Caspase-8-mediated apoptosis induced by oxidative stress is independent of the intrinsic pathway and dependent on cathepsins

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 293, Issue 1, 2007, Pages

  Baumgartner, Heidi K ^a   Gerasimenko, Julia V ^a   Thorne, Christopher ^a   Ashurst, Louise H ^a   Barrow, Stephanie L ^a   Chvanov, Michael A ^a   Gillies, Stuart ^a   Criddle, David N ^a   Tepikin, Alexei V ^a   Petersen, Ole H ^a   Sutton, Robert ^a   Watson, Alastair J M ^a   Gerasimenko, Oleg V ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Acinar cells; Menadione; Pancreas

Indexed keywords

2 NAPHTHYLAMINE; BAFILOMYCIN A1; BONGKREKIC ACID; CASPASE 10; CASPASE 12; CASPASE 2; CASPASE 8; CASPASE 9; CATHEPSIN; CATHEPSIN D; CATHEPSIN L; DIPEPTIDYL PEPTIDASE I; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GLYCYLPHENYLALANINE; MENADIONE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; PEPSTATIN;

ACUTE PANCREATITIS; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL DEATH; CELL DESTRUCTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME SUBSTRATE; INTESTINE MUCOSA PERMEABILITY; MALE; MITOCHONDRIAL PERMEABILITY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PANCREAS CELL; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; BONGKREKIC ACID; CALCIUM; CASPASE 8; CASPASE 9; CATHEPSIN D; CATHEPSINS; EGTAZIC ACID; ENZYME ACTIVATION; LYSOSOMES; MALE; MICE; MODELS, BIOLOGICAL; OXIDATIVE STRESS; PANCREAS; VITAMIN K 3;

EID: 34547100575     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00103.2007     Document Type: Article

References (66)

1. 2 is a consequence of lysosomal rupture. Biochem J 356: 549-555, 2001.
2. Basu A, Castle VP, Bouziane M, Bhalla K, Haldar S. Crosstalk between extrinsic and intrinsic cell death pathways in pancreatic cancer: synergistic action of estrogen metabolite and ligands of death receptor family. Cancer Res 66: 4309-4318, 2006.
3. Beaujouin M, Baghdiguian S, Glondu-Lassis M, Berchem G, Liaudet-Coopman E. Overexpression of both catalytically active and -inactive cathepsin D by cancer cells enhances apoptosis-dependent chemo-sensitivity. Oncogene 25: 1967-1973, 2006.
4. Beier M, Brandt-Nedelev B, Ruthenbuerger M, Jaroscakova I, Schachke N, Reinheckel T, Mayerle J, Halangk W, Lerch M. Experimental pancreatitis in cathepsin B-overexpressing mice (Abstract). Gastroenterology 130: A383, 2006.
5. Bhatia M, Brady M, Shokuhi S, Christmas S, Neoptolemos JP, Slavin J. Inflammatory mediators in acute pancreatitis. J Pathol 190: 117-125, 2000.
6. Bhatia M, Brady M, Shokuhi S, Zagorski J, Neoptolemos JP, Slavin J. Treatment with neutralizing antibody against cytokine-induced neutrophil chemoattractant protects rats against acute pancreatitis-associated lung injury (Abstract). Gastroenterology 118: A425, 2000.
7. Boldin MP, Goncharov TM, Gotsev YV, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 85: 803-815, 1996.
8. Broker LE, Huisman C, Span SW, Rodriguez JA, Kruyt FAE, Giaccone G. Cathepsin B mediates caspase-independent cell death induced by microtubule stabilizing agents in non-small cell lung cancer cells. Cancer Res 64: 27-30, 2004.
9. Brunk UT, Dalen H, Roberg K, Hellquist HB. Photo-oxidative disruption of lysosomal membranes causes apoptosis of cultured human fibroblasts. Free Radic Biol Med 23: 616-626, 1997.
10. 2+ homeostasis in health and disease. Biol Res 37: 653-660, 2004.
11. Cao Y, Adhikari S, Ang AD, Moore PK, Bhatia M. Mechanism of induction of pancreatic acinar cell apoptosis by hydrogen sulfide. Am J Physiol Cell Physiol 291: C503-C510, 2006.
12. Chandra D, Choy G, Deng X, Bhatia B, Daniel P, Tang DG. Association of active caspase 8 with the mitochondrial membrane during apoptosis: potential roles in cleaving BAP31 and caspase 3 and mediating mitochondrion-endoplasmic reticulum cross talk in etoposide-induced cell death. Mol Cell Biol 24: 6592-6607, 2004.
13. Chandra D, Tang DG. Mitochondrially localized active caspase-9 and caspase-3 result mostly from translocation from the cytosol and partly from caspase-mediated activation in the organelle. Lack of evidence for Apaf-1-mediated procaspase-9 activation in the mitochondria. J Biol Chem 278: 17408-17420, 2003.
14. Chen C, Chen WU, Zhou M, Arttamangkul S, Haugland RP. Probing the cathepsin D using a BODIPY FL-pepstatin A: applications in fluorescence polarization and microscopy. J Biochem Biophys Methods 42: 137-151, 2000.
15. Chvanov M, Gerasimenko OV, Petersen OH, Tepikin AV. Calcium-dependent release of NO from intracellular S-nitrosothiols. EMBO J 25: 3024-3032, 2006.
16. Chvanov M, Petersen OH, Tepikin A. Free radicals and the pancreatic acinar cells: role in physiology and pathology. Philos Trans R Soc Lond B Biol Sci 360: 2273-2284, 2005.
17. Chwieralski CE, Welte T, Buhling F. Cathepsin-regulated apoptosis. Apoptosis 11: 143-149, 2006.
18. Criddle DN, Gillies S, Baumgartner-Wilson HK, Jaffar M, Chinje EC, Passmore S, Chvanov M, Barrow S, Gerasimenko OV, Tepikin AV, Sutton R, Petersen OH. Menadione-induced reactive oxygen species generation via redox cycling promotes apoptosis of murine pancreatic acinar cells. J Biol Chem 281: 40485-40492, 2006.
19. Danial NN, Korsmeyer SJ. Cell death: critical control points. Cell 116: 205-219, 2004.
20. 2 provoke lysosomal damage in human astrocytoma D384 cells followed by apoptosis. Free Radic Biol Med 30: 1347-1356, 2001.
21. Davidson SM, Duchen MR. Calcium microdomains and oxidative stress. Cell Calcium 40: 561-574, 2006.
22. 2+ elevations and the mitochondrial permeability transition pore. J Cell Sci 115: 485-497, 2002.
23. Gukovskaya AS, Pandol SJ. Cell death pathways in pancreatitis and pancreatic cancer. Pancreatology 4: 567-586, 2004.
24. Halangk W, Lerch MM, Brandt-Nedelev B, Roth W, Ruthenbuerger M, Reinheckel T, Domschke W, Lippert H, Peters C, Deussing J. Role of cathepsin B in intracellular trypsinogen activation and the onset of acute pancreatitis. J Clin Invest 106: 773-781, 2000.
25. Hollensworth SB, Shen C, Sim JE, Spitz DR, Wilson GL, LeDoux SP. Glial cell type-specific responses to menadione-induced oxidative stress. Free Radic Biol Med 28: 1161-1174, 2000.
26. Ishisaka R, Utsumi T, Kanno T, Arita K, Katunuma N, Akiyama J, Utsumi K. Participation of a cathepsin L-type protease in the activation of caspase-3. Cell Struct Funct 24: 465-470, 1999.
27. Jadot M, Colmant C, Wattiauxdeconinck S, Wattiaux R. Intralysosomal hydrolysis of glycyl-L-phenylalanine 2-naphthylamide. Biochem J 219: 965-970, 1984.
28. Kagedal K, Zhao M, Svensson I, Brunk UT. Sphingosine-induced apoptosis is dependent on lysosomal proteases. Biochem J 359: 335-343, 2001.
29. Kalivendi SV, Donorev EA, Cunningham S, Vanamala SK, Kaji EH, Joseph J, Kalyanavaman B. Doxorubicin activates nuclear factor of activated T-lymphocytes and Fas ligand transcription: role of mitochondrial reactive oxygen species and calcium. Biochem J 389: 527-539, 2005.
30. Kegedal K, Johansson U, Ollinger K. The lysosomal protease cathepsin D mediates apoptosis induced by oxidative stress. FASEB J 15: 1592-1594, 2001.
31. Kerr JFR, Wyllie AH, Currie AR. Apoptosis - basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26: 239-257, 1972.
32. Lassus P, Opitz-Araya X, Lazebnik Y. Requirement for caspase-2 in stress-induced apoptosis before mitochondrial permeabilization. Science 297: 1352-1354, 2002.
33. Le Bras M, Clément MV, Pervaiz S, Brenner C. Reactive oxygen species and the mitochondrial signaling pathway of cell death. Histol Histopathol 20: 205-220, 2005.
34. 2+](i) studied in isolated rat cardiomyocytes. J Physiol 496: 111-128, 1996.
35. Li HL, Zhu H, Xu CJ, Yuan JY. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94: 491-501, 1998.
36. Li P, Nijhawan D, Budihardjo SM, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489, 1997.
37. Mareninova OA, Sung KF, Hong P, Lugea A, Pandol SJ, Gukovsky I, Gukovskaya AS. Cell death in pancreatitis - caspases protect from necrotizing pancreatitis. J Biol Chem 281: 3370-3381, 2006.
38. Marques CA, Keil U, Bonert A, Steiner B, Haass C, Muller WE, Eckert A. Neurotoxic mechanisms caused by the Alzheimer's disease-linked Swedish amyloid precursor protein mutation: oxidative stress, caspases, and the JNK pathway. J Biol Chem 278: 28294-28302, 2003.
39. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HLA, Prevost MC, Xie ZH, Matsuyama S, Reed JC, Kroemer G. Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281: 2027-2031, 1998.
40. Milhas D, Cuvillier O, Therville N, Clave P, Thomsen M, Levade T, Benoist H, Segui B. Caspase-10 triggers bid cleavage and caspase cascade activation in FasL-induced apoptosis. J Biol Chem 280: 19836-19842, 2005.
41. Muzio M, Chinnaiyan AM, Kischkel FC, O'Rourke K, Shevchenko A, Ni J, Scaffidi C, Bretz JD, Zhang M, Gentz R, Mann M, Krammer PH, Peter ME, Dixit VM. 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, 1996.
42. Nakagawa T, Zhu H, Morishima N, Li E, Xu J, Yankner BA, Yuan J. Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403: 98-103, 2000.
43. Nicholson DW. Caspase structure, proteolytic substrates, and function during apoptotic cell death. Cell Death Differ 6: 1028-1042, 1999.
44. Criddle DN, Gerasimenko JV, Baumgartner HK, Jaffar M, Voronina S, Sutton R, Petersen OH, Gerasimenko OV. Calcium signalling and pancreatic cell death: apoptosis or necrosis? Cell Death Differ. In press.
45. Nicotera P, Merlino G. Regulation of the apoptosis-necrosis switch. Oncogene 23: 2757-2765, 2004.
46. Ollinger K. Inhibition of cathepsin D prevents free-radical-induced apoptosis in rat cardiomyocytes. Arch Biochem Biophys 373: 346-351, 2000.
47. Orrenius S, Zhivotovsky B, Nicotera P. Regulation of cell death: the calcium-apoptosis link. Nats Rev Mol Cell Biol 4: 552-565, 2003.
48. Pandol SJ. Acute pancreatitis. Curr Opin Gastroenterol 22: 481-486, 2006.
49. 2+ homeostasis in the endoplasmic reticulum. Cell Death Differ 13: 1409-1418, 2006.
50. Riedl SJ, Shi YG. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 5: 897-907, 2004.
51. Rizzuto R, Pinton P, Ferrari D, Chami M, Szabadkai G, Magalhaes PJ, Di Virgilio F, Pozzan T. Calcium and apoptosis: facts and hypotheses. Oncogene 22: 8619-8627, 2003.
52. Roberg K, Kagedal K, Ollinger K. Microinjection of cathepsin D induces caspase-dependent apoptosis in fibroblasts. Am J Pathol 161: 89-96, 2002.
53. Sabri A, Alcott SG, Elouardighi H, Pak E, Derian C, Andrade-Gordon P, Kinnally K, Steinberg SF. Neutrophil cathepsin G promotes detachment-induced cardiomyocyte apoptosis via a protease-activated receptor-independent mechanism. J Biol Chem 278: 23944-23954, 2003.
54. Sanchez-Bernal C, Garcia-Morales OH, Dominguez C, Martin-Gallan P, Calvo JJ, Ferreira L, Perez-Gonzalez N. Nitric oxide protects against pancreatic subcellular damage in acute pancreatitis. Pancreas 28: E9-E15, 2004.
55. Schotte P, Van Criekinge W, Van de Craen M, Van Loo G, Desmedt M, Grooten J, Cornelissen M, De Ridder L, Vandekerckhove J, Fiers W, Vandenabeele P, Beyaert R. Cathepsin B-mediated activation of the proinflammatory caspase-11. Biochem Biophys Res Commun 251: 379-387, 1998.
56. Sharma AK, Rohrer B. Calcium-induced calpain mediates apoptosis via caspase-3 in a mouse photoreceptor cell line. J Biol Chem 279: 35564-35572, 2004.
57. Shikama Y, Mami U, Miyashita T, Yamada M. Comprehensive studies on subcellular localization and cell death-inducing activities of eight GFP-tagged apoptosis-related caspases. Exp Cell Res 264: 315-325, 2001.
58. Shimohama S, Tanino H, Fujimoto S. Differential subcellular localization of caspase family proteins in the adult rat brain. Neurosci Lett 315: 125-128, 2001.
59. Sprick MR, Rieser E, Stahl H, Grosse-Wilde A, Weigand MA, Walczak H. Caspase-10 is recruited to and activated at the native TRAIL and CD95 death-inducing signaling complexes in a FADD-dependent manner but cannot functionally substitute caspase-8. EMBO J 21: 4520-4530, 2002.
60. Stoka V, Turk B, Schendel SL, Kim T, Cirman T, Snipas SJ, Ellerby LM, Bredesen D, Freeze H, Abrahamson M, Bromme D, Krajewski S, Reed JC, Yin X, Turk V, Salvesen GS. Lysosomal protease pathways to apoptosis. J Biol Chem 276: 3149-3157, 2001.
61. Susin SA, Lorenzo HK, Zamzami IM, Brenner C, Lorochette N, Prevost M, Alzari PM, Kroemer G. Mitochondrial release of caspase-2 and -9 during the apoptotic process. J Exp Med 189: 381-393, 1999.
62. 2+ oscillations in exocrine cells evoked by agonists and inositol triphosphate. Cell 74: 661-668, 1993.
63. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science 281: 1312-1316, 1998.
64. Wang X, Ryter SW, Dai C, Tang ZL, Watkins SC, Yin XM, Song R, Choi AM. Necrotic cell death in response to oxidant stress involves the activation of the apoptogenic caspase-8/bid pathway. J Biol Chem 278: 29184-29191, 2003.
65. Watson AJM. Apoptosis and colorectal cancer. Gut 53: 1701-1709, 2004.
66. Wille A, Gerber A, Heimburg A, Reisenauer A, Peters C, Saftig P, Reinheckel T, Welte T, Buhling F. Cathepsin L is involved in cathepsin D processing and regulation of apoptosis in A549 human lung epithelial cells. Biol Chem 385: 665-670, 2004.