Ceramide accumulation precedes caspase-3 activation during apoptosis of A549 human lung adenocarcinoma cells

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 284, Issue 6 28-6, 2003, Pages

  Ravid, Tommer ^a   Tsaba, Adili ^a   Gee, Peter ^a   Rasooly, Reuven ^a   Medina, Edward A ^a   Goldkorn, Tzipora ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Bcl 2 overexpression; Hydrogen peroxide; Sphingolipid signaling

Indexed keywords

2 DECANOYLAMINO 3 MORPHOLINO 1 PHENYL 1 PROPANOL; BUTYLOXYCARBONYLASPARTYL FLUOROMETHYL KETONE; CASPASE 3; CASPASE INHIBITOR; CERAMIDE; CERAMIDE GLUCOSYLTRANSFERASE; DIACYLGLYCEROL KINASE; HYDROGEN PEROXIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BCL 2; SPHINGOLIPID; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL GROWTH; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; LIPID METABOLISM; LUNG ADENOCARCINOMA; LUNG ALVEOLUS EPITHELIUM; NICK END LABELING; OXIDATIVE STRESS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; THIN LAYER CHROMATOGRAPHY; WESTERN BLOTTING;

EID: 0038511312     PISSN: 10400605     EISSN: None     Source Type: Journal    
DOI: 10.1152/ajplung.00172.2002     Document Type: Article

References (36)

1. Adams JM and Cory S. The Bcl-2 protein family: arbiters of cell survival. Science 281: 1322-1326, 1998.
2. Allouche M, Bettaieb A, Vindis C, Rousse A, Grignon C, and Laurent G. Influence of Bcl-2 overexpression on the ceramide pathway in daunorubicin-induced apoptosis of leukemic cells. Oncogene 14: 1837-1845, 1997.
3. Alnemri ES, Livingston DJ, Nicholson DW, Salvesen G, Thornberry NA, Wong WW, and Yuan J. Human ICE/CED-3 protease nomenclature. Cell 87: 171, 1996.
4. Belaud-Rotureau MA, Lacombe F, Durrieu F, Vial JP, Lacoste L, Bernard P, and Belloc F. Ceramide-induced apoptosis occurs independently of caspases and is decreased by leupeptin. Cell Death Differ 6: 788-795, 1999.
5. Bose R, Verheij M, Haimovitz-Friedman A, Scotto K, Fuks Z, and Kolesnick R. Ceramide synthase mediates daunorubicin-induced apoptosis: an alternative mechanism for generating death signals. Cell 82: 405-414, 1995.
6. Chan C and Goldkorn T. Ceramide path in human lung cell death. Am J Respir Cell Mol Biol 22: 460-468, 2000.
7. Chen L, Kim TJ, and Pillai S. Inhibition of caspase activity prevents anti-IgM induced apoptosis but not ceramide generation in WEHI 231 B cells. Mol Immunol 35: 195-205, 1998.
8. Dbaibo GS, Perry DK, Gamard CJ, Platt R, Poirier GG, Obeid LM, and Hannun YA. Cytokine response modifier A (CrmA) inhibits ceramide formation in response to tumor necrosis factor (TNF)-alpha: CrmA and Bcl-2 target distinct components in the apoptotic pathway. J Exp Med 185: 481-490, 1997.
9. El-Assaad W, El-Sabban M, Awaraji C, Abboushi N, and Dbaibo GS. Distinct sites of action of Bcl-2 and Bcl-xL in the ceramide pathway of apoptosis. Biochem J 336: 735-741, 1998.
10. 2 acts on cellular membranes to generate ceramide signaling and initiate apoptosis in tracheobronchial epithelial cells. J Cell Sci 111: 3209-3220, 1998.
11. Goldkorn T, Dressler KA, Muindi J, Radin NS, Mendelsohn J, Menaldino D, Liotta D, and Kolesnick RN. Ceramide stimulates epidermal growth factor receptor phosphorylation in A431 human epidermoid carcinoma cells. Evidence that ceramide may mediate sphingosine action. J Biol Chem 266: 16092-16097, 1991.
12. Hannun YA. Functions of ceramide in coordinating cellular responses to stress. Science 274: 1855-1859, 1996.
13. Hannun YA and Luberto C. Ceramide in the eukaryotic stress response. Trends Cell Biol 10: 73-80, 2000.
14. Hofmann K and Dixit VM. Ceramide in apoptosis-does it really matter? Trends Biochem Sci 23: 374-377, 1998.
15. Jaffrezou JP, Levade T, Bettaieb A, Andrieu N, Bezombes C, Maestre N, Vermeersch S, Rousse A, and Laurent G. Daunorubicin-induced apoptosis: triggering of ceramide generation through sphingomyelin hydrolysis. EMBO J 15: 2417-2424, 1996.
16. Jaffrezou JP, Maestre N, de Mas-Mansat V, Bezombes C, Levade T, and Laurent G. Positive feedback control of neutral sphingomyelinase activity by ceramide. FASEB J 12: 999-1006, 1998.
17. Janicke RU, Sprengart ML, Wati MR, and Porter AG. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J Biol Chem 273: 9357-9360, 1998.
18. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, and Flavell RA. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384: 368-372, 1996.
19. Lavrentiadou SN, Chan C, Kawcak TN, Ravid T, Tsaba A, van der Vliet A, Rasooly R, and Goldkorn T. Ceramidemediated apoptosis in lung epithelial cells is regulated by glutathione. Am J Respir Cell Mol Biol 25: 676-684, 2001.
20. Metkar SS, Anand M, Manna PP, Naresh KN, and Nadkarni JJ. Ceramide-induced apoptosis in fas-resistant Hodgkin's disease cell lines is caspase independent. Exp Cell Res 255: 18-29, 2000.
21. Ogretmen B, Pettus BJ, Rossi MJ, Wood R, Usta J, Szulc Z, Bielawska A, Obeid LM, and Hannun YA. Biochemical mechanisms of the generation of endogenous long chain ceramide in response to exogenous short chain ceramide in the A549 human lung adenocarcinoma cell line. Role for endogenous ceramide in mediating the action of exogenous ceramide. J Biol Chem 277: 12960-12969, 2002.
22. Ogretmen B, Schady D, Usta J, Wood R, Kraveka JM, Luberto C, Birbes H, Hannun YA, and Obeid LM. Role of ceramide in mediating the inhibition of telomerase activity in A549 human lung adenocarcinoma cells. J Biol Chem 276: 24901-24910, 2001.
23. Radin NS. Killing cancer cells by poly-drug elevation of ceramide levels: a hypothesis whose time has come? Eur J Biochem 268:193-204, 2001.
24. Radin NS and Vunnam RR. Inhibitors of cerebroside metabolism. Methods Enzymol 72: 673-684, 1981.
25. Ravid T, Avner R, Polak-Charcon S, Faust JR, and Roitelman J. Impaired regulation of 3-hydroxy-3-methylglutaryl-coenzyme A reductase degradation in lovastatin-resistant cells. J Biol Chem 274: 29341-29351, 1999.
26. Reed JC. Bcl-2 and the regulation of programmed cell death. J Cell Biol 124: 1-6, 1994.
27. Ruvolo PP, Deng X, Ito T, Carr BK, and May WS. Ceramide induces Bcl2 dephosphorylation via a mechanism involving mitochondrial PP2A. J Biol Chem 274: 20296-20300, 1999.
28. Sawada M, Nakashima S, Banno Y, Yamakawa H, Hayashi K, Takenaka K, Nishimura Y, Sakai N, and Nozawa Y. Ordering of ceramide formation, caspase activation, and Bax/Bcl-2 expression during etoposide-induced apoptosis in C6 glioma cells. Cell Death Differ 7: 761-772, 2000.
29. Sawada M, Nakashima S, Banno Y, Yamakawa H, Takenaka K, Shinoda J, Nishimura Y, Sakai N, and Nozawa Y. Influence of Bax er Bcl-2 overexpression on the ceramide-dependent apoptotic pathway in glioma cells. Oncogene 19: 3508-3520, 2000.
30. Senchenkov A, Litvak DA, and Cabot MC. Targeting ceramide metabolism-a strategy for overcoming drug resistance. J Natl Cancer Inst 93: 347-357, 2001.
31. Smyth MJ, Perry DK, Zhang J, Poirier GG, Hannun YA, and Obeid LM. prICE: a downstream target for ceramide-induced apoptosis and for the inhibitory action of Bcl-2. Biochem J 316: 25-28, 1996.
32. Takeda Y, Tashima M, Takahashi A, Uchiyama T, and Okazaki T. Ceramide generation in nitric oxide-induced apoptosis. Activation of magnesium-dependent neutral sphingomyelinase via caspase-3. J Biol Chem 274: 10654-10660, 1999.
33. Tepper AD, de Vries E, van Blitterswijk WJ, and Borst J. Ordering of ceramide formation, caspase activation, and mitochondrial changes during CD95- and DNA damage-induced apoptosis. J Clin Invest 103: 971-978, 1999.
34. Yoshimura S, Banno Y, Nakashima S, Takenaka K, Sakai H, Nishimura Y, Sakai N, Shimizu S, Eguchi Y, Tsujimoto Y, and Nozawa Y. Ceramide formation leads to caspase-3 activation during hypoxic PC12 cell death. Inhibitory effects of Bcl-2 on ceramide formation and caspase-3 activation. J Biol Chem 273:6921-6927, 1998.
35. Zhang J, Alter N, Reed JC, Borner C, Obeid LM, and Hannun YA. Bcl-2 interrupts the ceramide-mediated pathway of cell death. Proc Natl Acad Sci USA 93: 5325-5328, 1996.
36. Zhang P, Liu B, Jenkins GM, Hannun YA, and Obeid LM. Expression of neutral sphingomyelinase identifies a distinct pool of sphingomyelin involved in apoptosis. J Biol Chem 272: 9609-9612, 1997.