Cytokine response modifier A (CrmA) inhibits ceramide formation in response to tumor necrosis factor (TNF)-α: CrmA and Bcl-2 target distinct components in the apoptotic pathway

Journal of Experimental Medicine

Volumn 185, Issue 3, 1997, Pages 481-490

  Dbaibo, Ghassan S ^a   Perry, David K ^a,b   Gamard, Chris J ^a,b   Platt, Rheanna ^a,b   Poirier, Guy G ^c   Obeid, Lina M ^a   Hannun, Yusuf A ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITÉ LAVAL   (Canada)

^c Box 3355 ^*

Author keywords

[No Author keywords available]

Indexed keywords

CERAMIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CANCER CELL CULTURE; CELL DEATH; CONTROLLED STUDY; CYTOKINE RESPONSIVE ELEMENT; GENE TARGETING; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

APOPTOSIS; CERAMIDES; HUMANS; NF-KAPPA B; POLY(ADP-RIBOSE) POLYMERASES; PROTO-ONCOGENE PROTEINS C-BCL-2; SERPINS; TUMOR CELLS, CULTURED; TUMOR NECROSIS FACTOR-ALPHA; VIRAL PROTEINS;

EID: 0031041448     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.185.3.481     Document Type: Article

References (63)

1. Arends, M.J., and A.H. Wyllie. 1991. Apoptosis: mechanisms and roles in pathology. Int. Rev. Exp. Pathol. 32:223-254.
2. Yuan, J., S. Shaham, S. Ledoux, H.M. Ellis, and H.R. Horvitz. 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-con verting enzyme. Cell. 75:641-652.
3. Miura, M., H. Zhu, R. Rotello, E.A. Hartwieg, and J. Yuan. 1993. Induction of apoptosis in fibroblasts by IL-1β converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell. 75:653-660.
4. Tewari, M., and V.M. Dixit. 1995. Fas- and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus crmA gene product. J. BioL Chem. 270:3255-3260.
5. Los, M., M. Van de Craen, L.C. Penning, H. Schenk, M. Westendorp, P.A. Baeuerle, W. Droge, P.H. Krammer, W. Fiers, and K. Schulze-Osthoff. 1995. Requirement of an ICE/ CED-3 protease for Fas/APO-1-mediated apoptosis. Nature (Leond.). 375:81-83.
6. Tewan, M., L.T. Quan, K. O'Rourke, S. Desnoyers, Z. Zeng, D.R. Beidler, G.G. Poirier. G.S. Salvesen, and V.M. Dixit. 1995. Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell. 81:801-809.
7. Nicholson, D.W., A. Ali, N.A. Thornberry, J.P. Vaillancourt, C.K. Ding, M. Gallant, Y. Gareau, P.R. Griffin, M. Labelle, Y.A. Lazebnik et al. 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature (Lond.). 376:37-43.
8. Schlegel, J., I. Peters, S. Orrenius, D.K. Miller, N.A. Thornberry, T. Yamin, and D.W. Nicholson. 1996. CPP32/Apopain is a key Interleukin 1 β converting enzyme-like protease involved in Fas-mediated apoptosis. J. Biol. Chem. 271:1841-1844.
9. Kaufmann, S.H., S. Desnoyers, Y. Ottaviano, N.E. Davidson, and G.G. Poirier. 1993. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 53:3976-3985.
10. Lazebnik, Y.A., S.H. Kaufmann, S. Desnoyers, G.G. Poirier, and W.C. Earnshaw. 1994. Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature (Lond.). 371:346-347.
11. Casciola-Rosen, L.A., D.K. Miller, G.J. Anhalt, and A. Rosen. 1994. Specific cleavage of the 70-kDa protein component of the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptotic cell death. J. Biol. Chem. 269: 30757-30760.
12. Martin, S.J., and D.R. Green. 1995. Protease activation during apoptosis: death by a thousand cuts? Cell. 82:349-352.
13. Fernandes-Alnemri, T., G. Litwack, and E.S. Alnemri. 1994. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1 β-convertmg enzyme. J. Biol. Chem. 269: 30761-30764.
14. Duan, H., A.M. Chinnaiyan, P.L. Hudson, J.P. Wing, W. He, and V.M. Dixit. 1996. ICE-LAP3, a novel mammalian homolog of the Caenorhabditis elegans cell death protein CED-3 is activated during Fas- and tumor necrosis factor-induced apoptosis. J. Biol. Chem. 271:1621-1625.
15. Boldin, M.P., T.M. Goncharov, Y.V. Goltsev, and D. Wallach. 1996. Involvement of MACH, a novel MORT1/ FADD-interacting protease, in Fas/APO1- and TNF receptor-induced cell death. Cell 85:803-815.
16. Muzio, M., A.M. Chinnaiyan, F.C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni. C. Scaffidi, J.D. Bretz, M. Zhang, R. Gentz et al. 1996. FLICE, a novel FADD-homologous ICE/ CED-3-like protease, is recruited to the CD95 (Fas/Apo-1) death-inducing signaling complex. Cell. 85:817-827.
17. Reed, J.C. 1994. Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124:1-6.
18. Hockenbery, D., G. Nunez, C. Milliman, R.D. Schreiber, and S.J. Korsmeyer. 1990. Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature (Lond). 348:334-336.
19. Nunez, G., R. Merino, D. Grillot, and M. Gonzalez-Garcia. 1994. Bcl-2 and Bcl-x: regulatory switches for lymphoid death and survival. Immunol Today. 15:582-588.
20. Hengartner, M.O., and H.R. Horvitz. 1994. C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian proto-oncogene bcl-2. Cell. 76:665-676.
21. Razvi, E.S., and R.M. Welsh. 1995. Apoptosis in viral infections. Adv. Virus Res. 45:1-60.
22. Komiyama, T., C.A. Ray, D.J. Pickup, A.D. Howard, N.A. Thornberry, E.P. Peterson, and G. Salvesen. 1994. Inhibition of interleukm-1 β converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition. J. Biol. Ghem. 269:19331-19337.
23. Wang, L., M. Miura, L. Bergeron, H. Zhu, and J. Yuan. 1994. Ich-1, an Ice/ced-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell. 78:739-750.
24. Miura, M., R.M. Friedlander, and J. Yuan. 1995. Tumor necrosis factor-induced apoptosis is mediated by a CrmA-sensitive cell death pathway. Proc. Natl. Acad. Sci. USA. 92:8318-8322.
25. Gagliardini, V., P.A. Fernandez, R.K. Lee, H.C. Drexler, R.J. Rotello, M.C. Fishman, and J. Yuan. 1994. Prevention of vertebrate neuronal death by the crmA gene. Science (Wash. DC). 263:826-828.
26. Ray, C.A., R.A. Black, S.R. Kronheim, T.A. Greenstreet, P.R. Sleath, G.S. Salvesen, and D.J. Pickup. 1992. Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1β converting enzyme. Cell. 69:597-604.
27. Hannun, Y.A. 1994. The Sphingomyelin cycle and the second messenger function of ceramide. J. Biol. Chem. 269: 3125-3128.
28. Obeid, L.M., C.M. Linardic, L.A. Karolak, and Y.A. Hannun. 1993. Programmed cell death induced by ceramide. Science (Wash. DC). 259:1769-1771.
29. Jayadev, S., B. Liu, A.E. Bielawska, J.Y. Lee, F. Nazaire, M.Y.U. Pushkareva, L.M. Obeid, and Y.A. Hannun. 1995. Role for ceramide in cell cycle arrest. J. Biol. Chem. 270: 2047-2052.
30. Jarvis, W.D., R.N. Kolesnick, F.A. Fornari, R.S. Traylor, D.A. Gewirtz, and S. Grant. 1994. Induction of apoptotic DNA damage and cell death by activation of the sphingomyelin pathway. Proc. Natl. Acad. Sci. USA. 91:73-77.
31. Strum, J.C., G.W. Small, S.B. Pauig, and L.W. Daniel. 1994. 1-β-D-arabinofuranosylcytosine stimulates ceramide and diglyccride formation in HL-60 cells. J. Biol. Chem. 269:15493-15497.
32. Haimovitz-Friedman, A., G.G. Kan, D. Ehleiter, R.S. Persaud, M. McLoughin, Z. Fuks, and R.N. Kolesnick. 1994. Ionizing radiation acts on cellular membranes to generate ceramide and initiate apoptosis. J. Exp. Med. 180:525-535.
33. Cifone, M.G., R. De Maria, P. Roncaioli, M.R. Rippo, M. Azuma, L.L. Lanier, A. Santoni, and R. Testi. 1994. Apoptotic signaling through CD95 (Fas/Apo-1) activates an acidic sphingomyelinase. J. Exp. Med. 180:1547-1552.
34. Tepper, G.G., S. Jayadev, B. Liu, A. Bielawska, R. Wolff, S. Yonehara, Y.A. Hannun, and M.F. Seldin. 1995. Role of ceramide as an endogenous mediator of Fas-induced cytotoxicity. Proc. Natl. Acad. Sci. USA. 92:8443-8447.
35. Ghinnaiyan, A.M., K. O'Rourke, M. Tewari, and V.M. Dixit. 1995. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell. 81:505-512.
36. Hsu, H., J. Xiong, and D.V. Goeddel. 1995. The TNF receptor 1-associated protein TRADD signals cell death and NF-κB activation. Cell. 81:495-504.
37. Stanger, B.Z., P. Leder, T.H. Lee, E. Kim, and B. Seed. 1995. RIP: a novel protein containing a death domain that interacts with Fas/APO-1 (CD95) in yeast and causes cell death. Cell. 81:513-523.
38. Chinnaiyan, A.M., C.G. Tepper, M.F. Seldin, K. O'Rourke, F.C. Kischkel, S. Hellbardt, P.H. Krammer, M.E. Peter, and V.M. Dixit. 1996. FADD/MORT1 is a common mediator of CD 95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271:4961-4965.
39. Pronk, G.J., K. Ramer, P. Amiri, and L.T. Williams. 1996. Requirement of an ICE-like protease for induction of apoptosis and ceramide generation by REAPER. Science (Wash. DC). 271:808-810.
40. Pushkareva, M., L.M. Obeid, and Y.A. Hannun. 1995. Ceramide: an endogenous regulator of apoptosis and growth suppression. Immunol. Today. 16:294-297.
41. Jaattela, M., M. Benedict, M. Tewari, J.A. Shayman, and V.M. Dixit. 1995. Bcl-x and Bcl-2 inhibit TNF and Fas-induced apoptosis and activation of phospholipase A2 in breast carcinoma cells. Oncogene. 10:2297-2305.
42. Bligh, E.G., and W.J. Dyer. 1959. A rapid method of total lipid extraction and purification. Can. J. Biochem. Physiol. 37: 911-917.
43. Preiss, J., C.R. Loomis, W.R. Bishop, R. Stem, J.E. Niedel, and R.M. Bell. 1986. Quantitative measurement of sn-1,2-diacylglycerols present in platelets, hepatocytes, and ras- and sis-transformed normal rat kidney cells. J. Biol. Chem. 261: 8597-8600.
44. 3-induced HL-60 cell differentiation. J. Biol. Chem. 265:15823-15831.
45. Rouser, G.A.N., S. Fleischer, and Y. Yamamoto. 1970. Two dimensional thin layer Chromatographic separation of polar lipids and determination of phospholipids by phosphorous analysis of spots. Lipids. 5:494-196.
46. Dignam, J.D., R.M. Lebovitz, and R.G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11:1475-1489.
47. Dbaibo, G.S., L.M. Obeid, and Y.A. Hannun. 1993. TNF-α signal transduction through ceramide: dissociation of growth inhibitory effects of TNF-α from activation of NF-κb. J. Biol. Chem. 268:17762-17766.
48. Martin, S.J., S. Takayama, A.J. McGahon, T. Miyashita, J. Corbeil, R.N. Kolesnick, J.C. Reed, and D.R. Green. 1995. Inhibition of ceramide-induced apoptosis by Bcl-2. Cell Death Differ. 2:253-257.
49. Zhang, J., N. Alter, J.C. Reed, C. Borner, L.M. Obeid, and Y.A. Hannun. 1996. Bcl-2 interrupts the ceramide-mediated pathway of cell death. Proc. Natl. Acad. Sci. USA. 93:5325-5328.
50. Smyth, M.J., D.K. Perry, J. Zhang, G.G. Poirier, Y.A. Hannun, and L.M. Obeid. 1996. prICE: a downstream target for ceramide-induced apoptosis and for the inhibitory action of bcl-2. Biochem. J. 316:25-28.
51. Baeuerle, P.A., and T. Henkel. 1994. Function and activation of NF-κB in the immune system. Annu. Rev. Immunol. 12: 141-179.
52. Beg, A.A., T.S. Finco, P.V. Nantermet, and A.S. Baldwin, Jr. 1993. Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of IκBa: a mechanism for NF-κB activation. Mol. Cell Biol. 13:3301-3310.
53. Henkel, T., T. Machleidt, I. Alkalay, M. Kronke, Y. Ben-Neriah, and P. Baeuerle. 1993. Rapid proteolysis of IκB-α is necessary for activation of transcription factor NF-κB. Nature 365:182-185.
54. Schütze, S., K. Potthoff, T. Machleidt, D. Berkovic, K. Wiegmann, and M. Krönke. 1992. TNF activates NF-κB by phosphatidylcholine-specific phospholipase C-induced "acidic" sphingomyelin breakdown. Cell. 71:765-776.
55. Xue, D., and H.R. Horvitz. 1995. Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein, Nature (Lond.). 377:248-251.
56. Machleidt, T., K. Wiegmann, T. Henkel, S. Schütze, P. Baeuerle, and M. Krönke. 1994. Sphingomyelinase activates proteolytic IκB-α degradation in a cell-free system. J. Biol. Chem. 269:13760-13765.
57. Yang, Z., M. Costanzo, D.W. Golde, and R.N. Kolesnick. 1993. Tumor necrosis factor activation of the sphingomyelin pathway signals nuclear factor KB translocation in intact HL-60 cells. J. Biol. Chem. 268:20520-20523.
58. Johns, L.D., T. Sarr, and G.E. Ranges. 1994. Inhibition of ceramide pathway does not affect ability of TNF-α to activate nuclear factor-κB. J. Immunol. 152:5877-5882.
59. Betts, J.C., A.B. Agranoff, G.J. Nabel, and J.A. Shayman. 1994. Dissociation of endogenous cellular ceramide from NF-κB activation. J. Biol. Chem. 269:8455-8458.
60. Kuno, K., K. Sukegawa, Y. Ishikawa, T. Orii, and K. Matsushima. 1994. Acid Sphingomyelinase is not essential for the IL-1 and tumor necrosis factor receptor signaling pathway leading to NFκB activation. Int. Immunol. 6:1269-1272.
61. Westwick, J.K., A.E. Bielawska, G. Dbaibo, Y.A. Hannun, and D.A. Brenner. 1995. Ceramide activates the stress-activated protein kmases. J. Biol. Chem. 270:22689-22692.
62. Dbaibo, G.S., M.Y. Pushkareva, S. Jayadev, J.K. Schwarz, J.M. Horowitz, L.M. Obeid, and Y.A. Hannun. 1995. Retinoblastoma gene product as a downstream target for a ceramide-dependent pathway of growth arrest. Proc. Natl. Acad. Sci. USA. 92:1347-1351.
63. Hurwitz, R., K. Ferlinz, G. Vielhaber, H. Moczall, and K. Sandhoff. 1994. Processing of human acid Sphingomyelinase in normal and I-cell fibroblasts. J. Biol. Chem. 269:5440-5445.