Interferon-γ and CXC chemokine induction by interleukin 12 in renal cell carcinoma

Clinical Cancer Research

Volumn 5, Issue 10, 1999, Pages 2780-2789

  Bukowski, Ronald M ^a   Rayman, Patricia ^a   Molto, Luis ^a   Tannenbaum, Charles S ^a   Olencki, Thomas ^a   Peereboom, David ^a   Tubbs, Raymond ^a   McLain, Denise ^a   Budd, G Thomas ^a   Griffin, Thomas ^b   Novick, Andrew ^a   Hamilton, Thomas A ^a   Finke, James ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b Cleveland Clinic Foundation ^*

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CHEMOKINE; GAMMA INTERFERON; RECOMBINANT INTERLEUKIN 12;

ANTIBODY RESPONSE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER REGRESSION; CYTOKINE PRODUCTION; GENE EXPRESSION; HUMAN; HUMAN TISSUE; KIDNEY CARCINOMA; PRIORITY JOURNAL; SKIN BIOPSY; TUMOR BIOPSY;

ANIMALS; CARCINOMA, RENAL CELL; CHEMOKINES, CXC; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTERFERON TYPE II; INTERLEUKIN-12; KIDNEY NEOPLASMS; MICE; RECOMBINANT PROTEINS; RNA, MESSENGER; TUMOR CELLS, CULTURED;

EID: 0032697304     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (62)

1. Kobayashi, M., Fitz, L., Ryan, M., Hewick, R. M., Clark, S. C., Chan, S., Loudon, R., Sherman, F., Perussia, B., and Trinchieri, G. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biologic effects on human lymphocytes. J. Exp. Med., 170: 827-845, 1989.
2. Stern, A. S., Podlaski, F. J., Hulrnes, J. D., Pan, Y. C., Quinn, P. M., Wolitzky, A. G., Familletti, P. C., Stremlo, D. L., Truitt, T., Chizzonite, R., and Gately, M. K. Purification to homogeneity and partial characterization of cytotoxic lymphocyte maturation factor from human B-lymphoblastoid cells. Proc. Natl. Acad. Sci. USA, 87: 6808-6812, 1990.
3. Wolf, S. F., Temple, P. A., Kobayashi, M., Young, D., Dicig, M., Lowe, L., Dzialo, R., Fitz, L., Ferenz, C., Hewick, R. M., Kelleher, K., Herrmann, S. H., Clark, S. C., Azzoni, L., Chan, S. H., Trinchieri, G., and Perussia, B. Cloning of cDNA for natural killer cell stimulalory factor, a heterodimeric cytokine with multiple biologic effects on T and natural killer cells. J. Immunol., 146: 3074-3081, 1991.
4. Chan, S. H., Kobayashi, M., Santoli, D., Perussia, B., and Trinchieri, G. Mechanisms of IFNγ induction by natural killer cell stimulatory factor (NKSF/IL-12). Role of transcription and mRNA stability in the synergistic interaction between NKSF and IL-2. J. Immunol., 148: 92-98, 1992.
5. Gately, M. K., Wolitzky, A. G., Quinn, P. M., and Chizzonite, R. Regulation of human cytolytic lymphocyte responses by interleukin-12. Cell Immunol., 143: 127-142, 1992.
6. Gately, M. K., Desai, B. B., Wolitzky, A. G., Quinn, P. M., Dwyer, C. M., Podlaski, F. J., Familletti, P. C., Sinigaglia, F. L., Chizonnite, R., Gubler, U., and Stern, A. S. Regulation of human lymphocyte proliferation by a heterodimeric cytokine, IL-12 (cytotoxic lymphocyte maturation factor). J. Immunol., 147: 874-884, 1991.
7. Bertagnolli, M. M., Lin, B. Y., Young, D., and Herrmann, S. H. IL-12 augments antigen-dependent proliferation of activated T lymphocytes. J. Immunol., 149: 3778-3883, 1992.
8. Gubler, U., Chua, A. O., Schoenhaut, D. S., Dwyer, C. M., McComas, W., Motyka, R., Nabavi, N., Wolitzky, A. G., Quinn, P. M., Familletti, P. C., and Gately, M. K. Coexpression of two distinct genes is required to generate secreted bioactive cytotoxic lymphocyte maturation factor. Proc. Natl. Acad. Sci. USA, 88: 4143-4147, 1991.
9. Roberston, M. J., Soiffer, R. J., Wolf, S. F., Manley, T. J., Donahue, C., Young, D., Herrmann, S. H., and Ritz, J. Response of human natural killer (NK) cells to NK cell stimulatory factor (NKSF): cytolytic activity and proliferation NK cells are differentially regulated by NKSF. J. Exp. Med., 175: 779-788, 1992.
10. + Th1 cells. Science (Washington DC), 263: 235-237, 1994.
11. Sypek, J. P., Chung, C. L., Mayor, S. E. H., Subramanyam, J. M., Goldman, S. J., Siebwith, D. S., Wolf, S. F., and Schaub, R. G. Resolution of cutaneous leishmaniasis: interleukin-12 initials a protective T-helper type 1 immune response. J. Exp. Med., 177: 1797-1802, 1993.
12. Zhou, P., Sieve, M. C., Bennett, J., Kwonchung, K. J., Tewari, R. P., Gazzinelli, R. T., and Shera Seder, R. A. IL-12 prevents mortality in mice infected with Histoplasma capsulatum through induction of IFN-γ. J. Immunol., 155: 785-795, 1995.
13. Wynn, T. A., Eltown, I., Oswald, I. P., Cheever, A. W., and Sher, A. Endogenous interleukin-12 (IL-12) regulates granuloma formation induced by eggs of Schistosoma mansoni and exogenous IL-12 both inhibits and prophylactically immunizes against egg pathology. J. Exp. Med., 179: 1551-1561, 1994.
14. Stern, A. S., Magram, J., and Presky, D. H. Interleukin-12 an integral cytokine in the immune response. Life Sci., 58: 639-654, 1996.
15. Orange, J. S., Wolf, S. F., and Biron, C. A. Effects of IL-12 on the response and susceptibility to experimental viral infections. J. Immunol., 152: 1253-1264, 1994.
16. Brunda, M. J., Luistro, L., and Warrier, R. R. Antitumor and antimetastatic activity of interleukin-12 against murine tumors. J. Exp. Med., 178: 1223-1230, 1993.
17. Brunda, M. J., and Gately, M. K. Antitumor activity of interleukin-12. Clin. Immunol. Immunopathol., 71: 253-255, 1994.
18. Takara, H., Zek, H. J., and Strokus, W. J. Fibroblasts genetically engineered to secret interleukin-12 can suppress tumor growth and induce antitumor immunity to a murine melanoma in vivo. Cancer Res., 54: 182-189, 1994.
19. 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.
20. Trinchieri, G. Interleukin-12 and its role in the generation of Th1 cells. Immunol. Today, 14: 335-338, 1993.
21. Trinchieri, G., and Scott, P. The role of interleukin 12 in the immune response, disease and therapy. Immunol. Today, 15: 460-463, 1994.
22. Manetti, R., Parronchi, P., Giudizi, M. G., Piccinni, M-P., Maggi, E., Trinchieri, G., and Romagnani, S. Natural killer cell stimulatory factor (interleukin 12 [IL-12]) induces T helper type 1 (Th1)-specific immune response and inhibits the development of IL-4 producing Th cells. J. Exp. Med., 177: 1199-1204, 1993.
23. Kobayashi, M., Fitz, L., Ryan, M., Hewick, R. M., Clark, S. C., Chan, S., Loudon, F., Sherman, F., Perussia, B., and Trinchieri, G. Identification and purification of natural killer cell stimulatory factor (NKSF), a cytokine with multiple biological effects on human lymphocytes. J. Exp. Med., 170: 827-845, 1989.
24. Trinchieri, G. Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu. Rev. Immunol., 13: 251-276, 1995.
25. 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 association with IFNγ production. J. Immunol., 153: 1697-1706, 1994.
26. Brunda, M. J., Luistro, L., Hendrzak, J. A., Fountoulakis, M., Garotta, G., and Gately, M. K. Role of interferon-γ mediating the antitumor efficiacy of interleukin-12. J. Immunother., 17: 71-77, 1995.
27. Farber, J. M. A macrophage mRNA selectively induced by γ-interferon encodes a member of the platelet factor 4 family of cytokines. Proc. Natl. Acad. Sci. USA, 87: 5238-5242, 1990.
28. Liao, F., Rabin, R. L., Yannelli, J. R., Konvares, L. G., Vanguri, P., and Farber, J. M. Human Mig chemokine: biochemical and functional characterization. J. Exp. Med., 182: 1301-1314, 1995.
29. Luster, A. D., Unkeless, J. C., and Ravetch, J. V. γ-interferon transcriptionally regulates an early response gene containing homology to platelet proteins. Nature (Lond.), 315: 672-676, 1985.
30. Taub, D. D., Lloyd, A. R., Conlon, K., Wang, J. M., Ortaldo, J. R., Harada, A., Matsushima, K., Kelvin, D. J., and Oppenheim, J. J. Recombinant human interferon inducible protein 10 is a chemoattractant for human monocytes and T-lymphocytes and promotes T-cell adhesion to endothelial cells. J. Exp. Med., 177: 1809-1814, 1993.
31. Loetscher, M. L., Gerber, B., Loetscher, P., Jones, S. A., Piali, L., Clark-Lewis, I., Baggiolini, M., and Moser, B. Chemokine receptor specific for IP-10 and Mig: structure, function and expression in activated T-lymphocytes. J. Exp. Med., 184: 963-969, 1996.
32. Luster, A. D., Greenberg, S. M., and Leder, P. The IP-10 chemokine binds to a specific cell surface heparin sulfate site shared with platelet factor 4 and inhibits endothelial cell proliferation. J. Exp. Med., 182: 219-231, 1995.
33. Angiolillo, A. L., Sgardari, C., Taub, D. D., Liao, F., Farber, J. M., Maheshwari, S., Kleinman, H. K., Reaman, G. H., and Tosato, G. Human interferon inducible protein 10 is a potent inhibitor of angiogenesis in vivo. J. Exp. Med., 182: 155-162, 1995.
34. Sgadari, C., Angiolillo, A. L., and Tosato, G. Inhibition of angiogenesis by interleukin-12 is mediated by the interferon-inducible protein 10, Blood, 87: 3877-3882, 1996.
35. Farber, J. M. Mig and IP-10: CXC chemokines that target lymphocytes. J. Leukocyte Biol., 61: 246-257, 1997.
36. Streiter, R. M., Polverini, P. J., Kunkel, S. L., Arenberg, D. A., Burdick, M. D., Kasper, J., Dzuiba, J., Van Damme, J., Waltz, A., Marriott, D., Chan, S-Y., Roczniak, S., and Shanafelt, A. B. The functional role of the ELR motif in CXC chemokine-mediated angiogenesis. J. Biol. Chem., 270: 27348-27357, 1995.
37. 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.
38. Bukowski, R. M., Olencki, T., and Gunn, H. Phase I trial of subcutaneous IL-3 in patients with refractory malignancy: hematologic, immunologic, and pharmacodynamic findings. Clin. Cancer Res., 2: 347-357, 1996.
39. Wang, Q., Redovan, C., Tubbs, R., Olencki, T., Klein, E., Kudoh, W., Finke, J., and Bukowski, R. M. Selective cytokine gene expression in renal cell carcinoma tumor cells and tumor infiltrating lymphocytes. Int. J. Cancer, 61: 780-785, 1995.
40. Wang, Q., Stanley, J., Kudoh, S., Myles, J., Kolenko, V., Yi, T., Tubbs, R., Bukowski, R., and Finke, J. T cells infiltrating non-Hodgkin's B cell lymphomas show altered tyrosine phosphorylation pattern even though T cell receptor/CD3-associated kinases are present. J. Immunol., 155: 1382-1392, 1995.
41. Kubin, M., Kamoun, M., and Trinchieri, G. Interleukin 12 synergizes with B7/CD28 interaction in inducing efficient proliferation and cytokine production of human T cells. J. Exp. Med., 180: 211-222, 1994.
42. Trinchieri, G. Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Annu. Rev. Immunol., 13: 251-276, 1995.
43. lck in T-cells infiltrating human renal cell carcinoma. Cancer Res., 53: 5613-5616, 1993.
44. Li, X., Liu, J., Park, J., Hamilton, T. A., Rayman, P., Klein, E., Edinger, M., Tubbs, R., Bukowski, R., and Finke, J. T-cells from renal cell carcinoma patients exhibit an abnormal pattern of κB-specific DNA-binding activity: a preliminary report. Cancer Res., 54: 5424-5429, 1994.
45. Alexander, J. P., Kudoh, S., Melsop, K. A., Hamilton, T. A., Edinger, M. G., Tubbs, R. R., Sica, D., Tuason, L., Klein, E., Bukowski, R. M., and Finke, J. T-cell infiltrating renal cell carcinoma display a poor proliferative response even though they can produce IL-2 and express IL-2 receptors. Cancer Res., 53: 1380-1387, 1993.
46. Coventry, B. J., Weeks, S. C., Heckford, S. E., Sykes, P. J., Bradley, J., and Skinner, J. M. Lack of IL-2 cytokine gene expression despite IL-2 messenger RNA transcription in tumor-infiltrating lymphocytes in primary human breast carcinoma. J. Immunol., 156: 3486-3492, 1996.
47. Bennett, M. W., O' Connell, J., O'Sullivan, G. C., Brady, C., Roche, D., Collins, J. K., and Shanahan, F. The Fas counterattack in vivo: apoptotic depletion of tumor-infiltrating lymphocytes associated with Fas ligand expression by human esophageal carcinoma. J. Immunol., 160: 5669-5675, 1998.
48. Browning, M. J., and Bodmer, W. F. MHC antigens and cancer: implications for T cell surveillance. Curr. Opin. Immunol., 4: 613-618, 1992.
49. Miescher, S., Whiteside, T. L., Carrel, S., and von Fliedner, V. Functional properties of tumor infiltrating and blood lymphocytes in patients with solid tumors: effects of tumor cells and their supernatants on proliferative responses of lymphocytes. J. Immunol., 136: 1899-1907, 1986.
50. Yagita, M., Seppo, A., Renkonen, O., and Saksela, E. Deacetylase activity of human tumor cells producing immunosuppressive amino sugars: its possible role in resistance to cell-mediated cytotoxicity. Cancer Res., 53: 5600-5604, 1993.
51. Li, R., Gage, D., and Ladisch, S. Biosynthesis and shedding of murine lymphoma gangliosides. Biochem. Biophys. Acta, 1170: 283-290, 1993.
52. Bergelson, L. D. Gangliosides and antitumor immunity. Clin. Investig., 71: 590-594, 1993.
53. Strand, S., Hofmann, W. J., Hug, H., Muller, M., Otto, G., Strand, D., Mariani, S. M., Stremmel, W., Krammer, P. H., and Galle, P. R. Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand-expressing tumor cells: a mechanism of immune evasion? Nat. Med., 2: 1361-1366, 1996.
54. Hahne, M., Rimoldi, D., Schroter, M., Romero, P., Schreier, M., French, L. E., Schneider, P., Bornand, T., Fontana, A., Lienard, D., Cerottini, J-C., and Tschopp, J. Melanoma cell expression of Fas (Apo-1/CD95) ligand: implications for tumor immune escape. Science (Washington DC), 274: 1363-1366, 1996.
55. Niehans, G. A., Brunner, T., Frizelle, S. P., Liston, J. C., Salerno, C. T., Knapp, D. J., Green, D. R., and Kratzke, R. A. Human lung carcinomas express Fas ligand. Cancer Res., 57: 1007-1012, 1997.
56. Saas, P., Walker, P. R., Hahne, M., Quiquerez, A-L., Schnuriger, V., Perrin, G., French, L., Van Meir, E. G., de Tribolet, N., Tschopp, J., and Dietrich, P-Y. Fas ligand expression by astrocytoma in vivo: maintaining immune privilege in the brain? J. Clin. Investig., 99: 1173-1178, 1997.
57. O'Connell, J., O'Sullivan, G. C., Collins, J. K., and Shanahan, F. The Fas-counterattack: Fas-mediated T cell killing by colon cancer cells expressing Fas ligand. J. Exp. Med., 184: 1075-1082, 1996.
58. Shiraki, K., Tsuji, N., Shioda, T., Isselbacher, K. J., and Takahashi, H. Expression of Fas ligand in liver metastases of human colonic adenocarcinomas. Proc. Natl. Acad. Sci. USA, 94: 6420-6425, 1997.
59. Rabinowich, H., Reichert, T. E., Kashii, Y., Gastman, B. R., Bell, M. C., and Whiteside, T. L. Lymphocyte apoptosis induced by Fas ligand-expressing ovarian carcinoma cells: implications for altered expression of T cell receptor in tumor-associated lymphocytes. J. Clin. Investig., 101: 2579-2588, 1998.
60. Walker, P. R., Saas, P., and Dietrich, P-Y. The role of Fas ligand (CD95L) in immune escape: the tumor strikes back. J. Immunol., 158: 4521-4524, 1997.
61. Cardi, G., Heaney, J. A., Schned, A. R., and Ernstoff, M. S. Expression of Fas (APO-1/CD95) in tumor-infiltrating and peripheral blood lymphocytes in patients with renal cell carcinoma. Cancer Res., 58: 2078-2080, 1998.
62. Uzzo, R. G., Rayman, P., Kolenko, V., Clark, P. E., Bloom, T., Ward, A. M., Molto, L., Tannenbaum, C. S., Worford, L. J., Bukowski, R., Tubbs, R., Hsi, E. D., Bander, N. H., Novick, A. C., and Finke, J. H. Mechanisms of apoptosis in T cells from patients with renal cell carcinoma. Clin. Cancer Res., 5: 1219-1229, 1999