Successful adoptive cellular immunotherapy is dependent on induction of a host immune response triggered by cytokine (IFN-γ and granulocyte/macrophage colony-stimulating factor) producing donor tumor- infiltrating lymphocytes

Journal of Immunology

Volumn 160, Issue 1, 1998, Pages 334-344

  Nagoshi, Makoto ^a   Goedegebuure, Peter S ^a   Burger, Ulrike L ^a,b   Sadanaga, Noriaki ^a   Chang, Maximilian P ^a   Eberlein, Timothy J ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; RECOMBINANT INTERLEUKIN 2; THY 1 ANTIGEN;

ADOPTIVE IMMUNOTHERAPY; ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; FEMALE; FIBROSARCOMA; INTRAPERITONEAL DRUG ADMINISTRATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR ASSOCIATED LEUKOCYTE;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, THY-1; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; FLOW CYTOMETRY; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; IMMUNITY, CELLULAR; IMMUNOTHERAPY; INTERFERON TYPE II; LYMPHOCYTES, TUMOR-INFILTRATING; METHYLCHOLANTHRENE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, SCID; SARCOMA, EXPERIMENTAL; T-LYMPHOCYTE SUBSETS;

EID: 0031883246     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (54)

1. Eberlein, T. J., M. Rosenstein, and S. A. Rosenberg. 1982. Regression of a disseminated syngeneic solid tumor by systemic transfer of lymphoid cells expanded in interleukin 2. J. Exp. Med. 156:385.
2. Geiger, J. D., P. D. Wagner, M. J. Cameron, S. Shu, and A. E. Chang. 1993. Generation of T-cells reactive to the poorly immunogenic B16-BL6 melanoma with efficacy in the treatment of spontaneous metastases. J. Immunother. 13:153.
3. Lafreniere, R., and S. A. Rosenberg. 1985. Successful immunotherapy of murine experimental hepatic metastases with lymphokine-activated killer cells and recombinant interleukin 2. Cancer Res. 45:3735.
4. Massaro, A. F., D. D. Schoof, A. Rubinstein, M. Zuber, V. F. Leonard, and T. J. Eberlein. 1990. Solid-phase anti-CD3 antibody activation of murine tumor-infiltrating lymphocytes. Cancer Res. 50:2587.
5. Matsumura, T., J. J. Sussman, R. A. Krinock, A. E. Chang, and S. Shu. 1994. Characteristics and in vivo homing of long-term T-cell lines and clones derived from tumor-draining lymph nodes. Cancer Res. 54:2744.
6. Rosenstein, M., I. Yron, Y. Kaufmann, and S. A. Rosenberg. 1984. Lymphokine-activated killer cells: lysis of fresh syngeneic natural killer-resistant murine tumor cells by lymphocytes cultured in interleukin 2. Cancer Res. 44:1946.
7. Tuttle, T. M., T. H. Inge, K. P. Bethke, C. W. McCrady, G. R. Pettit, and H. D. Bear. 1992. Activation and growth of murine tumor-specific T-cells which have in vivo activity with bryostatin 1. Cancer Res. 52:548.
8. Wallace, P. K., L. D. Palmer, L. D. Perry, E. S. Bolton, R. B. Alexander, P. K. Horan, J. C. Yang, and K. A. Muirhead. 1993. Mechanisms of adoptive immunotherapy: improved methods for in vivo tracking of tumor-infiltrating lymphocytes and lymphokine-activated killer cells. Cancer Res. 53:2358.
9. Yoshizawa, H., A. E. Chang, and S. Shu. 1991. Specific adoptive immunotherapy mediated by tumor-draining lymph node cells sequentially activated with anti-CD3 and IL-2. J. Immunol. 147:729.
10. Rosenberg, S. A., P. Spiess, and R. Lafreniere. 1986. A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science 233:1318.
11. Spiess, P. J., J. C. Yang, and S. A. Rosenberg. 1987. In vivo antitumor activity of tumor-infiltrating lymphocytes expanded in recombinant interleukin-2. J. Natl. Cancer Inst. 79:1067.
12. Burton, R. C., and N. L. Warner. 1977. In vitro induction of tumor-specific immunity. IV. Specific adoptive immunotherapy with cytotoxic T cells induced in vitro to plasmacytoma antigens. Cancer Immunol. Immunother. 2:91.
13. Kedar, E., M. Schwartzbach, Z. Raanan, and S. Hefetz. 1977. In vitro induction of cell-mediated immunity to murine leukemia cells. II. Cytotoxic activity in vitro and tumor-neutralizing capacity in vivo of anti-leukemia cytotoxic lymphocytes generated in macrocultures. J. Immunol. Methods 16:39.
14. + tumor-infiltrating lymphocytes. J. Exp. Med. 173:647.
15. Shu, S., R. A. Krinock, T. Matsumura, J. J. Sussman, B. A. Fox, A. E. Chang, and D. S. Terman. 1994. Stimulation of tumor-draining lymph node cells with superantigenic staphylococcal toxins leads to the generation of tumor-specific effector T cells. J. Immunol. 152:1277.
16. Tuttle, T. M., C. W. McCrady, T. H. Inge, M. Salour, and H. D. Bear. 1993. Gamma-interferon plays a key role in T-cell-induced tumor regression. Cancer Res. 53:833.
17. Aruga, A., S. Shu, and A. E. Chang. 1995. Tumor-specific granulocyte/macrophage colony-stimulating factor and interferon gamma secretion is associated with in vivo therapeutic efficacy of activated tumor-draining lymph node cells. Cancer Immunol. Immunother. 41:317.
18. Goedegebuure, P. S., M. Zuber, V. D. Leonard, U. L. Burger, J. J. Cusack, M. P. Chang, L. M. Douville, and T. J. Eberlein. 1994. Reactivation of murine tumour-infiltrating lymphocytes with solid-phase anti-CD3 antibody: in vitro cytokine production is associated with in vivo efficacy. Surg. Oncol. 3:79.
19. + T cells by tumor-infiltrating lymphocytes and recombinant interleukin-2 during adoptive immunotherapy of cancer. Surgery 117:325.
20. Shu, S., and S. A. Rosenberg. 1985. Adoptive immunotherapy of a newly induced sarcoma: immunologic characteristics of effector cells. J. Immunol. 135:2895.
21. Parker, G. A., and S. A. Rosenberg. 1977. Serologic identification of multiple tumor-associated antigens on murine sarcomas. J. Natl. Cancer Inst. 58:1303.
22. Fekete, E. 1938. A comparative morphological study of the mammary gland in a high and low tumor strain of mice. Am. J. Pathol. 14:557.
23. Sander, B., J. Andersson, and U. Andersson. 1991. Assessment of cytokines by immunofluorescence and the paraformaldehyde-saponin procedure. Immunol. Rev. 119:65.
24. Sander, B., I. Hoiden, U. Andersson, E. Moller, and J. Abrams. 1993. Similar frequencies and kinetics of cytokine producing cells in murine peripheral blood and sera. J. Immunol. Methods 166:201.
25. Stoppacciaro, A., C. Melani, M. Parenza, A. Mastracchio, C. Bassi, C. Baroni, G. Parmiani, and M. P. Colombo. 1993. Regression of an established tumor genetically modified to release granulocyte colony-stimulating factor requires granulocyte-T cell cooperation and T cell-produced interferon gamma. J. Exp. Med. 178:151.
26. Suda, T., A. O'Garra, I. MacNeil, M. Fischer, M. W. Bond, and A. Zlotnik. 1990. Identification of a novel thymocyte growth-promoting factor derived from B cell lymphomas. Cell. Immunol. 129:228.
27. Aebersold, P., C. Hyatt, S. Johnson, K. Hines, L. Korcak, M. Sanders, M. Lotze, S. Topalian, J. Yang, and S. A. Rosenberg. 1991. Lysis of autologous melanoma cells by tumor-infiltrating lymphocytes: association with clinical response. J. Natl. Cancer Inst. 83:932.
28. Alexander, R. B., and S. A. Rosenberg. 1990. Long-term survival of adoptively transferred tumor-infiltrating lymphocytes in mice. J. Immunol. 145:1615.
29. Alexander, R. B., and S. A. Rosenberg. 1991. Adoptively transferred tumor-infiltrating lymphocytes can cure established metastatic tumor in mice and persist long-term in vivo as functional memory T lymphocytes. J. Immunother. 10:389.
30. Kurt, R. A., J. A. Park, M. C. Panelli, S. F. Schluter, J. J. Marchalonis, B. Carolus. and E. T. Akporiaye. 1995. T lymphocytes infiltrating sites of tumor rejection and progression display identical V beta usage but different cytotoxic activities. J. Immunol. 154:3969.
31. Bannerji, R., C. D. Arroyo, C. C. Cordon, and E. Gilboa. 1994. The role of IL-2 secreted from genetically modified tumor cells in the establishment of antitumor immunity. J. Immunol. 152:2324.
32. Dranoff, G., E. Jaffee, A. Lazenby, P. Golumbek, H. Levitsky, K. Brose, V. Jackson, H. Hamada, D. Pardoll, and R. C. Mulligan. 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.
33. + tumor-infiltrating lymphocytes following adoptive immunotherapy in a murine tumor model system. Eur. J Immunol. 21:1815.
34. Evans, R., S. J. Kamdar, T. Duffy, and L. Edison. 1993. Intratumor gene expression after adoptive immunotherapy in a murine tumor model: regulation of messenger RNA levels associated with the differential expansion of tumor-infiltrating lymphocytes. J. Immunol. 150:177.
35. Mule, J. J., M. C. Custer, W. D. Travis, and S. A. Rosenberg. 1992. Cellular mechanisms of the antitumor activity of recombinant IL-6 in mice. J. Immunol. 148:2622.
36. Vagliani, M., M. Rodolfo, F. Cavallo, M. Parenza, C. Melani, G. Parmiani, G. Forni, and M. P. Colombo. 1996. Interleukin 12 potentiates the curative effect of a vaccine based on interleukin 2-transduced tumor cells. Cancer Res. 56:467.
37. Meltzer, M. S. 1981. Macrophage activation for tumor cytotoxicity: characterization of priming and trigger signals during lymphokine activation. J. Immunol. 127:179.
38. Boraschi, D., D. Soldateschi, and A. Tagliabue. 1982. Macrophage activation by interferon: dissociation between tumoricidal capacity and suppressive activity. Eur. J. Immunol. 12:320.
39. Pace, J. L., S. W. Russell, B. A. Torres, H. M. Johnson, and P. W. Gray. 1983. Recombinant mouse gamma interferon induces the priming step in macrophage activation for tumor cell killing. J. Immunol. 130:2011.
40. Mule, J. J., M. Rosenstein, S. Shu, and S. A. Rosenberg. 1985. Eradication of a disseminated syngeneic mouse lymphoma by systemic adoptive transfer of immune lymphocytes and its dependence upon a host component(s). Cancer Res. 45:526.
41. Sallusto, F., and A. Lanzavecchia. 1994. Efficient presentation of soluble antigen by cultured human dendritic cells is maintained by granulocyte/macrophage colony-stimulating factor plus interleukin 4 and downregulated by tumor necrosis factor alpha. J. Exp. Med. 179:1109.
42. Paglia, P., C. Chiodoni, M. Rodolfo, and M. P. Colombo. 1996. Murine dendritic cells loaded in vitro with soluble protein prime cytotoxic T lymphocytes against tumor antigen in vivo (see comments). J. Exp. Med. 183:317.
43. Heufler, C., F. Koch, and G. Schuler. 1988. Granulocyte/macrophage colony-stimulating factor and interleukin 1 mediate the maturation of murine epidermal Langerhans cells into potent immunostimulatory dendritic cells. J. Exp. Med. 167:700.
44. Armstrong, C. A., R. Botella, T. H. Galloway, N. Murray, J. M. Kramp, I. S. Song, and J. C. Ansel. 1996. Antitumor effects of granulocyte-macrophage colony-stimulating factor production by melanoma cells. Cancer Res. 56:2191.
45. Zitvogel, L., J. I. 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.
46. + tumor-infiltrating lymphocytes. J. Immunol. 153:1202.
47. Rosenberg, S. A., B. S. Packard, P. M. Aebersold, D. Solomon, S. L. Topalian, S. T. Toy, P. Simon, M. T. Lotze, J. C. Yang, C. A. Seipp, C. Simpson, and C. Carter. 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.
48. Rosenberg, S. A., P. Aebersold, K. Cornetta, A. Kasid, R. A. Morgan, R. Moen, E. M. Karson, M. T. Lotze, J. C. Yang, S. L. Topalian, M. J. Merino, and K. Culver. 1990. Gene transfer into humans: immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction. N. Engl. J. Med. 323:570.
49. Eberlein, T. J., M. L. Rodrick, A. F. Massaro, S. E. Jung, J. A. Mannick, and D. D. Schoof. 1989. Immunomodulatory effects of systemic low-dose recombinant interleukin-2 and lymphokine-activated killer cells in humans. Cancer Immunol. Immunother. 30:145.
50. Schoof, D. D., B. A. Gramolini, D. L. Davidson, A. F. Massaro, R. E. Wilson, and T. J. Eberlein. 1988. Adoptive immunotherapy of human cancer using low-dose recombinant interleukin 2 and lymphokine-activated killer cells. Cancer Res. 48:5007.
51. Eberlein, T. J., D. D. Schoof, S. E. Jung, D. Davidson, B. Gramolini, K. McGrath, A. Massaro, and R. E. Wilson. 1988. A new regimen of interleukin 2 and lymphokine-activated killer cells: efficacy without significant toxicity. Arch. Intern. Med. 148:2571.
52. Goedegebuure, P. S., L. M. Douville, H. Li, G. C. Richmond, D. D. Schoof, M. Scavone, and T. J. Eberlein. 1995. Adoptive immunotherapy with tumor-infiltrating lymphocytes and interleukin-2 in patients with metastatic malignant melanoma and renal cell carcinoma: a pilot study. J. Clin. Oncol. 13:1939.
53. Yoshino, I., P. S. Goedegebuure, G. E. Peoples, A. S. Parikh, J. M. DiMaio, H. K. Lyerly, A. F. Gazdar, and T. J. Eberlein. 1994. HER2/neu-derived peptides are shared antigens among human non-small cell lung cancer and ovarian cancer. Cancer Res. 54:3387.
54. Peoples, G. E., P. S. Goedegebuure, R. Smith, D. C. Linehan, I. Yoshino, and T. J. Eberlein. 1995. Breast and ovarian cancer-specific cytotoxic T lymphocytes recognize the same HER2/neu-derived peptide. Proc. Natl. Acad. Sci. USA 92: 432.