Elevated levels of select gangliosides in T cells from renal cell carcinoma patients is associated with T cell dysfunction

Journal of Immunology

Volumn 183, Issue 8, 2009, Pages 5050-5058

  Biswas, Soumika ^a   Biswas, Kaushik ^a   Richmond, Amy ^a   Ko, Jennifer ^a   Ghosh, Sankar ^a   Simmons, Matthew ^b   Rayman, Patricia ^a   Rini, Brian ^b   Gill, Inderbir ^c   Tannenbaum, Charles S ^a   Finke, James H ^a,b  

^a LERNER RESEARCH INSTITUTE   (United States)

^b TAUSSIG CANCER INSTITUTE   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; GANGLIOSIDE; GANGLIOSIDE GD 1A; GANGLIOSIDE GD2; GANGLIOSIDE GD3; GANGLIOSIDE GM2; MESSENGER RNA; REACTIVE OXYGEN METABOLITE; SYNTHETASE;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER PATIENT; CONTROLLED STUDY; DISEASE ASSOCIATION; ENZYME ACTIVATION; HUMAN; HUMAN CELL; HUMAN TISSUE; KIDNEY CARCINOMA; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SUPERNATANT; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION;

APOPTOSIS; CARCINOMA, RENAL CELL; CASPASES; CELL LINE, TUMOR; GANGLIOSIDES; GANGLIOSIDOSES, GM2; HUMANS; KIDNEY NEOPLASMS; REACTIVE OXYGEN SPECIES; T-LYMPHOCYTES;

EID: 77954134113     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900259     Document Type: Article

References (40)

1. 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.
2. 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.
3. Maggard, M., L. Meng, B. Ke, R. Allen, L. Devgan, and D. K. Imagawa. 2001. Antisense TGF-β2 immunotherapy for hepatocellular carcinoma: treatment in a rat tumor model. Ann. Surg. Oncol. 8: 32-37.
4. Whiteside, T. L., and H. Rabinowich. 1998. The role of Fas/FasL in immunosuppression induced by human tumors. Cancer Immunol. Immunother. 46: 175-184.
5. 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.
6. 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.
7. Das, T., G. Sa, C. Hilston, D. Kudo, P. Rayman, K. Biswas, L. Molto, R. Bukowski, B. Rini, J. H. Finke, and C. Tannenbaum. 2008. GM1 and tumor necrosis factor-α, overexpressed in renal cell carcinoma, synergize to induce T-cell apoptosis. Cancer Res. 68: 2014-2023.
8. Gastman, B. R., D. E. Johnson, T. L. Whiteside, and H. Rabinowich. 2000. Tumor-induced apoptosis of T lymphocytes: elucidation of intracellular apoptotic events. Blood 95: 2015-2023.
9. Chahlavi, A., P. Rayman, A. L. Richmond, K. Biswas, R. Zhang, M. Vogelbaum, C. Tannenbaum, G. Barnett, and J. H. Finke. 2005. Glioblastomas induce Tlymphocyte death by two distinct pathways involving gangliosides and CD70. Cancer Res. 65: 5428-5438.
10. Dong, H., S. E. Strome, D. R. Salomao, H. Tamura, F. Hirano, D. B. Flies, P. C. Roche, J. Lu, G. Zhu, K. Tamada, et al. 2002. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat. Med. 8: 793-800.
11. Curiel, T. J. 2007. Tregs and rethinking cancer immunotherapy. J. Clin. Invest. 117: 1167-1174.
12. Zea, A. H., P. C. Rodriguez, M. B. Atkins, C. Hernandez, S. Signoretti, J. Zabaleta, D. McDermott, D. Quiceno, A. Youmans, A. O'Neill, et al. 2005. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res. 65: 3044-3048.
13. Gabrilovich, D. 2004. Mechanisms and functional significance of tumour-induced dendritic-cell defects. Nat. Rev. Immunol. 4: 941-952. (Pubitemid 39620069)
14. Ko, J. S., A. H. Zea, B. I. Rini, J. L. Ireland, P. Elson, P. Cohen, A. Golshayan, P. A. Rayman, L. Wood, J. Garcia, et al. 2009. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin. Cancer Res. 15: 2148-2157.
15. Ritter, G., and P. O. Livingston. 1991. Ganglioside antigens expressed by human cancer cells. Semin. Cancer Biol. 2: 401-409.
16. Ladisch, S., and Z. L. Wu. 1985. Detection of a tumour-associated ganglioside in plasma of patients with neuroblastoma. Lancet 1: 136-138.
17. 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. (Pubitemid 24350855)
18. Satoh, M., K. Handa, S. Saito, S. Tokuyama, A. Ito, N. Miyao, S. Orikasa, and S. Hakomori. 1996. Disialosyl galactosylgloboside as an adhesion molecule expressed on renal cell carcinoma and its relationship to metastatic potential. Cancer Res. 56: 1932-1938.
19. Ladisch, S., H. Becker, and L. Ulsh. 1992. Immunosuppression by human gangliosides: I. Relationship of carbohydrate structure to the inhibition of T cell responses. Biochim. Biophys. Acta 1125: 180-188.
20. Peguet-Navarro, J., M. Sportouch, I. Popa, O. Berthier, D. Schmitt, and J. Portoukalian. 2003. Gangliosides from human melanoma tumors impair dendritic cell differentiation from monocytes and induce their apoptosis. J. Immunol. 170: 3488-3494.
21. Dumontet, C., A. Rebbaa, J. Bienvenu, and J. Portoukalian. 1994. Inhibition of immune cell proliferation and cytokine production by lipoprotein-bound gangliosides. Cancer Immunol. Immunother. 38: 311-316.
22. Irani, D. N., K. I. Lin, and D. E. Griffin. 1996. Brain-derived gangliosides regulate the cytokine production and proliferation of activated T cells. J. Immunol. 157: 4333-4340. (Pubitemid 126449350)
23. 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.
24. 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.
25. 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.
26. Livingston, P. O., G. Y. Wong, S. Adluri, Y. Tao, M. Padavan, R. Parente, C. Hanlon, M. J. Calves, F. Helling, G. Ritter, et al. 1994. Improved survival in stage III melanoma patients with GM2 antibodies: a randomized trial of adjuvant vaccination with GM2 ganglioside. J. Clin. Oncol. 12: 1036-1044.
27. 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.
28. Ravindranath, M. H., S. Muthugounder, N. Presser, S. R. Selvan, J. Portoukalian, S. Brosman, and D. L. Morton. 2004. Gangliosides of organ-confined versus metastatic androgen-receptor-negative prostate cancer. Biochem. Biophys. Res. Commun. 324: 154-165.
29. Tsuchida, T., R. E. Saxton, and R. F. Irie. 1987. Gangliosides of human melanoma: GM2 and tumorigenicity. J. Natl. Cancer Inst. 78: 55-60. (Pubitemid 17009770)
30. Ito, A., S. B. Levery, S. Saito, M. Satoh, and S. Hakomori. 2001. A novel ganglioside isolated from renal cell carcinoma. J. Biol. Chem. 276: 16695-16703.
31. Ruan, S., B. K. Raj, and K. O. Lloyd. 1999. Relationship of glycosyltransferases and mRNA levels to ganglioside expression in neuroblastoma and melanoma cells. J Neurochem. 72: 514-521.
32. McKallip, R., R. Li, and S. Ladisch. 1999. Tumor gangliosides inhibit the tumor-specific immune response. J. Immunol. 163: 3718-3726. (Pubitemid 29450894)
33. Shurin, G. V., M. R. Shurin, S. Bykovskaia, J. Shogan, M. T. Lotze, and E. M. Barksdale, Jr. 2001. Neuroblastoma-derived gangliosides inhibit dendritic cell generation and function. Cancer Res. 61: 363-369.
34. Molotkovskaya, I. M., R. V. Kholodenko, N. A. Zelenova, A. M. Sapozhnikov, I. I. Mikhalev, and J. G. Molotkovsky. 2000. Gangliosides induce cell apoptosis in the cytotoxic line CTLL-2, but not in the promyelocyte leukemia cell line HL-60. Membr. Cell Biol. 13: 811-822.
35. Zhang, S., C. Cordon-Cardo, H. S. Zhang, V. E. Reuter, S. Adluri, W. B. Hamilton, K. O. Lloyd, and P. O. Livingston. 1997. Selection of tumor antigens as targets for immune attack using immunohistochemistry: I. Focus on gangliosides. Int. J. Cancer. 73: 42-49. (Pubitemid 27445989)
36. Ravindranath, M. H., E. C. Hsueh, M. Verma, W. Ye, and D. L. Morton. 2003. Serum total ganglioside level correlates with clinical course in melanoma patients after immunotherapy with therapeutic cancer vaccine. J. Immunother. 26: 277-285.
37. Sa, G., T. Das, C. Moon, C. M. Hilston, P. A. Rayman, B. I. Rini, C. S. Tannenbaum, and J. H. Finke. 2009. GD3, an overexpressed tumor-derived ganglioside, mediates the apoptosis of activated but not resting T cells. Cancer Res. 69: 3095-3104.
38. Gastman, B. R., Y. Atarshi, T. E. Reichert, T. Saito, L. Balkir, H. Rabinowich, and T. L. Whiteside. 1999. Fas ligand is expressed on human squamous cell carcinomas of the head and neck, and it promotes apoptosis of T lymphocytes. Cancer Res. 59: 5356-5364.
39. 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.
40. Ye, J. N., T. G. Gu, L. A. Xia, M. J. Murphy, Jr., W. Lee, N. H. Gao, J. R. Gu, and J. P. Fuhrer. 1990. Enhanced expression of ganglioside GD3 in human and rat hepatocellular carcinoma cells and NIH 3T3 cells transfected with human tumor DNAs. Cancer Res. 50: 7697-7702.