TNF-α induction of GM2 expression on renal cell carcinomas promotes T cell dysfunction

Journal of Immunology

Volumn 178, Issue 10, 2007, Pages 6642-6652

  Raval, Gira ^a   Biswas, Soumika ^a   Rayman, Patricia ^a   Biswas, Kaushik ^a   Sa, Gaurisankar ^c   Ghosh, Sankar ^a   Thornton, Mark ^a   Hilston, Cynthia ^a   Das, Tanya ^c   Bukowski, Ronald ^b   Finke, James ^a,b   Tannenbaum, Charles S ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b TAUSSIG CANCER INSTITUTE   (United States)

^c BOSE INSTITUTE   (India)

Author keywords

[No Author keywords available]

Indexed keywords

GANGLIOSIDE GM2; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CELL INFILTRATION; DNA MODIFICATION; HUMAN; HUMAN CELL; KIDNEY CARCINOMA; MOLECULAR CLONING; NORMAL HUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE;

EID: 34248165998     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.10.6642     Document Type: Article

References (58)

1. Wang, R. F., G. Zeng, S. F. Johnston, K. Voo, and H. Ying. 2002. T cell-mediated immune responses in melanoma: implications for immunotherapy. Crit. Rev. Oncol. Hematol. 43: 1-11.
2. Finke, J., S. Ferrone, A. Frey, A. Mufson, and A. Ochoa. 1999. Where have all the T cells gone? Mechanisms of immune evasion by tumors. Immunol. Today 20: 158-160.
3. Nielsen, M. B., and F. M. Marincola. 2001. Melanoma vaccines: the paradox of T cell activation without clinical response. Cancer Chemother. Pharmacol. 46(Suppl.): S62-S66.
4. Garrido, F., and I. Algarra. 2001. MHC antigens and tumor escape from immune surveillance. Adv. Cancer Res. 83: 117-158.
5. Chen, Q., V. Daniel, D. W. Maher, and P. Hersey. 1994. Production of IL-10 by melanoma cells: examination of its role in immunosuppression mediated by melanoma. Int. J. Cancer 56: 755-760.
6. Tada, T., S. Ohzeki, K. Utsumi, H. Takiuchi, M. Muramatsu, X. F. Li, J. Shimizu, H. Fujiwara, and T. Hamaoka. 1991. Transforming growth factor-β-induced inhibition of T cell function: susceptibility difference in T cells of various phenotypes and functions and its relevance to immunosuppression in the tumor-bearing state. J. Immunol. 146: 1077-1082.
7. Uzzo, R. G., P. Rayman, V. Kolenko, P. E. Clark, M. K. Cathcart, T. Bloom, A. C. Novick, R. M. Bukowski, T. Hamilton, and J. H. Finke. 1999. Renal cell carcinoma-derived gangliosides suppress nuclear factor-κB activation in T cells. J. Clin. Invest. 104: 769-776.
8. Gastman, B. R., X. M. Yin, D. E. Johnson, E. Wieckowski, G. Q. Wang, S. C. Watkins, and H. Rabinowich. 2001. Tumor-induced apoptosis of T cells: amplification by a mitochondrial cascade. Cancer Res. 60: 6811-6687.
9. Kudo, D., P. Rayman, C. Horton, M. K. Cathcart, R. M. Bukowski, M. Thornton, C. Tannenbaum, and J. H. Finke. 2003. Gangliosides expressed by the renal cell carcinoma cell line SK-RC-45 are involved in tumor-induced apoptosis of T cells. Cancer Res. 63: 1676-1683.
10. Uzzo, R. G., P. Rayman, A. C. Novick, R. M. Bukowski, and J. H. Finke. 2000. Molecular mechanisms of immune dysfunction in renal cell carcinoma. In Renal Cell Carcinoma: Molecular Biology, Immunology and Clinical Management. R. M. Bukowski and A. C. Novick, eds. Humana Press, Totowa, pp. 63-78.
11. Ritter, G., and P. O. Livingston. 1991. Ganglioside antigens expressed by human cancer cells. Semin. Cancer Biol. 2: 401-409.
12. Black, P. H. 1980. Shedding from the cell surface of normal and cancer cells. Adv. Cancer Res. 32: 75-199.
13. Hoon, D. S., E. Okun, H. Neuwirth, D. L. Morton, and R. F. Irie. 1993. Aberrant expression of gangliosides in human renal cell carcinomas. J. Urol. 150: 2013-2018.
14. Biswas, K., A. Richmond, P. Rayman, S. Biswas, M. Thornton, G. Sa, T. Das, R. Zhang, A. Chahlavi, C. S. Tannenbaum, et al. 2006. GM2 expression in renal cell carcinoma: potential role in tumor-induced T-cell dysfunction. Cancer Res. 66: 6816-6825.
15. MacEwan, D. J. 2002. TNF receptor subtype signalling: differences and cellular consequences. Cell. Signal. 14: 477-492.
16. Goeddel, D. V. 1999. Signal transduction by tumor necrosis factor: the Parker B. Francis Lectureship. Chest 116: 69S-73S.
17. Anderson, G. M., M. T. Nakada, and M. DeWitre. 2004. Tumor necrosis factor-α in the pathogenesis and treatment of cancer. Curr. Opin. Pharmacol. 4: 314-320.
18. Qi, H., and M. Ohh. 2003. The von Hippel-Lindau tumor suppressor protein sensitizes renal cell carcinoma cells to tumor necrosis factor-induced cytotoxicity by suppressing the nuclear factor-κB-dependent antiapoptotic pathway. Cancer Res. 63: 7076-7080.
19. Caldwell, M. C., C. Hough, S. Furer, W. M. Linehan, P. J. Morin, and M. Gorospe. 2002. Serial analysis of gene expression in renal carcinoma cells reveals VHL-dependem sensitivity to TNFα cytotoxicity. Oncogene 21: 929-936.
20. Katopodis, N., and C. C. Stock. 1980. Improved method to determine lipid bound sialic acid in plasma or serum. Res. Commun. Chem. Pathol. Pharmacol. 30: 171-180.
21. Ladisch, S., and R. Li. 2000. Purification and analysis of gangliosides. Methods Enzymol. 312: 135-145.
22. McKallip, R., R. Li, and S. Ladisch. 1999. Tumor gangliosides inhibit the tumor-specific immune response. J. Immunol. 163: 3718-3726.
23. Gazzotti, G., S. Sonnino, and R. Ghidoni. 1985. Normal-phase high-performance liquid chromatographic separation of non-derivatized ganglioside mixtures. J. Chromatogr. 348: 371-378.
24. Retter, M. W., J. C. Johnson, D. W. Peckham, J. E. Bannink, C. S. Bangur, K. Dresser, F. Cai, T. M. Foy, N. A. Fanger, G. R. Fanger, et al. 2005. Characterization of a proapoptotic antiganglioside GM2 monoclonal antibody and evaluation of its therapeutic effect on melanoma and small cell lung carcinoma xenografts. Cancer Res. 65: 6425-6434.
25. Schraml, P., K. Struckmann, F. Hatz, S. Sonnet, C. Kully, T. Gasser, G. Sauter, M. J. Mihatsch, and H. Moch. 2002. VHL mutations and their correlation with tumor cell proliferation, microvessel density, and patient prognosis in clear cell renal cell carcinoma. J. Pathol. 196: 186-193.
26. Igarashi, H., M. Esumi, H. Ishida, and K. Okada. 2002. Vascular endothelial growth factor overexpression is correlated with von Hippel-Lindau tumor suppressor gene inactivation in patients with sporadic renal cell carcinoma. Cancer 95: 47-53.
27. Galban, S., J. Fan, J. L. Martindale, C. Cheadle, B. Hoffman, M. P. Woods, G. Temeles, J. Brieger, J. Decker, and M. Gorospe. 2003. von Hippel-Lindau protein-mediated repression of tumor necrosis factor α translation revealed through use of cDNA arrays. Mol. Cell. Biol. 23: 2316-2328.
28. Markotic, A., R. Lumen, A. Marusic, S. Jonjic, and J. Muthing. 1999. Ganglioside expression in tissues of mice lacking the tumor necrosis factor receptor 1. Carbohydr. Res. 321: 75-87.
29. Hayakawa, T., and M. Hirai. 2003. An assay of ganglioside using fluorescence image analysis on a thin-layer chromatography plate. Anal. Chem. 75: 6728-6731.
30. Fahr, C., and R. Schauer. 2001. Detection of sialic acids and gangliosides with special reference to 9-O-acetylated species in basaliomas and normal human skin. J. Invest. Dermatol. 116: 254-260.
31. Miescher, S., M. Stoeck, L. Qiao, C. Barras, L. Barrelet, and F. von Fliedner. 1988. Preferential clonogenic deficit of CD8-positive T-lymphocytes infiltrating human solid tumors. Cancer Res. 48: 6992-6998.
32. Morford, L. A., A. R. Dix, W. H. Brooks, and T. L. Roszman. 1999. Apoptotic elimination of peripheral T lymphocytes in patients with primary intracranial tumors. J. Neurosurg. 91: 935-946.
33. Zbar, A. P. 2004. The immunology of colorectal cancer. Surg. Oncol. 13: 45-53.
34. Whiteside, T. L., Y. L. Wang, R. G. Selker, and R. B. Herberman. 1988. In vitro generation and antitumor activity of adherent lymphokine-activated killer cells from the blood of patients with brain tumors. Cancer Res. 48: 6069-6075.
35. O'Connell, J., G. C. O'Sullivan, J. K. Collins, and F. Shanahan. 1996. The Fas counterattack: Fas-mediated T cell killing by colon cancer cells expressing Fas ligand. J. Exp. Med. 184: 1075-1082.
36. Uzzo, R. G., P. Rayman, V. Kolenko, P. E. Clark, T. Bloom, A. M. Ward, L. Molto, C. Tannenbaum, L. J. Worford, R. Bukowski, et al. 1999. Mechanisms of apoptosis in T cells from patients with renal cell carcinoma. Clin. Cancer Res. 5: 1219-1229.
37. Kume, T., K. Oshima, Y. Yamashita, T. Shirakusa, and M. Kikuchi. 1999. Relationship between Fas-ligand expression on carcinoma cell and cytotoxic T-lymphocyte response in lymphoepithelioma-like cancer of the stomach. Int. J. Cancer 84: 339-343.
38. Koyama, S., N. Koike, and S. Adachi. 2002. Expression of TNF-related apoptosis-inducing ligand (TRAIL) and its receptors in gastric carcinoma and tumor-infiltrating lymphocytes: a possible mechanism of immune evasion of the tumor. J. Cancer Res. Clin. Oncol. 128: 73-79.
39. Wischhusen, J., G. Jung, I. Radovanovic, C. Beier, J. P. Steinbach, A. Rimner, H. Huang, J. B. Schulz, H. Ohgaki, A. Aguzzi, et al. 2002. Identification of CD70-mediated apoptosis of immune effector cells as a novel immune escape pathway of human glioblastoma. Cancer Res. 62: 2592-2599.
40. Zaks, T. Z., D. B. Chappell, S. A. Rosenberg, and N. P. Restifo. 1999. Fas-mediated suicide of tumor-reactive T cells following activation by specific tumor: selective rescue by caspase inhibition. J. Immunol. 162: 3273-3279.
41. Finke, J. H., P. Rayman, R. George, C. S. Tannenbaum, V. Kolenko, R. Uzzo, A. C. Novick, and R. M. Bukowski. 2001. Tumor-induced sensitivity to apoptosis in T cells from patients with renal cell carcinoma: role of nuclear factor-κB suppression. Clin. Cancer Res. 1: 940s-946s.
42. Thornton, M. V., D. Kudo, P. Rayman, C. Horton, L. Molto, M. K. Cathcart, C. Ng, E. Paszkiewicz-Kozik, R. Bukowski, I. Derweesh, et al. 2004. Degradation of NF-κB in T cells by gangliosides expressed on renal cell carcinomas. J. Immunol. 172: 3480-3490.
43. Garcia-Ruiz, C., A. Colell, A. Morales, M. Calvo, C. Enrich, and J. C. Fernandez-Checa. 2002. Trafficking of ganglioside GD3 to mitochondria by tumor necrosis factor-α. J. Biol. Chem. 277: 36443-36448.
44. Zhou, Y. W., Y. Komada, H. Inaba, E. Azuma, and M. Sakurai. 1998. Down-regulation of Fas-associated phosphatase-1 (FAP-1) in interleukin-2- activated T cells. Cell. Immunol. 186: 103-110.
45. Furukawa, K., Y. Arita, N. Satomi, M. Eisinger, and K. O. Lloyd. 1990. Tumor necrosis factor enhances GD3 ganglioside expression in cultured human melanocytes. Arch. Biochem. Biophys. 281: 70-75.
46. Kjaer, T. W., J. Rygaard, K. Bendtzen, K. Josefsen, T. Bock, and K. Buschard. 1992. Interleukins increase surface ganglioside expression of pancreatic islet cells in vitro. APMIS 100: 509-514.
47. Garcia-Ruiz, C., A. Colell, R. Paris, and J. C. Fernandez-Checa. 2000. Direct interaction of GD3 ganglioside with mitochondria generates reactive oxygen species followed by mitochondrial permeability transition, cytochrome c release, and caspase activation. FASEB J. 14: 847-858.
48. Ikemoto, S., N. Yoshida, K. Narita, S. Wada, T. Kishimoto, K. Sugimura, and T. Nakatani. 2003. Role of tumor-associated macrophages in renal cell carcinoma. Oncol. Rep. 10: 1843-1849.
49. Waase, I., M. Bergholz, A. Iglauer, S. Beissert, M. Blech, A. Schauer, and M. Kronke. 1992. Heterogeneity of tumor necrosis factor production in renal cell carcinoma. Eur. J. Cancer 28A: 1660-1664.
50. Gogusev, J., M. Augusti, Y. Chretien, and D. Droz. 1993. Interleukin-6 and TNF α production in human renal cell carcinoma. Kidney Int. 44: 585-592.
51. Zhang, X., and F. L. Kiechle. 2004. Review: glycosphingolipids in health and disease. Ann. Clin. Lab. Sci. 34: 3-13.
52. Yuyama, Y., T. Dohi, H. Morita, K. Furukawa, and M. Oshima. 1995. Enhanced expression of GM2/GD2 synthase mRNA in human gastrointestinal cancer. Cancer 75: 1273-1280.
53. Nakamura, K., M. Koike, K. Shitara, Y. Kuwana, K. Kiuragi, S. Igarashi, M. Hasegawa, and N. Hanai. 1994. Chimeric anti-ganglioside GM2 antibody with antitumor activity. Cancer Res. 54: 1511-1516.
54. Zhang, H., S. Zhang, N. K. Cheung, G. Ragupathi, and P. O. Livingston. 1998. Antibodies against GD2 ganglioside can eradicate syngeneic cancer micrometastases. Cancer Res. 58: 2844-2849.
55. Imai, M., C. Landen, R. Ohta, N. K. Cheung, and S. Tomlinson. 2005. Complement-mediated mechanisms in anti-GD2 monoclonal antibody therapy of murine metastatic cancer. Cancer Res. 65: 10562-10568.
56. D2 in small cell lung cancer cell lines: enhancement of cell proliferation and mediation of apoptosis. Cancer Res. 61: 4244-4252.
57. Irie, R. F., T. Matsuki, and D. L. Morton. 1989. Human monoclonal antibody to ganglioside GM2 for melanoma treatment. Lancet 1: 786-787.
58. Albertini, M. R., J. Gan, P. Jaeger, J. A. Hank, B. Storer, K. Schell, T. Rivest, J. Surfus, R. A. Reisfeld, J. H. Schiller, and P. M. Sondel. 1996. Systemic interleukin-2 modulates the anti-idiotypic response to chimeric anti-GD2 antibody in patients with melanoma. J. Immunother. Emphasis Tumor Immunol. 19: 278-295.