Distinct stress and cell destruction pathways are engaged by TNF and ceramide during apoptosis of MCF-7 cells

Experimental Cell Research

Volumn 294, Issue 2, 2004, Pages 523-533

  Donato, Nicholas J ^a   Klostergaard, Jim ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

Cell death; Ceramide; TNF

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CASPASE; CERAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; STRESS ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE INHIBITOR; TUMOR NECROSIS FACTOR;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL DEATH; CELL DESTRUCTION; CELL LINE; CELL MEMBRANE PERMEABILITY; CELL STIMULATION; CELL STRAIN; CELL STRAIN MCF 7; CONTROLLED STUDY; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; INCUBATION TIME; INTERMETHOD COMPARISON; MASS SPECTROMETRY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION;

MINK CELL FOCUS-FORMING VIRUS;

EID: 1542328922     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2003.11.021     Document Type: Article

References (61)

1. Liu Z.-G., Hsu H., Goeddel D.V., Karin M. Dissection of TNF receptor-1 effector functions: JNK activation is not linked to apoptosis while NF-kB activation prevents cell death. Cell. 87:1996;565-576.
2. Hsu H., Xiong J., Goeddel D.V. The TNF receptor 1-associated protein TRADD signals cell death and NF-kB activation. Cell. 81:1995;495-504.
3. Moriguchi T., Toyoshima F., Masuyama N., Hanafusa H., Gotoh Y., Nishida E. A novel JNK/SAPK kinase, MKK7, stimulated by TNFα and cellular stresses. EMBO J. 16:1997;7045-7053.
4. Lee F.S., Hagler J., Chen Z.-J., Maniatis T. Activation of the IkBα kinase complex by MEKK1, a kinase of the JNK pathway. Cell. 88:1997;213-222.
5. Vercammen D., Beyaert R., Denecker G., Goossens V., Van Loo G., Declercq 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.
6. Leroux M.E., Auzenne E., Weidner D., Wu Z.Y., Donato N.J., Klostergaard J. Febrile and acute hyperthermia enhance TNF-induced necrosis of murine L929 fibrosarcoma cells via caspase-regulated production of reactive oxygen intermediates. J. Cell. Phys. 187:2001;256-263.
7. Dbaibo G.S., Obeid L.M., Hannun Y.A. Tumor necrosis factor-α (TNF-α) signal transduction through ceramide. J. Biol. Chem. 268:1993;17762.
8. Kolesnick R., Golde D. The sphingomyelin pathway in tumor necrosis factor and interleukin-1 signaling. Cell. 77:1994;325-328.
9. Liud B., Andrieu-Abadie N., Levade T., Zhang P., Obeid L.M., Hannun Y.A. Glutathione regulation of neutral sphingomyelinase in tumor necrosis factor-alpha-induced cell death. J. Biol. Chem. 273:1998;11313-11320.
10. Luberto C., Hassler D.F., Signorelli P., Okamoto Y., Sawai H., Boros E., Hazen-Martin D.J., Obeid L.M., Hannun Y.A., Smith G.K. Inhibition of tumor necrosis factor-induced cell death in MCF7 by a novel inhibitor of neutral sphingomyelinase. J. Biol. Chem. 277:2002;41128-41139.
11. Kronke M. The mode of ceramide action: the alkyl chain protrusion model. Cytokine Growth Factor Rev. 8:1997;103-107.
12. Muller G., Storz P., Bourteele S., Doppler H., Pfizenmaier K., Mischak H., Phillip A., Kaiser C., Kolch W. Regulation of Raf-1 kinase by TNF via its second messenger ceramide and cross-talk with mitogenic signaling. EMBO J. 17:1998;732-742.
13. Balzquez C., Galve-Roperh I., Guzman M. De novo-synthesized ceramide signals apoptosis in astrocytes via extracellular signal-regulated kinase. FASEB. 14:2000;2315-2322.
14. Zhou H., Summers S.A., Birnbaum M.J., Pittman R.N. Inhibition of Akt kinase by cell-permeable ceramide and its implications for ceramide-induced apoptosis. J. Biol. Chem. 273:1998;16568-16575.
15. Lozano J., Berra E., Municio M.M., Diaz-Meco M.T., Dominguez I., Sanz L., Moscat J. Protein kinase C zeta isoform is critical for kappa B-dependent promoter activation by sphingomyelinase. J. Biol. Chem. 269:1994;19200-19202.
16. Dobrowsky R.T. Sphingolipid signaling domains. Floating on rafts or buried in caves? Cell. Signalling. 12:2000;81-90.
17. Gulbins E., Grassme H. Ceramide and cell death receptor clustering. Biochim. Biophys. Acta. 1585:2002;139-145.
18. Moriguchi T., Kawasaki H., Matsuda S., Gotoh Y., Nishida E. Evidence for multiple activators for stress-activated protein kinase/c-Jun amino-terminal kinases. Evidence of novel activators. J. Biol. Chem. 270:1995;12969-12972.
19. Meier R., Rouse J., Cuenda A., Nebreda A.R., Cohen P. Cellular stresses and cytokines activate multiple mitogen-activated-protein kinase kinase homologues in PC12 and KB cells. Eur. J. Biochem. 236:1996;796-805.
20. Verheij M., Bose R., Lin X.-H., Yao B., 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 JNK/SAPK signaling in stress-induced apoptosis. Nature. 380:1996;75-79.
21. 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.
22. Shirakabe K., Yamaguchi K., Shibuya H., Irie K., Matsuda S., Moriguchi T., Gotoh Y., Matsumoto K., Nishida E. TAK1 mediates the ceramide signaling to stress-activated protein kinase/c-Jun N-terminal kinase. J. Biol. Chem. 272:1997;8141.
23. Pyne S., Chapman J., Steele L., Pyne N.J. Sphingomyelin-derived lipids differently regulate the extracellular signal-regulated kinase 2 (ERK-2) and c-Jun N-terminal kinase (JNK) signal cascades in airway smooth muscle. Eur. J. Biochem. 327:1996;819-826.
24. Ameyari M., Atfi A., Cai Z., Stancou R., Shatrov V., Bettaieb A., Chouaib S. Analysis of human breast adenocarcinoma MCF7 resistance to tumor necrosis factor-induced cell death. J. Biol. Chem. 273:1998;29002.
25. Soule H.D., Vazquez J., Long A., Albert S., Brennan M. A human cell line from a pleural effusion derived from a breast carcinoma. J. Natl. Cancer Inst. 51:1973;1409-1416.
26. Doman R.K., Perez M., Donato N.J. JNK and p53 stress signaling cascades are altered in MCF-7 cells resistant to tumor necrosis factor-mediated apoptosis. J. Interferon Cytokine Res. 19:1999;261-269.
27. Mcconkey D.J., Goodrich D., Bucana C., Klostergaard J. The human retinoblastoma gene product suppresses ceramide-induced apoptosis in human bladder tumor cells. Oncogene. 13:1996;1693-1700.
28. Klostergaard J., Auzenne E., Leroux E. Characterization of cytotoxicity induced by sphingolipids in multidrug-resistant leukemia cells. Leuk. Res. 22:1998;1049-1056.
29. Nicholson D.W., Ali A., Thornberry N.A., Vaillancourt J.P., Ding C.K., Gallant M., Gareau Y., Griffin P.R., Labelle M., Lazenbnik Y.A.et al. Identification and inhibition of the ICE/CED3 protease necessary for mammalian apoptosis. Nature. 376:1995;37-43.
30. Thornberry N.A., Peterson E.P., Zhao J.J., Howard A.D., Griffin P.R., Chapman K.T. Inactivation of interleukin-1 beta converting enzyme by peptide (acyloxy)methyl ketones. Biochemistry. 33:1994;3934-3940.
31. Sachs C.W., Safa A., Harrison S., Fine R.L. Partial inhibition of multidrug resistance by safingol is independent of modulation of P-glycoprotein substrate activities and correlated with inhibition of protein kinase C. J. Biol. Chem. 270:1995;26639-26648.
32. 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. U. S. A. 91:1994;73-77.
33. Tewari M., Quan L.T., O'Rourke K., Desnoyers S., Zeng Z., Beidler D.R., Poirier G.G., Salvesen G.S., Dixit V.M. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell. 81:1995;801-809.
34. Bielawska A., Crane H.M., Liotta D., Obeid L.M., Hannun Y.A. Selectivity of ceramide-mediated biology. Lack of activity of erythro-dihydroceramide. J. Biol. Chem. 268:1993;26226-26232.
35. Jarvis W.D., Grant S., Kolesnick R.N. Ceramide and the induction of apoptosis. Clin. Cancer Res. 2:1996;1-6.
36. Bose R., Verheij M., Haimovitz-Friedman A., Scotto K., Fuks Z., Kolesnick R. Ceramide synthase mediates daunorubicin-induced apoptosis: a new mechanism for generating death signals. Cell. 82:1995;405-414.
37. Wiegmann K., Schutze S., Machleit T., Witte D., Kronke M. Functional dichotomy of neutral and acidic sphingomyelinase in tumor necrosis factor signaling. Cell. 78:1994;1005-1015.
38. Adam D., Wiegmann K., Adam-Lages S., Ruff A., Kronke M. A novel receptor cytoplasmic domain of the p55 tumor necrosis factor receptor initiates the neutral sphingomyelinase pathway. J. Biol. Chem. 271:1996;14617-14622.
39. Berghe T.V., Kalai M., Van Loo G., Declercq W., Vandenabeele P. Disruption of HSP90 function reverts tumor necrosis factor-induced necrosis to apoptosis. J. Biol. Chem. 278:2002;5622-5629.
40. Kim M.-Y., Linardic C., Obeid L., Hannun Y. Identification of sphingomyelin turnover as an effector mechanism for the action of tumor necrosis factor α and γ-interferon. J. Biol. Chem. 266:1991;484-489.
41. Jayadev S., Liu B., Bielawska A.E., Lee J.Y., Nazaire F., Pushkareva M.Y., Obeid L.M., Hannun Y.A. Role for ceramide in cell cycle arrest. J. Biol. Chem. 270:1995;2047-2052.
42. Mathias S., Dressler K.A., Kolesnick R.N. Characterization of a ceramide-activated protein kinase: stimulation by tumor necrosis factor α Proc. Natl. Acad. Sci. 88:1991;10009-10013.
43. Tomiuk S., Hofmann K., Nix M., Zumbansen M., Stoffel W. Cloned mammalian neutral sphingomyelinase: functions in sphingolipid signaling? Proc. Natl. Acad. Sci. U. S. A. 95:1998;3638-3643.
44. DeMaria R., Lenti L., Malisan F., D'Agostino F., Tomassini B., Zeuner A., Rippo M.R., Testi R. Requirement for CD3 ganglioside in CD95- and ceramide-induced apoptosis. Science. 277:1997;1652-1655.
45. Stroh C., Schulze-Osthoff K. Death by a thousand cuts: an ever increasing list of caspase substrates. Cell Death Differ. 5:1998;997-1000.
46. Wang Z.Q., Stingl L., Morrison C., Jantsch M., Los M., Schulze-Osthoff K., Wagner E.F. PARP is important for genomic stability but dispensable in apoptosis. Genes Dev. 11:1997;2347-2358.
47. Sweeney E.A., Inokuchi J., Igarashi Y. Inhibition of sphingolipid induced apoptosis by caspase inhibitors indicates that sphingosine acts in an earlier part of the apoptotic pathway than ceramide. FEBS Lett. 425:1998;61-65.
48. Cuvillier O., Rosenthal D.S., Smulson M.E., Spiegel S. Sphingosine 1-phosphate inhibits activation of caspases that cleave poly(ADP-ribose) polymerase and lamins during Fas- and ceramide-mediated apoptosis in Jurkat T lymphocytes. J. Biol. Chem. 273:1998;2910-2916.
49. Gamen S., Hanson D.A., Kaspar A., Naval J., Krensky A.M., Anel A. Granulysin-induced apoptosis: I. Involvement of at least two distinct pathways. J. Immunol. 161:1998;1758-1764.
50. Spinedi A., Amendola A., Di Bartolomeo S., Piacentini M. Ceramide-induced apoptosis is mediated by caspase activation independently from retinoblastoma protein post-translational modification. Biochem. Biophys. Res. Commun. 243:1998;852-857.
51. Belaud-Rotureau M.-A., Lacombe F., Durrieu F., Vial J.-P., Lacoste L., Bernard P., Belloc F. Ceramide-induced apoptosis occurs independently of caspases and is decreased by leupeptin. Cell Death Differ. 6:1999;788-795.
52. 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. U. S. A. 94:1997;7292-7296.
53. Watts J.D., Gu M., Patterson S.D., Aebersold R., Polverino A.J. On the complexities of ceramide changes in cells undergoing apoptosis: lack of evidence for a second messenger function in apoptotic induction. Cell Death Differ. 6:1999;105-114.
54. Thomas R.L., Matsko C.M., Lotze M.T., Amoscato A.A. Mass spectrometric identification of increased C16 ceramide levels during apoptosis. J. Biol. Chem. 274:1999;30580-30588.
55. Liebish G., Drobnik W., Reil M., Trunbach B., Arnecke R., Oligemuller B., Roscher A., Schmitz G. J. Lipid Res. 40:1999;1539-1546.
56. Hartfield P.J., Bilney A.J., Murray A.W. Neurotrophic factors prevent ceramide-induced apoptosis downstream of c-Jun N-terminal kinase activation in PC12 cells. J. Neurochem. 71:1998;161-169.
57. Pettus B.J., Chalfant C.E., Hannun Y.A. Ceramide in apoptosis: an overview and current perspectives. Biochim. Biophys. Acta. 1585:2002;114-125.
58. Hartfield P.J., Bilney A.J., Murray A.W. Neurotrophic factors prevent ceramide-induced apoptosis downstream of c-Jun N-terminal kinase activation in PC12 cells. J. Neurochem. 71:1998;161-169.
59. Nakajima K., Honda S., Tohyama Y., Kurihara T., Kohsaka S. Ceramide-enhanced urokinase-type plasminogen activator (uPA) release is mediated by protein kinase C in cultured microglia. Glia. 32:2000;226-233.
60. Kim H.J., Lee K.J. Heat shock and ceramide have different apoptotic pathways in radiation induced fibrosarcoma (RIF) cells. Mol. Cell. Biochem. 229:2002;139-151.
61. Caricchio R., D'Adamio L., Cohen P.L. Fas, ceramide and serum withdrawal induce apoptosis via a common pathway in a type II Jurkat cell line. Cell Death Differ. 9:2002;574-580.