0032103188     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI510     Document Type: Article

References (44)

1. Pardoll, D.M. 1993. New strategies for enhancing the immunogenicity of tumors. Curr. Opin. Immunol. 5:719-725.
2. Fearon, E.R., D.M. Pardoll, T. Itaya, P. Golumbek, H.I. Levitsky, J.W. Simons, H. Karasuyama, B. Vogelstein, and P. Frost. 1990. Interleukin-2 production by tumor cells bypasses T helper function in the generation of an anti-tumor response. Cell. 60:397-403.
3. Gansbacher, B., K. Zier, B. Daniels, K. Cronin, R. Bannerji, and E. Gilboa. 1990. Interleukin-2 gene transfer into tumor cells abrogates tumorigenicity and induces protective immunity. J. Exp. Med. 172:1217-1224.
4. Golumbek, P.T., A.J. Lazenby, H.I. Levitsky, L.M. Jaffee, H. Karasuyama, M. Baker, and D.M. Pardoll. 1991. Treatment of established renal cell cancer by tumor cells engineered to secrete interleukin-4. Science. 254:713-716.
5. Dranoff, G., E. Jaffee, A. Lazenby, P. Golumbek, H. Levitsky, K. Brose, V. Jackson, H. Hamada, D. Pardoll, and R. Mulligan. 1993. Vaccination with irradiated tumor cells engineered to secrete granulocyte-macrophage colony-stimulating factor stimulates potent, specific, and long-lasting anti-tumor immunity. Proc. Natl. Acad. Sci. USA. 90:3539-3543.
6. Lotze, M.T. 1996. Cytokine gene therapy of cancer. Cancer J. 2:63-72.
7. Townsend, H.E., and J.P. Allison. 1993. Tumor rejection after direct costimulation of CD8+ T cells by B7-transfected melanoma cells. Science. 259: 368-370.
8. Li, Y., P. McGowan, I. Hellstrom, K.E. Hellstrom, and L. Chen. 1994. Costimulation of tumor-reactive CD4+ and CD8+ T lymphocytes by B7, a natural ligand for CD28, can be used to treat established mouse melanoma. J. Immunol. 153:421-427.
9. Baskar, B.S., L. Glimcher, N. Nabavi, R.T. Jones, and S. Rosenberg-Ostrand. 1995. Major histocompatibility complex class II + B7-1 + tumor cells are potent vaccines for stimulating tumor rejection in tumor-hearing mice. J. Exp. Med. 181:619-629.
10. Eynde, B., and V.G. Brichard. 1995. New tumor antigens recognized by T cells. Curr. Opin. Immunol. 7:674-681.
11. Van der Bruggen, P., C. Travcrsari, P. Chomez, C. Lurquin, E. DePlaen. B. Van den Eynde, A. Knuth, and T. Boon. 1991. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science. 254: 1643-1647.
12. Mandelboim, O., E. Vadam, M. Fridkin, A. Katz-Hillel, M. Feldman, G. Berke, and L. Eisenbach. 1995. Regression of established murine carcinoma metastases following vaccination with tumour-associated antigen peptides. Nat. Med. 1:1179-1183.
13. Young, J.W., and K. Inaba. 1996. Dendritic cells as adjuvants for class I major histocompatihility complex-restricted antitumor immunity. J. Exp. Med. 183:7-11.
14. Zitvogel, L., J.L. Mayordomo, T. Tjandrawan, A.B. DeLeo, M.R. Clarke, M.T. Lotze, and W.J. Storkus. 1996. Therapy of murine tumors with tumor peptide-pulsed dendritic cells: dependence on T cells, B7 costimulation, and T helper cell 1-associated cytokines. J. Exp. Med. 183:87-97.
15. Boczkowski, D., S.K. Nair, D. Snyder, and E. Gilboa, 1996. Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J. Exp. Med. 184:465-472.
16. Plautz, G.E., Z.Y. Yang, B.Y. Wu, X. Gao, L. Huang, and G.J. Nabel. 1993. Immunotherapy of malignancy by in vivo gene transfer into tumors. Proc. Natl. Acad. Sci. USA. 90:4645-4649.
17. Nabel, G.J., E.G. Nabel, Z.Y. Yang, B.A. Fox, G.E. Plautz, X. Gao, L. Huang, S. Shu, D. Gordon, and A.E. Chang. 1993. Direct gene transfer with DNA-liposome complexes in melanoma: expression, biologic activity, and lack of toxicity in humans. Proc. Natl. Acad. Sci. USA. 90:11307-11311.
18. Speiser, D.E., R. Miranda, A. Zazkarian, M.F. Bachmann, K. McKall-Faienza, B. Odermatt, D. Hanahan, R.M. Zinkernagel, and P.S. Ohashi. 1997. Self-antigens expressed by solid tumors do not efficiently stimulate naive or activated T cells: implications for immunotherapy. J. Exp. Med. 186:645-653.
19. Rakmilevich, A.L., J. Turner, M.J. Ford, D. McCabe, W.H. Sun, P.M. Sondel, K. Grota, and N. Yang. 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.
20. Sun, W.H., J.K. Burkholder, J. Sun, J. Culp, J. Turner, X.G. Lu, T.D. Pugh, W.B. Ershler, and N. Yang. 1995. In vivo cytokine gene transfer by gene gun reduces tumor growth in mice. Proc. Natl. Acad. Sci. USA. 92:2889-2893.
21. Kotzin, B.L., D.Y.M. Leung, J. Kappler, and P. Marrack. 1993. Superantigens and their potential role in human disease. Adv. Immunol. 54:99-165.
22. Leung, D.Y.M., G.M. Gately, A. Trumble, B. Ferguson-Darnell, P.M. Schlievert, and L.J. Picker. 1995. Bacterial superantigens induce T cell expression of the skin-selective homing receptor, the cutaneous lymphocyte-associated antigen, via stimulation of interleukin-12 production. J. Exp. Med. 181: 747-753.
23. Sriskandan, S., T.J. Evans, and J. Cohen. 1996. Bacterial superantigeninduced human lymphocyte responses are nitric oxide dependent and mediated by IL-12 and IFN-gamma. J. Immunol. 156:2430-2435.
24. Lando, P.A., G. Hedlund, M. Dohlsten, and T. Kalland. 1991. Bacterial superantigens as anti-tumour agents: induction of tumour cytotoxicity in human lymphocytes by staphylococcal enterotoxin A. Cancer Immunol. Immunother. 33:231-237.
25. Ochi, A., K. Migita, J. Xu, and K. Simonovitch. 1993. In vivo tumor immunotherapy by a bacterial superantigen. J. Immunol. 151:3180-3186.
26. Newell, K.A., J.D.I. Ellenhorn, D.S. Bruce, and J.A. Bluestone. 1991. In vivo T-cell activation by staphylococcal enterotoxin B prevents outgrowth of a malignant tumor. Proc. Natl. Acad. Sci. USA. 88:1074-1078.
27. Shu, S., R.A. Krinock, T. Matsumura, J.L. Sussman, B.A. Fox, A.E. Chang, and D.S. Terman. 1944. Stimulation of tumor-draining lymph node cells with superantigenic staphylococcal toxins leads to the generation of tumor-specific effector cells. J. Immunol. 152:1277-1288.
28. Dohlsten, M., L. Abrahamsen, P. Bjork, P.A. Lando, G. Hedlund, G. Forsberg, T. Brodin, N.R.J. Gascoigne, C. Forberg, P. Lind, and T. Kalland. 1994. Monoclonal antihody-superantigen fusion proteins: tumor-specific agents for T-cell-based tumor therapy. Proc. Natl. Acad. Sci. USA. 91:8945-8949.
29. Dow, S.W., and T.A. Potter. 1997. Expression of bacterial superantigen genes in mice induces localized mononuclear cell responses. J. Clin. Invest. 99: 2616-2623.
30. Carlsson, R., H. Fischer, and H.O. Sjogren. 1988. Binding of staphylococcal enterotoxin A to accessory cells is a requirement for its ability to activate human T cells. J. Immunol. 140:2484-2488.
31. Harvey, H.J., E.G. MacEwen, D. Braun, and A.K. Patnaik. 1981. Prognostic criteria for dogs with oral melanoma. J. Am. Vet. Med. Assoc. 178:580-582.
32. Withrow, S.J. 1989. Tumors of the gastrointestinal system and oral cavity. In Clinical Veterinary Oncology. S.J. Withrow and E.G. MacEwen, editors. J.B. Lippincott Co., Philadelphia. 227-261.
33. Zhu, N., D. Liggitt, Y. Liu, and R. Debs. 1993. Systemic gene expression after intravenous DNA delivery into adult mice. Science. 261:209-211.
34. Solodin, I., C.S. Brown, M.S. Bruno, C. Chow, E. Jang, R.J. Debs, and T.D. Heath, 1995. A novel series of amphiphilic imidazolinium compounds for in vitro and in vivo gene delivery. Biochemistry. 34:13537-13544.
35. Cobbold, S.P., and S. Metcalf. 1994. Monoclonal antibodies that define canine homologues of human CD antigens: summary of the first international canine leukocyte antigen workshop (CLAW). Tissue Antigens. 43:137-154.
36. Kawakami, Y., S. Eliyahu, C. Jennings, K. Sakaguchi, X. Kang, S. Southwood, P.F. Robbins, A. Seite, E. Appella, and S.A. Rosenberg. 1995. Recognition of multiple epitopes in the human melanoma antigen gp100 by tumor infiltrating lymphocytes associated with in vivo tumor regression. J. Immunol. 154:3961-3968.
37. Rosenberg, S.A., B.S. Packard, B.M. Aebersold, D. Solomon, S.L. Topalian, S.T., Toy, P. Simon, M.T. Lotze, J.C. Yang, C.A. Seipp, et al. 1988. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. N. Engl. J. Med. 319: 1676-1680.
38. Herman, A., J.W. Kappler, P. Marrack, and A.M. Pullen. 1991. Superantigens: mechanism of T-cell stimulation and role in immune responses. Annu. Rev. Immunol. 9:745-772.
39. Prohaska, J.V., V. Kocandrle, and E. Houttuin. 1966. Hemodynamic changes in response to staphylococcal exotoxin and enterotoxin. Bull. Soc. Int. Chir. 25:727-736.
40. Gilbert, C.F. 1966. Effects of staphylococcal enterotoxin B on the coagulation mechanism and leukocytic response in beagle dogs: a preliminary study. Thromb. Diath. Haemorrh. 16:697-706.
41. MacEwen, E.G., A.K. Patnaik, H.J. Harvey, A.A. Hayes, and R. Matus. 1986. Canine oral melanoma: comparison of surgery versus surgery plus Corynebacterium parvum. Cancer Invest. 4:397-406.
42. McCormack, J.E., J. Kappler, and P. Marrack. 1994. Stimulation with specific antigen can block superantigen-mediated deletion of T cells in vivo. Proc. Natl. Acad. Sci. USA. 91:2086-2090.
43. Pisetsky, D.S. 1996. Immune activation by bacterial DNA: a new genetic code. Immunity. 5:303-310.
44. Parker, S.E., S. Khatibi, M. Margalith, D. Anderson, M. Yankauckas, S.H. Gromkowski, T. Latimer, D. Lew, M. Marquet, M. Manthorpe, et al. 1996. Plasmid DNA gene therapy: studies with the human interleukin-2 gene in tumor cells in vitro and in the murine B16 melanoma model in vivo. Cancer Gene Ther. 3:175-185.