A novel role for ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation

Journal of Clinical Investigation

Volumn 101, Issue 12, 1998, Pages 2790-2799

  Rodrigues, Cecilia M P ^a,b   Fan, Guangsheng ^a   Ma, Xiaoming ^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

Bile acid; Fas ligand; Mitochondrial membrane permeability transition; Okadaic acid; Transforming growth factor beta

Indexed keywords

ALCOHOL; BILE ACID; DEOXYCHOLIC ACID; FAS LIGAND; OKADAIC ACID; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE; TRANSFORMING GROWTH FACTOR BETA1; URSODEOXYCHOLIC ACID;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE; CELL STRUCTURE; CELL VIABILITY; CONTROLLED STUDY; HELA CELL; HUMAN; HUMAN CELL; LIVER CELL; MALE; MEMBRANE PERMEABILITY; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; RAT;

EID: 0032525819     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1325     Document Type: Article

References (52)

1. Schumucker, D.L., M. Ohta, S. Kanai, Y. Sato, and K. Kitani. 1990. Hepatic injury induced by bile salts: correlation between biochemical and morphological events. Hepatology. 12:1216-1221.
2. Heuman, D.M., A.S. Mills, J. McCall, P.B. Hylemon, W.M. Pandak, and Z.R. Vlahcevic. 1991. Conjugates of ursodeoxycholate protect against cholestasis and hepatocellular necrosis caused by more hydrophobic bile salts. In vivo studies in the rat. Gastroenterology. 100:203-211.
3. Quist, R.G., H.-T. Ton-Nu, J. Lillienau, A.F. Hofmann, and K.E. Barrett. 1991. Activation of mast cells by bile acids. Gastroenterology. 101:446-456.
4. Spivey, J.R., S.F. Bronk, and G.J. Gores. 1993. Glycochenodeoxycholate-induced lethal hepatocellular injury in rat hepatocytes. Role of ATP depletion and cytosolic free calcium. J. Clin. Invest. 92:17-24.
5. Patel, T., S.F. Bronk, and G.J. Gores. 1994. Increases of intracellular magnesium promote glycodeoxycholate-induccd apoptosis in rat hepatocytes. J. Clin. Invest. 94:2183-2192.
6. Heuman, D.M., and R. Bajaj. 1994. Ursodeoxycholate conjugates protect against disruption of cholesterol-rich membranes by bile salts. Gastroenterology. 106:1333-1341.
7. Podda, M., C. Ghezzi, P.M. Battezzati, A. Crosignani, M. Zuin, and A. Roda. 1990. Effects of ursodeoxycholic acid and taurine on serum liver enzymes and bile acids in chronic hepatitis. Gastroenterology. 98:1044-1050.
8. Chazouillères, O., R. Poupon, J.-P. Capron, E.-H. Metman, D. Dhumeaux, M. Amouretti, P. Couzigou, D. Labayle, and J.-C. Trinchet. 1990. Ursodeoxycholic acid for primary sclerosing cholangitis. J. Hepatology. 11:120-123.
9. Poupon, R.E., R. Poupon, and B. Balkau. 1994. Ursodiol for the long-term treatment of primary biliary cirrhosis. The UDCA-PBC Study Group. N. Engl. J. Med. 330:1342-1347.
10. Columbano, A. 1995. Cell death: current difficulties in discriminating apoptosis from necrosis in the context of pathological processes in vivo. J. Cell. Biochem. 58:181-190.
11. Wyllie, A.H., J.F.R. Kerr, and A.R. Currie. 1980. Cell death: the significance of apoptosis. Int. Rev. Cytol. 68:251-306.
12. Kroemer G., P. Petit, N. Zamzami, J.-L. Vayssière, and B. Mignotte. 1995. The biochemistry of programmed cell death. FASEB (Fed. Am. Soc. Exp. Biol.) J. 9:1277-1287.
13. Walker, P.R., L. Kokileva, J. Leblank, and M. Sikorska. 1993. Detection of the initial stages of DNA fragmentation in apoptosis. BioTechniques. 15: 1032-1040.
14. Jones, B.A., Y.-P. Rao, R.T. Stravitz, and G.J. Gores. 1997. Bile salt-induced apoptosis of hepatocytes involves activation of protein kinase C. Am. J. Physiol. 272:G1109-G1115.
15. Patel, T., and G.J. Gores. 1995. Apoptosis and hepatobiliary disease. Hepatology. 21:1725-1741.
16. Koga, H., S. Sakisaka, M. Ohishi, M. Sata, and K. Tanikawa. 1997. Nuclear DNA fragmentation and expression of Bcl-2 in primary biliary cirrhosis. Hepatology. 25:1077-1084.
17. Botla, R., J.R. Spivey, H. Aguilar, S.F. Bronk, and G.J. Gores. 1995. Ursodeoxycholate (UDCA) inhibits the mitochondrial membrane permeability transition induced by glycochenodeoxycholate: a mechanism of UDCA cytoprotection. J. Pharmacol. Exp. Ther. 272:930-938.
18. Reed, J.C. 1997. Double identity for proteins of the Bcl-2 family. Nature. 387:773-776.
19. Kroemer, G. 1997. The proto-oncogene Bcl-2 and its role in regulating apoptosis. Nat. Med. 3:614-620.
20. Jacobson, M.D., J.F. Burne, and M.C. Raff. 1994. Programmed cell death and Bcl-2 protection in the absence of a nucleus. EMBO (Eur. Mol. Biol. Organ.) J. 13:1899-1910.
21. Schulze-Osthoff, K., H. Walczak, W. Dröge, and P.H. Krammer. 1994. Cell nucleus and DNA fragmentation are not required for apoptosis. J. Cell Biol. 127:15-20.
22. S14 induction. J. Biol. Chem. 261:9583-9586.
23. Kren, B.T., C.M.P. Rodrigues, K.D.R. Setchell, and C.J. Steer. 1995. Posttranscriptional regulation of steady-state mRNA levels in rat liver associated with deoxycholic acid feeding. Am. J. Physiol. 269:G961-G973.
24. Lawson, A.M., and K.D.R. Setchell. 1988. Mass spectrometry of bile acids. In The Bile Acids. K.D.R. Setchell, D. Kritchevsky, and P.P. Nair, editors. Vol. 4. Plenum Press, New York. 167-267.
25. Oberhammer, F.A., M. Pavelka, S. Sharma, R. Tiefenbacher, A.F. Purchio, W. Bursch, and R. Schulte-Hermann. 1992. Induction of apoptosis in cultured hepatocytes and in regressing liver by transforming growth factor β1. Proc. Natl. Acad. Sci. USA. 89:5408-5412.
26. Walajtys-Rhode, E., J. Zapatero, G. Moehren, and J.B. Hoek. 1992. The role of the matrix calcium level in the enhancement of mitochondrial pyruvate carboxylation by glucagon pretreatment. J. Biol. Chem. 267:370-379.
27. Sokol, R.J., M. Devereaux, G.W. Mierau, K.M. Hambidge, and R.H. Shikes. 1990. Oxidant injury to hepatic mitochondrial lipids in rats with dietary copper overload. Gastroenterology. 99:1061-1071.
28. Pastorino, J.G., J.W. Synder, A. Serroni, J.B. Hoek, and J.L. Farber. 1993. Cyclosporine and carnitine prevent the anoxic death of cultured hepatocytes by inhibiting the mitochondrial permeability transition. J. Biol. Chem. 268:13791-13798.
29. Cathcart, R., E. Schwiers, and B.N. Ames. 1983. Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal. Biochem. 134:111-116.
30. Zamzami, N., P. Marchetti, M. Castedo, C. Zanin, J.-L. Vayssière, P.X. Petit, and G. Kroemer. 1995. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 181:1661-1672.
31. Carter, W.O., P.K. Narayanan, and J.P. Robinson. 1994. Intracellular hydrogen peroxide and superoxide anion detection in endothelial cells. J. Leukocyte Biol. 55:253-258.
32. Fan, G., X. Ma, B.T. Kren, and C.J. Steer. 1996. The retinoblastoma gene product inhibits TGF-β1 induced apoptosis in primary rat hepatocytes and human HuH-7 hepatoma cells. Oncogene. 12:1909-1919.
33. Nagata, S., and P. Golstein. 1995. The Fas death factor. Science. 267: 1449-1456.
34. Gunter, T.E., and D.R. Pfeiffer. 1990. Mechanisms by which mitochondria transport calcium. Am. J. Physiol. 258:C755-C786.
35. Kandell, R.L., and C. Bernstein. 1991. Bile salt/acid induction of DNA damage in bacterial and mammalian cells: implications for colon cancer. Nutr. Cancer. 16:227-238.
36. Kwo, P., T. Patel, S.F. Bronk, and G.J. Gores. 1995. Nuclear serine protease activity contributes to bile acid-induced apoptosis in hepatocytes. Am. J. Physiol. 268:G613-G621.
37. Patel, T., G.J. Gores, and S.H. Kaufmann. 1996. The role of proteases during apoptosis. FASEB (Fed. Am. Soc. Exp. Biol.) J. 10:587-597.
38. Patel, T., and G.J. Gores. 1997. Inhibition of bile-salt-induced hepatocyte apoptosis by the antioxidant lazaroid U83836E. Toxicol. Appl. Pharmacol. 142:116-122.
39. Suchy, F.J. 1993. Hepatocellular transport of bile acids. Semin. Liver Dis. 13:235-247.
40. Jänicke, R.U., P.A. Walker, X. Y. Lin, and A.G. Porter. 1996. Specific cleavage of the retinoblastoma protein by an ICE-like protease in apoptosis. EMBO (Eur. Mol. Biol. Organ.) J. 15:6969-6978.
41. Roberts, L.R., H. Kurosawa, S.F. Bronk, P.J. Fesmier, L.B. Agellon, W.-Y. Leung, F. Mao, and G.J. Gores. 1997. Cathepsin B contributes to bile salt-induced apoptosis of rat hepatocytes. Gastroenterology. 113:1714-1726.
42. Benedetti, A., E. Brunelli, R. Risicato, T. Cilluffo, A.M. Jézéquel, and F. Orlandi. 1988. Subcellular changes and apoptosis induced by ethanol in rat liver. J. Hepatol. 6:137-143.
43. Goldin, R.D., N.C. Hunt, J. Clark, and S.N. Wickramasinghe. 1993. Apoptotic bodies in a murine model of alcoholic liver disease: reversibility of ethanol-induced changes. J. Pathol. 171:73-76.
44. Ogasawara, J., R. Watanabe-Fukunaga, M. Adachi, A. Matsuzawa, T. Kasugai, Y. Kitamura, N. Itoh, T. Suda, and S. Nagata. 1993. Lethal effect of the anti-Fas antibody in mice. Nature. 364:806-809.
45. Bouscarel, B., S. Ceryak, T.W. Gettys, H. Fromm, and F. Noonan. 1995. Alteration of cAMP-mediated hormonal responsiveness by bile acids in cells of nonhepatic origin. Am. J. Physiol. 268:G908-G916.
46. Zamzami, N., P. Marchetti, M. Castedo, D. Decaudin, A. Macho, T. Hirsch, S.A. Susin, P.X. Petit, B. Mignotte, and G. Kroemer. 1995. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 182:367-377.
47. Kroemer, G., N. Zamzami, and S.A. Susin. 1997. Mitochondrial control of apoptosis. Immunol. Today. 18:44-51.
48. Stefaniwsky, A.B., G.S. Tint, J. Speck, S. Shefer, and G. Salen. 1985. Ursodeoxycholic acid treatment of bile reflux gastritis. Gastroenterology. 89:1000-1004.
49. Earnest, D.L., H. Holubec, R.K. Wali, C.S. Jolley, M. Bissonette, A.K. Bhattacharyya, H. Roy, S. Khare, and T.A. Brasitus. 1994. Chemoprevention of azoxymethane-induced colonie carcinogenesis by supplemental dietary ursodeoxycholic acid. Cancer Res. 54:5071-5074.
50. Setchell, K.D.R., C.M.P. Rodrigues, M. Podda, and A. Crosignani. 1996. Metabolism of orally administered tauroursodeoxycholic acid in patients with primary biliary cirrhosis. Gut. 38:439-446.
51. Thompson, C.B. 1995. Apoptosis in the pathogenesis and treatment of disease. Science. 267:1456-1462.
52. Ortiz, A., F.N. Ziyadeh, and E.G. Neilson. 1997. Expression of apoptosis-regulatory genes in renal proximal tubular epithelial cells exposed to high ambient glucose and in diabetic kidneys. J. Invest. Med. 45:50-56.