Ursodeoxycholic acid prevents cytochrome c release in apoptosis by inhibiting mitochondrial membrane depolarization and channel formation

Cell Death and Differentiation

Volumn 6, Issue 9, 1999, Pages 842-854

  Rodrigues, Cecilia M P ^a,b   Ma, Xiaoming ^a   Linehan Stieers, Cheryle ^a   Fan, Guangsheng ^a   Kren, Betsy T ^a   Steer, Clifford J ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b INSTITUTO SUPERIOR DE CIÊNCIAS DA SAÚDE EGAS MONIZ   (Portugal)

Author keywords

Bax; Bile acid; Cytochrome c; Mitochondria; Permeability transition

Indexed keywords

CASPASE; CYTOCHROME C; DEOXYCHOLIC ACID; DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; OKADAIC ACID; PROTEIN BAX; TRANSFORMING GROWTH FACTOR BETA1; URSODEOXYCHOLIC ACID;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA DEGRADATION; ENZYME RELEASE; LIVER CELL CULTURE; MALE; MEMBRANE CHANNEL; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALIA;

EID: 0032846812     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4400560     Document Type: Article

References (69)

1. Colombo C, Setchell KDR, Podda M, Crosignani A, Roda A, Curcio L, Ronchi M and Giunta A (1990) Effects of ursodeoxycholic acid therapy for liver disease associated with cystic fibrosis. J. Pediatr. 117: 482-489
2. Podda M, Ghezzi C, Battezzati PM, Crosignani A, Zuin M and Roda A (1990) Effects of ursodeoxycholic acid and taurine on serum liver enzymes and bile acids in chronic hepatitis. Gastroenterology 98: 1044-1050
3. Beuers U, Spengler U, Kruis W, Aydemir Ü, Wiebecke B, Heldwein W, Weinzierl M, Pape GR, Sauerbruch T and Paumgartner G (1992) Ursodeoxycholic acid for treatment of primary sclerosing cholangitis: a placebo-controlled trial. Hepatology 16: 707-714
4. Palma J, Reyes H, Ribalta J, Iglesias J, Gonzalez MC, Hernandez I, Alvarez C, Molina C and Danitz AM (1992) Effect of ursodeoxycholic acid in patients with intrahepatic cholestasis of pregnancy. Hepatology 15: 1043-1047
5. Poupon RE, Poupon R, Balkau B and the UDCA-PBC Study Group (1994) Ursodiol for the long-term treatment of primary biliary cirrhosis. N. Engl. J. Med. 330: 1342-1347
6. Beuers U, Boyer JL and Paumgartner G (1998) Ursodeoxycholic acid in cholestasis: potential mechanisms of action and therapeutic applications. Hepatology 28: 1449-1453
7. Spivey JR, Bronk SF and Gores GJ (1993) Glycochenodeoxycholate-induced lethal hepatocellular injury in rat hepatocytes. Role of ATP depletion and cytosolic free calcium. J. Clin. Invest. 92: 17-24
8. Patel T, Bronk SF and Gores GJ (1994) Increases of intracellular magnesium promote glycodeoxycholate-induced apoptosis in rat hepatocytes. J. Clin. Invest. 94: 2183-2192
9. Jones BA, Rao Y-P, Stravitz RTand Gores GJ (1997) Bile salt-induced apoptosis of hepatocytes involves activation of protein kinase C. Am. J. Physiol. 272: G1109-G1115
10. Rodrigues CMP, Fan G, Ma X, Kren BT and Steer CJ (1998) A novel role for ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation. J. Clin. Invest. 101: 2790-2799
11. Botla R, Spivey JR, Aguilar H, Bronk SF and Gores GJ (1995)Ursodeoxycholate (UDCA) inhibits the mitochondrial membrane permeability transition induced by glycochenodeoxycholate: a mechanism of UDCA cytoprotection. J. Pharmacol. Exp. Ther. 272: 930-938
12. Lieser MJ, Park J, Natori S, Jones BA, Bronk SF and Gores GJ (1998) Cholestasis confers resistance to the rat liver mitochondrial permeability transition. Gastroenterology 115: 693-701
13. Rodrigues CMP, Fan G, Wong PY, Kren BT and Steer CJ (1998) Ursodeoxycholic acid may inhibit deoxycholic acid-induced apoptosis by modulating mitochondrial transmembrane potential and reactive oxygen species production. Mol. Med. 4: 165-178
14. Newmeyer DD, Farschon DM and Reed JC (1994) Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79: 353-364
15. Liu X, Kim CN, Yang J, Jemmerson R and Wang X (1996) Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 86: 147-157
16. L inhibits Ara-C-induced mitochondrial loss of cytochrome c and other perturbations that activate the molecular cascade of apoptosis. Cancer Res. 57: 3115-3120
17. Kluck RM, Bossy-Wetzel E, Green DR and Newmeyer DD (1997) The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132-1136
18. Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng T-I, Jones DP and Wang X (1997) Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275: 1129-1132
19. Neame SJ, Rubin LL and Philpott KL (1998)Blocking cytochrome c activity within intact neurons inhibits apoptosis. J. Cell Biol. 142: 1583-1593
20. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B and Kroemer G (1995) Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxyen species in early programmed cell death. J. Exp. Med. 182: 367-377
21. Zamzami N, Susin SA, Marchetti P, Hirsch T, Gómez-Monterrey I, Castedo M and Kroemer G (1996) Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183: 1533-1544
22. Marchetti P, Castedo M, Susin SA, Zamzami N, Hirsch T, Macho A, Haeffner A, Hirsch F, Geuskens M and Kroemer G (1996) Mitochondrial permeability transition is a central coordinating event of apoptosis. J. Exp. Med. 184: 1155-1160
23. Petit PX, Susin S-A, Zamzami N, Mignotte B and Kroemer (1996) Mitochondria and programmed cell death: back to the future. FEBS Lett. 396: 7-13.
24. Kroemer G (1997) Mitochondrial implication in apoptosis. Towards an endosymbiont hypothesis of apoptosis evolution. Cell Death Differ. 4: 443-456
25. Kroemer G (1997) The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3: 614-620
26. Zamzami N, Marchetti P, Castedo M, Hirsch T, Susin SA, Masse B and Kroemer G (1996) Inhibitors of permeability transition interfere with the disruption of the mitochondrial transmembrane potential during apoptosis. FEBS Lett. 384: 53-57
27. Shimizu S, Eguchi Y, Kamiike W, Matsuda H and Tsujimoto Y (1996) Bcl-2 expression prevents activation of the ICE protease cascade. Oncogene 12: 2251-2257
28. Shimizu S, Eguchi Y, Kamiike W, Waguri S, Uchiyama Y, Matsuda H and Tsujimoto Y (1996) Bcl-2 blocks loss of mitochondrial membrane potential while ICE inhibitors act at a different step during inhibition of death induced by respiratory chain inhibitors. Oncogene 13: 21-29.
29. Matsuyama S, Schendel SL, Xie Z and Reed JC (1998) Cytoprotection by Bcl-2 requires the pore-forming 25 and 26 helices. J. Biol. Chem. 273: 30995-31001
30. Xiang J, Chao DT and Korsmeyer SJ (1996) BAX-induced cell death may not require interleukin 1β-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA 93: 14559-14563
31. Pastorino JG, Chen S-T, Tafani M, Snyder JW and Farber JL (1998) The overexpression of Bax produces cell death upon induction of the mitochondrial permeability transition. J. Biol. Chem. 273: 7770-7775
32. Narita M, Shimizu S, Ito T, Chittenden T, Lutz RJ, Matsuda H and Tsujimoto Y (1998) Bax interacts with the permeability transition pore to induce permeabilily transition and cytochrome c release in isolated mitochondria. Prcc. Natl. Acad. Sci. USA 95: 14681-14686
33. Marzo I, Brenner C, Zamzami N, Jürgensmeier JM, Susin SA, Vieira HLA, Prévost M-C, Xie Z, Matsuyama S, Reed JC and Kroemer G (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281: 2027-2031
34. L regulates the membrane potential and volume homeostasis of mitochondria. Cell 91: 627-637
35. Bossy-Wetzel E, Newmeyer DD and Green DR (1998) Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO J 17: 37-49
36. Susin SA, Zamzami N, Castedo M, Daugas E, Wang H-G, Geley S, Fassy F, Reed JC and Kroemer G (1997) The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/ CD95-and ceramide-induced apoptosis. J. Exp. Med. 186: 25-27
37. Marzo I, Brenner C, Zamzami N, Susin SA, Beutner G, Brdiczka D, Remy R, Xie Z-H, Reed JC and Kroemer G (1998) The permeability transition pore complex: a target for apoptosis regulation by caspases and Bcl-2-related proteins. J. Exp. Med. 187: 1261-1271
38. 2+ ions. J. Cell Biol. 143: 217-224
39. Jürgensmeier JM, Xie Z, Deveraux Q, Ellerby L, Bredesen D and Reed JC (1998) Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. USA 95: 4997-5002
40. Okuno S-i, Shimizu S, Ito T, Nomura M, Hamada E, Tsujimoto Y and Matsuda H (1998) Bcl-2 prevents caspase-independent cell death. J. Biol. Chem. 273: 34272-34277
41. Vayssière J-L, Petit PX, Risler Y and Mignotte B (1994)Commitment to apoptosis is associated with changes in mitochondrial biogenesis and activity in cell lines conditionally immortalized with simian virus 40. Proc. Natl. Acad Sci. USA 91: 11752-11756
42. Krippner A, Matsuno-Yagi A, Gottlieb RA and Babior BM (1996) Loss of functicn of cytochrome c in Jurkat cells undergoing Fas-mediated apoptosis. J. Biol. Chem. 271: 21629-21636
43. Susin SA, Zamzami N, Castedo M, Hirsch T, Marchetti P, Macho A, Daugas E, Geuskens M and Kroemer G (1996) Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184: 1331-1341
44. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmed M, Alnemri ES and Wang X (1997) Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489
45. Zou H, Henzel WJ, Liu X, Lutschg A and Wang X (1997) Apaf-1, a human pratein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90: 405-413
46. Jones B, Roberts PJ, Faubion WA, Kominami E and Gores GJ (1998) Cystatin A expression reduces bile salt-induced apoptosis in a rat hepatoma cell line. Am. J. Physiol. 275: G723-G730
47. Bradham CA, Qian T, Streetz K, Trautwein C, Brenner DA and Lemasters JJ (1998) The mitochondrial permeability transition is required for tumor necrosis factor alpha-mediated apoptosis and cytochrome c release. Mol. Cell. Biol. 18: 6353-6364
48. Scaffidi C, Fulda S, Srinivasan A, Fiesen C, Li F, Tomaselli KJ, Debatin K-M, Krammer PH and Peter ME (1998) Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 17: 1675-1687
49. L. FEBS Lett. 415: 29-32
50. McCarthy NJ, Whyte MKB, Gilbert CS and Evan GI (1997) Inhibition of Ced-3/ ICE-related proteases does not prevent cell death induced by oncogenes, DNA damage, or the Bcl-2 homologue Bak. J. Cell Biol. 136: 215-227
51. Rossé T, Olivier R, Monney L, Rager M, Conus S, Fellay I, Jansen B and Borner C (1998) Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature 391: 496-499
52. Man J, Sabbatini P, Perez D, Rao L, Modha D and White E (1996) The E1B 19K protein blocks apoptosis by interacting with and inhibiting p53-inducible and death-promoting Bax protein. Genes Dev. 10: 461-477
53. Zha H, Fisk HA, Yaffe MP, Mahajan N, Herman B and Reed JC (1996) Structure-function comparisons of the proapoptotic protein Bax in yeast and mammalian cells. Mol. Cell. Biol. 16: 6494-6508
54. L during apoptosis. Proc. Natl. Acad. Sci. USA 94: 3668-3672
55. Coping IS, Gross A, Lavoie JN, Nguyen M, Jemmerson R, Roth K, Korsmeyer SJ and Shore GC (1998) Regulated targeting of BAX to mitochondria. J. Cell Biol. 143: 207-215
56. Gross A, Jockel J, Wei MC and Korsmeyer SJ (1998) Enforced dimerization of BAX results in its translocation, mitochondrial dysfunction and apoptosis. EMBO J. 17: 3878-3885
57. Wolter KG, Hsu Y-T, Smith CL, Nechushtan A, Xi X-G and Youle RJ (1997) Movement of Bax from the cytosol to mitochondria during apoptosis. J. Cell Biol. 139: 1281-1292
58. Antonsson B, Conti F, Ciavatta AM, Montessuit S, Lewis S, Martinou I, Bernasconi L, Bernard A, Mermod J-J, Mazzei G, Maundrell K, Gambale F, Sadoul R and Matinou J-C (1997) Inhibition of Bax channel-forming activity by Bcl-2. Science 277: 370-372
59. Schlesinger PH, Gross A, Yin X-M, Yamamoto K, Saito M, Waksman G and Korsmeyer SJ (1997) Comparison of the ion channel characteristics of proapoptotic BAX and antiapoptotic BCL-2. Proc. Natl. Acad. Sci. USA 94: 11357-11362
60. Reed JC (1997) Cytochrome c: can't live with it - can't live without it. Cell 91: 559-562
61. Finucane DM, Bossy-Wetzel E, Waterhouse NJ, Cotter TG and Green DR (1999) Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J. Biol.Chem. 274: 2225-2233
62. Hsu Y-T and Youle RJ (1997) Nonionic detergents induce dimerization among members of the Bcl-2 family. J. Biol. Chem. 272: 13829-13834
63. Hsu Y-T and Youle RJ (1998) Bax in murine thymus is a soluble monomeric protein that displays differential detergent-induced conformations. J. Biol. Chem. 273: 10777-10783
64. Desagher S, Osen-Sand A, Nichols A, Eskes R, Montessuit S, Lauper S, Maundrell K, Antonsson B and Martinou J-C (1999) Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144: 891-901
65. S14 induction. J. Biol. Chem. 261: 9583-9586
66. Oberhammer FA, Pavelka M, Sharma S, Tiefenbacher R, Purchio AF, Bursch W and Schulte-Hermann R (1992) Induction of apoptosis in cultured hepatocytes and in regressing liver by transforming growth factor β1. Proc. Natl. Acad. Sci. USA 89: 5408-5412
67. Walajtys-Rhode E, Zapatero J, Moehren G and Hoek JB (1992) The role of the matrix calcium level in the enhancement of mitochondrial pyruvate carboxylation by glucagon pretreatment. J. Biol. Chem. 267: 370-379
68. Sokol RJ, Devereaux M, Mierau GW, Hambidge KM and Shikes RH (1990) Oxidant injury to hepatic mitochondrial lipids in rats with dietary copper overload. Modification by vitamin E deficiency. Gastroenterology 99: 1061-1071
69. Pastorino JG, Synder JW, Serroni A, Hoek JB and Farber JL (1993) Cyclosporin and carnitine prevent the anoxic death of cultured hepatocytes by inhibiting the mitochondrial permeability transition. J. Biol. Chem. 268: 13791-13798