Killing of T lymphocytes by synthetic ceramide is by a nonapoptotic mechanism and is abrogated following mitogenic activation

Experimental Cell Research

Volumn 249, Issue 1, 1999, Pages 116-122

  Mengubas, Kamuran ^a   Fahey, Anne A ^a   Lewin, Jackie ^b   Mehta, Atul B ^a   Hoffbrand, A Victor ^a   Wickremasinghe, R Gitendra ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

Author keywords

Apoptosis; Caspase; Cell cycle; Ceramide; Okadaic acid; T lymphocyte

Indexed keywords

CASPASE; CERAMIDE;

ARTICLE; CELL CYCLE; CYTOTOXICITY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MITOGENESIS; PRIORITY JOURNAL; T LYMPHOCYTE;

EID: 0033602773     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1999.4474     Document Type: Article

References (42)

1. Kerr J. F. R., Winterford C. M., Harmon B. V. Apoptosis: Its significance in cancer and cancer treatment. Cancer. 73:1994;2013-2025.
2. Salvesen G. S., Dixit V. M. Caspases: Intracellular signalling by proteolysis. Cell. 91:1997;443-446.
3. Hannun Y. A. Functions of ceramide in coordinating cellular responses to stress. Science. 274:1996;1855-1859.
4. Haimovitz-Friedman A., Kan C-C., Ehleiter D., Persaud R. S., McLoughlin M., Fuks Z., Kolesnick R. N. Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J. Exp. Med. 180:1994;525-535.
5. Tepper C. G., Jayadev S., Liu B., Bielawska A., Wolff R., Yonehara S., Hannun Y., Seldin M. F. Role for ceramide as an endogenous mediator of Fas-induced cytotoxicity. Proc. Natl. Acad. Sci. USA. 92:1995;8443-8447.
6. Schutze S., Potthoff K., Machleidt T., Berkovic D., Wiegmann K., Kronke M. TNF activates NF-kB by phosphatidylcholine-specific phospholipase c-induced "acidic" sphingomyelin breakdown. Cell. 71:1992;765-776.
7. Jarvis W. D., Kolesnick R. N., Fornari F. A., Traylor R. S., Gewirtz D. A., Grant S. Induction of apoptotic DNA damage and cell death by activation of the sphingomyelin pathway. Proc. Natl. Acad. Sci. USA. 91:1994;73-77.
8. Bose R., Verheij M., Haimovitz-Friedman A., Scotto K., Fuks Z., Kolesnick R. Ceramide synthase mediates daunorubicin-induced apoptosis: An alternative mechanism for generating death signals. Cell. 82:1995;405-414.
9. Obeid L. M., Linardic C. M., Karolak L. A., Hannun Y. A. Programmed cell death induced by ceramide. Science. 259:1993;1769-1771.
10. Chinnaiyan A. M., Tepper C. G., Seldin M. F., O'Rourke K., Kischkel F. C., Hellbardt S., Krammer P. H., Peter M. E., Dixit V. M. FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271:1996;4961-4965.
11. Hofmann K., Dixit V. M. Ceramide in apoptosis - Does it really matter? Trends Biochem. Sci. 23:1998;374-377.
12. Watts J. D., Gu M., Polverino A. J., Patterson S. D., Aebersold R. Fas-induced apoptosis of T cells occurs independently of ceramide generation. Proc. Natl. Acad. Sci. USA. 94:1997;7292-7296.
13. Ashkenazi A., Dixit V. M. Death receptors: Signaling and modulation. Science. 281:1998;1305-1308.
14. Horinouchi K., Erlich S., Perl D. P., Ferlinz K., Bisgaier C. L., Sandhoff K., Desnick R. J., Stewart C. L., Schuchman E. H. Acid sphingomyelinase deficient mice: A model of types A and B Niemann-Pick disease. Nature Genet. 10:1995;288-293.
15. Otterbach B., Stoffel W. Acid sphingomyelinase-deficient mice mimic the neurovisceral form of human lysosomal storage disease. Cell. 81:1995;1053-1061.
16. Santana P., Pena L. A., Haimovitz-Friedman A., Martin S., Green D., McLoughlin M., Cordon-Cardo C., Schuchman E. H., Fuks Z., Kolesnick R. Acid sphingomyelinase-deficient human lymphocytes and mice are defective in radiation-induced apoptosis. Cell. 86:1996;189-199.
17. Wright S. C., Zheng H., Zhong J. Tumor cell resistance to apoptosis due to a defect in the activation of sphingomyelinase and the 24 kDa apoptotic protease (AP24). FASEB J. 10:1996;325-332.
18. Chmura S. J., Nodzenski E., Beckett M. A., Kufe D. W., Quintans J., Weichselbaum R. R. Loss of ceramide production confers resistance to radiation-induced apoptosis. Cancer Res. 57:1997;1270-1275.
19. Michael J. M., Lavin M. F., Watters D. J. Resistance to radiation-induced apoptosis in Burkitt's lymphoma cells is associated with defective ceramide signaling. Cancer Res. 57:1997;3600-3605.
20. Haimovitz-Friedman A., Kolesnick R. N., Fuks Z. Ceramide signaling in apoptosis. Br. Med. Bull. 53:1997;539-553.
21. Mire-Sluis A. R., Wickremasinghe R. G., Hoffbrand A. V., Timms A. M., Francis G. E. Human T lymphocytes stimulated by polyclonal mitogens undergo a single round of cell division without a requirement for interleukin 2 or accessory cells. Immunology. 60:1987;7-12.
22. Cotter T. G., Martin S. J. Techniques in Apoptosis: A User's Guide. 1996;Portland Press, London.
23. Datta R., Banach D., Kojima H., Talanian R. V., Alnemri E. S., Wong W. W., Kufe D. W. Blood. 88:1996;1936-1943.
24. Swain S. L., Croft M., Dubey C., Haynes L., Rogers P., Zhang X., Bradley L. M. From naive to memory T cells. Immunol. Rev. 150:1996;143-167.
25. Fernandez-Sanchez M-T., Garcia-Rodriguez A., Diaz-Trelles R., Novelli A. Inhibition of protein phosphatases induces IGF-1-blocked, neurotrophin-insensitive neuronal apoptosis. FEBS Lett. 398:1996;106-112.
26. McCarthy N. J., Whyte M. K. B., Gilbert C. S., Evan G. I. Inhibition of Ced-3/ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage or the bcl-2 homologue Bak. J. Cell Biol. 136:1997;215-227.
27. Mengubas K., Riordan F. A., Bravery C. A., Lewin J., Owens D. L., Mehta A. B., Hoffbrand A. V., Wickremasinghe R. G. Ceramide-induced killing of normal and malignant human lymphocytes is by a non-apoptotic mechanism. Oncogene. 1999.
28. Leist M., Single B., Castoldi A. F., Kuhnle S., Nicotera P. Intracellular adenosine triphosphate (ATP) concentration: A switch in the decision between apoptosis and necrosis. J. Exp. Med. 185:1997;1481-1486.
29. Zhang Y., Yao B., Delikat S., Bayoumy S., Lin X-H., Basu S., McGinley M., Chan-Hui P-Y., Lichenstein H., Kolesnick R. Kinase suppressor of ras is ceramide-activated protein kinase. Cell. 89:1997;63-72.
30. Wolff R. A., Dobrowsky R. T., Bielawska A., Obeid L. M., Hannun Y. A. Role of ceramide-activated protein phosphatase in ceramide-mediated signal transduction. J. Biol. Chem. 269:1994;19605-19609.
31. Sawai H., Okazaki T., Yamamoto H., Okano H., Takeda Y., Toshima M., Sawada H., Okuma M., Ishikura H., Umehara H., Domae N. J. Biol. Chem. 270:1995;27326-27331.
32. Westwick J. K., Bielawska A. E., Dbaibo G., Hannun Y. A., Brenner D. A. Ceramide activates the stress-activated protein kinases. J. Biol. Chem. 270:1995;22689-22692.
33. Verheij M., Bose R., Lin X. H., Jarvis W. D., Grant S., Birrer M. J., Szabo E., Zon L. I., Kyriakis J. M., Haimovitz-Friedman A., Fuks Z., Kolesnick R. N. Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature. 380:1996;75-79.
34. Ohmori M., Shirasawa S., Furuse M., Okumura K., Sasazuki T. Activated Ki-ras enhances sensitivity of ceramide-induced apoptosis without c-Jun NH2-terminal kinase/stress-activated protein kinase or extracellular signal-regulated kinase activation in human colon cancer cells. Cancer Res. 57:1997;4714-4717.
35. Susin S. A., Zamzami N., Larochette N., Dallaporta B., Marzo I., Brenner C., Hirsch T., Petit P. X., Geuskens M., Kroemer G. A cytofluorometric assay of nuclear apoptosis in a cell-free system: Application to ceramide-induced apoptosis. Exp. Cell Res. 36:1997;397-403.
36. Zamzami N., Susin S. A., Marchetti P., Hirsch T., Gomez-Monterrey I., Castedo M., Kroemer G. Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183:1996;1533-1544.
37. Shimizu S., Eguchi Y., Kamiike W., Waguri S., Uchiyama Y., Matsuda H., Tsujimoto Y. Retardation of chemical hypoxia-induced necrotic cell death by bcl-2 and ICE inhibitors: Possible involvement of common mediators in apoptotic and necrotic signal transductions. Oncogene. 12:1996;2045-2050.
38. Majno G., Joris I. Apoptosis, oncosis and necrosis: An overview of cell death. Am. J. Pathol. 146:1995;3-15.
39. Fiers W., Beyaert R., Boone E., Comelis S., Declerq W., Decoster E., Denecke G., Depuydt B., DeValck D., deWilde G., Goossens V., Grooten J., Haegeman G., Heyninck K., Penning L., Plaisance S., Vancompemolle K., Van Criekinge W., Vandenabeele P., Vanden Berghe W., Van de Craen M., Vandevoorde V., Vercammen D. TNF-induced intracellular signaling leading to gene induction or to cytotoxicity by necrosis or by apoptosis. J. Inflam. 47:1995;67-75.
40. Vercammen D., Beyaert R., Denecker G., Goossens V., Van Loo G., Declerq W., Grooten J., Fiers W., Vandenabeele P. Inhibition of caspases increases the sensitivity of L929 cells to necrosis mediated by tumor necrosis factor. J. Exp. Med. 187:1998;1477-1485.
41. Vercammen D., Brouckaert G., Denecker G., Van de Craen M., Declerq W., Fiers W., Vandenabeele P. Dual control of the Fas receptor: Initiation of both apoptotic and necrotic cell death pathways. J. Exp. Med. 188:1998;919-930.
42. Kawahara A., Ohsawa Y., Matsumura H., Uchiyama Y., Nagata S. Caspase-independent cell killing by Fas-associated protein with death domain. J. Cell Biol. 143:1998;1353-1360.