Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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Roles of Neutral Sphingomyelinase 1 on CD95-Mediated Apoptosis in Human Jurkat T Lymphocytes

  • Received : 2010.05.24
  • Accepted : 2010.06.22
  • Published : 2010.07.31
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Abstract

CD95 receptor is a member of tumor necrosis factor receptor family that mediates apoptosis in many cell types when bound by CD95 ligand or cross-linked by agonistic anti-CD95 antibodies. To determine the role of neutral sphingomyelinase (nSMase) on CD95-mediatd apoptosis, human Jurkat T lymphocytes were exposed to recombinant human CD95 ligand. Treatment with CD95 ligand induced cell death in a concentration and time-dependent manner. CD95-induced cell death was suppressed by inhibitors of SMase such as AY9944 or desipramine. Transfection with human nSMase1 siRNA plasmid into CD95 ligand-treated cells significantly prevented CD95-mediated cell death. CD95-mediated elevation of intracellular ceramide level detected by FACS analysis with anti-ceramide antibody was also decreased by nSMase1 siRNA. Knock-down of nSMase1 expression also blocked cytochrome c release into cytosol and caspase-3 cleavage in CD95-treated cells. Taken together, these results suggest that nSMase1 may play an important role in CD95-mediated apoptotic cell death in Jurkat T cells.

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References

  1. Bezombes, C., Segui, B., Cuvillier, O., Bruno, A. P., Uro-Coste,E., Gouaze, V., Andrieu-Abadie, N., Carpentier, S., Laurent,G., Salvayre, R., Jaffrezou, J. P. and Levade, T. (2001).Lysosomal sphingomyelinase is not solicited for apoptosis signaling. FASEB J. 15, 297-299. https://doi.org/10.1096/fj.00-0466fje
  2. Brady, R. O., Kanfer, J. N., Mock, M. N. and Fredrickson, D. S.(1966). The metabolism of sphingomyelin II. Evidence of an enzymatic deficiency in Niemann-Pick disease. Proc. Natl. Acad. Sci. U S A 55, 366-369. https://doi.org/10.1073/pnas.55.2.366
  3. Chalfant, C. E., Ogretmen, B., GalaDari, S., Kroesen, B. J.,Pettus, B. J. and Hannun, Y. A. (2001). Fas activation induces dephosphorylation of SR proteins: dependence on the de novo generation of ceramide and activation of protein phosphatase 1. J. Biol. Chem. 276, 44848-44855. https://doi.org/10.1074/jbc.M106291200
  4. Chiba, T., Takahashi, S., Sato, N., Ishii, S. and Kikuchi, K.(1996). Fas-mediated apoptosis is modulated by intracellular glutathione in human T cells. Eur. J. Immunol. 26, 1164-1169. https://doi.org/10.1002/eji.1830260530
  5. Clarke, C. J. and Hannun, Y. A. (2006). Neutral sphingomyelinases and nSMase2: Bridging the gaps. Biochim. Biophys. Acta.1758, 1893-1901. https://doi.org/10.1016/j.bbamem.2006.06.025
  6. Clarke, C. J., Snook, C. F., Tani, M., Matmati, N., Marchesini, N.and Hannun, Y. A. (2006). The extended family of neutral sphingomyelinases. Biochemistry 45,11247-11256. https://doi.org/10.1021/bi061307z
  7. Cock, J. G., Tepper, A. D., de Vries, E., van Blitterswijk, W. and Borst, J. (1998). CD95(Fas/Apo-1) induces ceramide formation and apoptosis in the absence of a functional acid sphingomyelinase. J. Biol. Chem. 273, 7560-7565. https://doi.org/10.1074/jbc.273.13.7560
  8. Cremesti, A., Paris, F., Grassmé, H., Holler, N., Tschopp, J.,Fuks, Z., Gulbins, E. and Kolesnick, R. (2001). Ceramide enables fas to cap and kill. J. Biol. Chem. 276, 23954-23961. https://doi.org/10.1074/jbc.M101866200
  9. De Maria, R., Rippo, M. R., Schuchman, E. H. and Testi, R.(1998). Acidic sphingomyelinase (ASM) is necessary for Fas-induced GD3 ganglioside accumulation and efficient apoptosis of lymphoid cells. J. Exp. Med. 187, 897-902. https://doi.org/10.1084/jem.187.6.897
  10. Grassme, H., Jekle, A., Riehle, A., Schwarz, H., Berger, J.,Sandhoff, K., Kolesnick, R. and Gulbins, E. (2001). CD95 signaling via ceramide-rich membrane rafts. J. Biol. Chem.276, 20589-20596. https://doi.org/10.1074/jbc.M101207200
  11. Hannun, Y. A. and Luberto, C. (2000). Ceramide in the eukaryotic stress response. Trends Cell Biol. 10, 73-80. https://doi.org/10.1016/S0962-8924(99)01694-3
  12. Hirofumi, S., Naochika, D., Narasimhan, N. and Hannun, Y. A.(1999). Function of the cloned putative neutral sphingomyelinase as lyso-platelet activating factor-phospholipase C.J. Biol. Chem. 274, 38131-38139. https://doi.org/10.1074/jbc.274.53.38131
  13. Hofmann, K., Tomiuk, S., Wolff, G. and Stoffel, W. (2000).Cloning and characterization of the mammalian brainspecific, $Mg^{2+}$-dependent neutral sphingomyelinase. Proc. Natl. Acad. Sci. U S A 97, 5895-5900. https://doi.org/10.1073/pnas.97.11.5895
  14. Horinouchi, K., Erlich, S., Perl, D. P., Ferlinz, K., Bisgaier, C. L.,Sandhoff, K., Desnick, R. J., Stewart, C. L. and Schuchman,E. H. (1995). Acid sphingomyelinase deficient mice: A model of types A and B Niemann-Pick disease. Nat. Genet. 10, 288-293. https://doi.org/10.1038/ng0795-288
  15. Inna, L., Alexander, G. and Peter, H. K. (2005). Death receptor signaling. J. Cell. Sci. 118, 265-267. https://doi.org/10.1242/jcs.01610
  16. Jarvis, W. D. and Grant, S. (1998). The role of ceramide in the cellular response to cytotoxic agent. Curr. Opin. Oncol. 10,552-559. https://doi.org/10.1097/00001622-199811000-00013
  17. Kirschnek, S., Paris, F., Wellwe, M., Grassme, H., Ferliz, K.,Riehle, A., Fuks, Z., Kolesnick, R. and Gulbins, E. (2000).CD95-mediated apoptosis in vivo involves acid sphingomyelinase.J. Biol. Chem. 275, 27316-27323.
  18. Kondo, T., Kitano, T., Iwai, K., Watanabe, M., Taguchi, Y., Yabu,T., Umehara, H., Domae, N., Uchiyama, T. and Okazaki, T.(2002). Control of ceramide-induced apoptosis by IGF-1: involvement of PI-3 kinase, caspase-3 and catalase. Cell Death Differ. 9, 682-692. https://doi.org/10.1038/sj.cdd.4401019
  19. Krut, O., Wiegmann, K., Kashkar, H., Yazdanpanah, B. andKrönke, M. (2006). Novel tumor necrosis factor-responsive mammalian neutral sphingomyelinase-3 is a C-tail-anchored protein. J. Biol. Chem. 281, 13784-13793. https://doi.org/10.1074/jbc.M511306200
  20. Lin, T., Genestier, L., Pinkoski, M. J., Castro, A., Nicholas, S.,Mogil, R., Paris, F., Fuks, Z., Schuchman, E. H., Kolesnick,R. N. and Green, D. R. (2000). Role of acidic sphingomyelinase in Fas/CD95-mediated cell death. J. Biol. Chem. 275, 8657-8663. https://doi.org/10.1074/jbc.275.12.8657
  21. Liu, B., Andrieu-Abadie, N., Levade, T., Zhang, P., Obeid, L. M.and Hannun, Y. A. (1998a). Glutathione regulation of neutral sphingomyelinase in tumor necrosis factor-alpha-induced cell death. J. Biol. Chem. 273, 11313-11320. https://doi.org/10.1074/jbc.273.18.11313
  22. Liu, B. and Hannun, Y. A. (1997). Inhibition of the neutral magnesium-dependent sphingomyelinase by glutathione. J. Biol. Chem. 272, 16281-16287. https://doi.org/10.1074/jbc.272.26.16281
  23. Liu, B., Hassler, D. F., Smith, G. K., Weaver, K. and Hannun, Y. A. (1998b). Purification and characterization of a membrane bound neutral pH optimum magnesium-dependent and phosphatidylserine-stimulated sphingomyelinase from rat brain. J. Biol. Chem. 273, 34472-34479. https://doi.org/10.1074/jbc.273.51.34472
  24. Marchesini, N., Luberto, C. and Hannun, Y. A. (2003). Biochemical properties of mammalian neutral sphingomyelinase 2 and its role in sphingolipid metabolism. J. Biol. Chem. 278,13775-13783. https://doi.org/10.1074/jbc.M212262200
  25. Martin, S. F., Sawai, H., Villalba, J. M. and Hannun, Y. A.(2007). Redox regulation of neutral sphingomyelinase-1 activity in HEK293 cells through a GSH-dependent mechanism.Arch. Biochem. Biophys. 459, 295-300. https://doi.org/10.1016/j.abb.2006.11.007
  26. Martin, S. J., Newmeyer, D. D., Mathias, S., Farschon, D. M.,Wang, H. G., Reed, J. C., Kolesnick, R. N. and Green, D. R.(1995). Cell-free reconstitution of Fas-, UV radiation-, and ceramide-induced apoptosis. EMBO J. 14, 5191-5200.
  27. Mitsumasa, W., Toshiyuki, K., Tadakazu, K., Takeshi, Y., Yoshimitsu,T., Masaro, T., Hisanori, U., Naochika, D., Takashi, U.and Toshiro, O. (2004). Increase of nuclear ceramide through caspase-3-dependent regulation of "sphingomyelin cycle" in Fas-induced apoptosis. Cancer Res. 64, 1000-1007. https://doi.org/10.1158/0008-5472.CAN-03-1383
  28. Miyaji, M., Jin, Z. X., Yamaoka, S., Amakawa, R., Fukuhara, S.,Sato, S. B., Kobayashi, T., Domae, N., Mimori, T., Bloom, E.T., Okazaki, T. and Umehara, H. (2005). Role of membrane sphingomyelin and ceramide in platform formation for Fas-mediated apoptosis. J. Exp. Med. 202, 249-259. https://doi.org/10.1084/jem.20041685
  29. Neuberger, Y., Shogomori, H., Levy, Z., Fainzilber, M. andFuterman, A. H. (2000). A lyso-platelet activating factor phospholipase C, originally suggested to be a neutral-sphingomyelinase, is located in the endoplasmic reticulum. FEBS Lett. 469, 44-46. https://doi.org/10.1016/S0014-5793(00)01235-7
  30. Nieves, E., Pilar, F. V., Salvador, A., Eduardo, L. C. and Juan,C. L. (2000). Apoptosis induced by rac GTPase correlates with induction of FasL and ceramides production. Mol. Biol. Cell 11, 4347-4358. https://doi.org/10.1091/mbc.11.12.4347
  31. Norma, M., Chiara, L. and Hannun, Y. A. (2003) Biochemical properties of mammalian neutral sphingomyelinase2 and its role in sphingolipid metabolism. J. Biol. Chem. 278, 13775-13783. https://doi.org/10.1074/jbc.M212262200
  32. Norma, M., Walid, O., Jacek, B., Chiara, L., Lina, M. O. andHannun, Y. A. (2004). Role of mammalian neutral sphingomyelinase 2 in confluence-induced growth arrest of MCF7 cells. J. Biol. Chem. 279, 25101-25111. https://doi.org/10.1074/jbc.M313662200
  33. Obeid, L. M. and Hannun, Y. A. (1995). Ceramide: a stress signal and mediator of growth suppression and apoptosis. J. Biol. Chem. 258, 191-198.
  34. Ogasawara, J., Watanabe-Fukunaga, R., Adachi, M., Matsuzawa,A., Kasugai, T., Kitamura, Y., Itoh, N., Suda, T. andNagata, S. (1993). Lethal effect of the anti-Fas antibody in mice. Nature 364, 806-809. https://doi.org/10.1038/364806a0
  35. Oliver, C., Lisa, E. and Sarah, S. (2000). Involvement of sphingosin in mitochondria-dependent Fas-induced apoptosis of type II Jurkat T cells. J. Biol. Chem. 275, 15691-15700. https://doi.org/10.1074/jbc.M000280200
  36. Paris, F., Grassmé, H., Cremesti, A., Zager, J., Fong, Y., Haimovitz-Friedman, A., Fuks, Z., Gulbins, E. and Kolesnick, R. (2000).Natural ceramide reverses Fas resistance of acid sphingomyelinase-/- hepatocytes. J. Biol. Chem. 276, 8297-8305. https://doi.org/10.1074/jbc.M008732200
  37. Ram, K., ManLin, J., Maria-A, G. and David, R, H. (2004).Ceramide-induced apoptosis: role of catalase and hepatocyte growth factor. Free Radical Biol. Med. 37, 166-175. https://doi.org/10.1016/j.freeradbiomed.2004.04.011
  38. Reinehr, R., Becker, S., Eberle, A., Grether-Beck, S. and Häussinger,D. (2005). Involvement of NADPH oxidase isoforms and src family kinases in CD95-dependent hepatocyte apoptosis. J. Biol. Chem. 280, 27179-27194. https://doi.org/10.1074/jbc.M414361200
  39. Sawada, M., Kiyono, T., Nakashima, S., Shinoda, J., Naganawa,T., Hara, S., Iwama, T. and Sakai, N. (2004). Molecular mechanisms of TNF-α-induced ceramide formation in human glioma cells: p53-mediated oxidant stress-dependent and -independent pathways. Cell Death Differ. 11, 997-1008. https://doi.org/10.1038/sj.cdd.4401438
  40. Sawai, H., Domae, N., Nagan, N. and Hannun, Y. A. (1999).Function of the cloned putative neutral sphingomyelinase as lyso-platelet activating factor-phospholipase C. J. Biol. Chem.274, 38131-38139. https://doi.org/10.1074/jbc.274.53.38131
  41. Schneider, P. B. and Kennedy, E. P. (1967). Sphingomyelinase in normal human spleens and in spleens from subjects with Niemann-Pick disease. J. Lipid Res. 8, 202-209.
  42. Segui, B., Bezombes, C., Uro-Coste, E., Medin, J. A., Andrieu-Abadie, N., Auge, N., Brouchet, A., Laurent, G., Salvayre, R.,Jaffrezou, J. P. and Levade, T. (2000). Stress-induced apoptosis is not mediated by endolysosomal ceramide. FASEB J.14, 36-47. https://doi.org/10.1096/fasebj.14.1.36
  43. Spiegel, S. and Merrill, A. H. Jr. (1996). Sphingolipid metabolism and cell growth regulation. FASEB J. 10, 1388-1397. https://doi.org/10.1096/fasebj.10.12.8903509
  44. Stoffel, W., Jenke, B., Holz, B., Binczek, E., Günter, R. H.,Knifka, J., Koebke, J. and Niehoff, A. (2007). Neutral sphingomyelinase (SMPD3) deficiency causes a novel form of chondrodysplasia and dwarfism that is rescued by Col2A1- driven smpd3 transgene expression. Am. J. Pathol.171, 153-161. https://doi.org/10.2353/ajpath.2007.061285
  45. Tepper, A. D., Ruurs, P., Borst, J. and van Blitterswijk, W. J.(2001). Effect of overexpression of a neutral sphingomyelinase on CD95-induced ceramide production and apoptosis. Biochem. Biophys. Res. Commun. 280, 634-639. https://doi.org/10.1006/bbrc.2000.4166
  46. Tomiuk, S., Hofmann, K., Nix, M., Zumbansen, M. and Stoffel,W. (1998). Cloned mammalian neutral sphingomyelinase: functions in sphingolipid signaling? Proc. Natl. Acad. Sci. U S A 95, 3638-3643. https://doi.org/10.1073/pnas.95.7.3638
  47. Tomiuk, S., Zumbansen, M. and Stoffel, W. (2000). Characterization and subcellular localization of murine and human magnesium-dependent neutral sphingomyelinase. J. Biol. Chem. 275, 5710-5717. https://doi.org/10.1074/jbc.275.8.5710
  48. Tonnetti, L., Veri, M. C., Bonvini, E. and D’Adamio, L. (1999). A role for neutral sphingomyelinase-mediated ceramide production in T cell receptor-induced apoptosis and mitogenactivated protein kinase-mediated signal transduction. J.Exp. Med. 189, 1581-1589. https://doi.org/10.1084/jem.189.10.1581
  49. van den Dobbelsteen, D. J., Nobel, C. S. I., Schlegel, J.,Cotgreave, I. A., Orrenius, S. and Slater, A. F. G. (1996).Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/Apo-1 antibody. J. Biol. Chem.271, 15420-15427. https://doi.org/10.1074/jbc.271.26.15420
  50. Watanabe, M., Kitano, T., Kondo, T., Yabu, T., Taguchi, Y.,Tashima, M., Umehara, H., Domae, N., Uchiyama, T. andOkazaki, T. (2004). Increase of nuclear ceramide through caspase-3-dependent regulation of the "sphingomyelin cycle" in Fas-induced apoptosis. Cancer Res. 64, 1000-1007. https://doi.org/10.1158/0008-5472.CAN-03-1383
  51. Yabu, T., Imamura, S., Yamashita, M. and Okazaki, T. (2008).Identification of $Mg^{2+}$-dependent neutral sphingomyelinase 1 as a mediator of heat stress-induced ceramide generation and apoptosis. J. Biol. Chem. 280, 29971-29982.
  52. Yoshida, Y., Arimoto, K., Sato, M., Sakuragawa, N., Arima, M. and Satoyoshi, E. (1985). Reduction of acid sphingomyelinase activity in human fibroblasts induced by AY-9944 and other cationic amphiphific drugs. J. Biochem. 98, 1669-1679. https://doi.org/10.1093/oxfordjournals.jbchem.a135438
  53. Zhou, Q., Band, M. R., Hernandez, A., Liu, Z. L. and Kummerow, F. A. (2004). 27-Hydroxycholesterol inhibits neutral sphingomyelinase in cultured human endothelial cells. Life Sci. 75, 1567-1577. https://doi.org/10.1016/j.lfs.2004.05.004

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