Oxidative stress and apoptosis in fetal rat liver induced by maternal cholestasis. Protective effect of ursodeoxycholic acid

Journal of Hepatology

Volumn 43, Issue 2, 2005, Pages 324-332

  Perez, Maria J ^a   Macias, Rocio I R ^b   Duran, Cristina ^a   Monte, Maria J ^b   Gonzalez Buitrago, Jose M ^a   Marin, Jose J G ^b  

^a HOSPITAL UNIVERSITARIO DE SALAMANCA   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Bax; Bile acid; Caspase; Glutathione; Pregnancy

Indexed keywords

CASPASE 3; CASPASE 8; GLUTATHIONE; PROTEIN BAX; PROTEIN BCL 2; URSODEOXYCHOLIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BILE ACID BLOOD LEVEL; BILE ACID SYNTHESIS; BLOOD LEVEL; CARBONYLATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYP27 GENE; CYP7A1 GENE; CYP8B1 GENE; ENZYME ACTIVITY; FEMALE; GENE; INTRAHEPATIC CHOLESTASIS; LABOR; LIPID PEROXIDATION; MOTHER; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BILE ACIDS AND SALTS; BIOLOGICAL MARKERS; CASPASE 3; CASPASES; CHOLAGOGUES AND CHOLERETICS; CHOLESTASIS; DISEASE MODELS, ANIMAL; ENZYME PRECURSORS; FEMALE; LIVER; MATERNAL-FETAL EXCHANGE; OXIDATIVE STRESS; PREGNANCY; PROTO-ONCOGENE PROTEINS C-BCL-2; RATS; RATS, WISTAR; URSODEOXYCHOLIC ACID;

EID: 21844466507     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2005.02.028     Document Type: Article

References (51)

1. A.F. Attili, M. Angelico, A. Cantafora, D. Alvaro, and L. Capocaccia Bile acid-induced liver toxicity: relation to the hydrophobic-hydrophilic balance of bile acids Med Hypotheses 19 1986 57 69
2. D. Billington, C.E. Evans, P.P. Godfrey, and R. Coleman Effects of bile salts on the plasma membranes of isolated rat hepatocytes Biochem J 188 1980 321 327
3. R.J. Sokol, M.S. Straka, R. Dahl, M.W. Devereaux, B. Yerushalmi, and E. Gumpricht Role of oxidant stress in the permeability transition induced in rat hepatic mitochondria by hydrophobic bile acids Pediatr Res 49 2001 519 531
4. P. Ljubuncic, B. Fuhrman, J. Oiknine, M. Aviram, and A. Bomzon Effect of deoxycholic acid and ursodeoxycholic acid on lipid peroxidation in cultured macrophages Gut 39 1996 475 478
5. M.J. Czaja Induction and regulation of hepatocyte apoptosis by oxidative stress Antioxid Redox Signal 4 2002 759 767
6. W.A. Faubion, M.E. Guicciardi, H. Miyoshi, S.F. Bronk, P.J. Roberts, and P.A. Svingen Toxic bile salts induce rodent hepatocyte apoptosis via direct activation of Fas J Clin Invest 103 1999 137 145
7. C.M. Rodrigues, G. Fan, X. Ma, B.T. Kren, and C.J. Steer A novel role for ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation J Clin Invest 101 1998 2790 2799
8. B. Yerushalmi, R. Dahl, M.W. Devereaux, E. Gumpricht, and R.J. Sokol Bile acid-induced rat hepatocyte apoptosis is inhibited by antioxidants and blockers of the mitochondrial permeability transition Hepatology 33 2001 616 626
9. S.H. Oh, K.J. Yun, J.X. Nan, D.H. Sohn, and B.H. Lee Changes in expression and immunolocalization of protein associated with toxic bile salts-induced apoptosis in rat hepatocytes Arch Toxicol 77 2003 110 115
10. M. Narita, S. Shimizu, T. Ito, T. Chittenden, R.J. Lutz, and H. Matsuda Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria Proc Natl Acad Sci USA 95 1998 14681 14686
11. P. Li, D. Nijhawan, I. Budihardjo, S.M. Srinivasula, M. Ahmad, and E.S. Alnemri Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade Cell 91 1997 479 489
12. G. Paumgartner, and U. Beuers Ursodeoxycholic acid in cholestatic liver disease: mechanisms of action and therapeutic use revisited Hepatology 36 2002 525 531
13. S. Guldutuna, M. Leuschner, N. Wunderlich, A. Nickel, S. Bhatti, and K. Hubner Cholic acid and ursodeoxycholic acid therapy in primary biliary cirrhosis. Changes in bile acid patterns and their correlation with liver function Eur J Clin Pharmacol 45 1993 221 225
14. M. Dumont, S. Erlinger, and S. Uchman Hypercholeresis induced by ursodeoxycholic acid and 7-ketolithocholic acid in the rat: possible role of bicarbonate transport Gastroenterology 79 1980 82 89
15. H. Mitsuyoshi, T. Nakashima, Y. Sumida, T. Yoh, Y. Nakajima, and H. Ishikawa Ursodeoxycholic acid protects hepatocytes against oxidative injury via induction of antioxidants Biochem Biophys Res Commun 263 1999 537 542
16. G. Serviddio, J. Pereda, F.V. Pallardo, J. Carretero, C. Borras, and J. Cutrin Ursodeoxycholic acid protects against secondary biliary cirrhosis in rats by preventing mitochondrial oxidative stress Hepatology 39 2004 711 720
17. F. Lammert, H.U. Marschall, and S. Matern Intrahepatic cholestasis of pregnancy Curr Treat Options Gastroenterol 6 2003 123 132
18. A. Zimber, and I. Zusman Effects of secondary bile acids on the intrauterine development in rats Teratology 42 1990 215 224
19. M.A. Serrano, D. Brites, M.G. Larena, M.J. Monte, M.P. Bravo, and N. Oliveira Beneficial effect of ursodeoxycholic acid on alterations induced by cholestasis of pregnancy in bile acid transport across the human placenta J Hepatol 28 1998 829 839
20. J. Palma, H. Reyes, J. Ribalta, I. Hernandez, L. Sandoval, and R. Almuna Ursodeoxycholic acid in the treatment of cholestasis of pregnancy: a randomized, double-blind study controlled with placebo J Hepatol 27 1997 1022 1028
21. C.M.P. Rodrigues, J.J.G. Marin, and D. Brites Bile acid patterns in meconium are influenced by cholestasis of pregnancy and not altered by ursodeoxycholic acid treatment Gut 45 1999 446 452
22. G. Mazzella, N. Rizzo, F. Azzaroli, P. Simoni, L. Bovicelli, and A. Miracolo Ursodeoxycholic acid administration in patients with cholestasis of pregnancy: effects on primary bile acids in babies and mothers Hepatology 33 2001 504 508
23. J. Palma, H. Reyes, J. Ribalta, J. Iglesias, M.C. Gonzalez, and I. Hernandez Effects of ursodeoxycholic acid in patients with intrahepatic cholestasis of pregnancy Hepatology 15 1992 1043 1047
24. M.J. Monte, A.I. Morales, M. Arevalo, I. Alvaro, R.I.R. Macias, and J.J.G. Marin Reversible impairment of neonatal hepatobiliary function by maternal cholestasis Hepatology 23 1996 1208 1217
25. M.A. Serrano, R.I. Macias, M. Vallejo, O. Briz, A. Bravo, and M.J. Pascual Effect of ursodeoxycholic acid on the impairment induced by maternal cholestasis in the rat placenta-maternal liver tandem excretory pathway J Pharmacol Exp Ther 305 2003 515 524
26. U. Mashige, K. Imai, and T. Osuga Simple and sensitive assay of serum total bile acids Clin Chim Acta 70 1976 79 86
27. M.Y. El-Mir, M.J. Monte, A.I. Morales, M. Arevalo, M.A. Serrano, and J.J.G. Marin Effect of maternal cholestasis on biliary lipid and bile acid secretion in the infant rat Hepatology 26 1997 527 536
28. W.G. Niehaus, and B. Samuelsson Formation of malonaldehyde from phospholipid arachidonate during microsomal lipid peroxidation Eur J Biochem 6 1968 126 130
29. A.Z. Reznick, and L. Packer Oxidative damage to proteins: spectrophotometric method for carbonyl assay Methods Enzymol 233 1994 357 363
30. F. Tietze Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues Anal Biochem 27 1969 502 522
31. O.W. Griffith Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine Anal Biochem 106 1980 207 212
32. A. Clairborne, and I. Fridovich Purification of the o-dianisidine peroxidase from Escherichia coli B. Physicochemical characterization and analysis of its dual catalatic and peroxidatic activities J Biol Chem 254 1979 4245 4252
33. L. Flohé, and W.A. Günzler Assays of glutathione peroxidase Methods Enzymol 105 1984 114 121
34. I. Carlberg, and B. Mannervick Glutathione reductase Methods Enzymol 113 1985 484 490
35. W.H. Habig, M.J. Pabst, and W.B. Jakoby Glutathione S-transferases. The first enzymatic step in mercapturic acid formation J Biol Chem 249 1974 7130 7139
36. J.I. Hasegawa, S. Kamada, W. Kamiike, S. Shimizu, T. Imazu, and H. Matsuda Involvement of CPP32/Yama (-like) proteases in Fas-mediated apoptosis Cancer Res 56 1996 1713 1718
37. M.A. Markwell, S.M. Haas, L.L. Bieber, and N.E. Tolbert A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples Anal Biochem 87 1978 206 210
38. J. Muntane, J.L. Montero, T. Marchal, C. Perez-Seoane, J.M. Lozano, and E. Fraga Effect of PGE1 on TNF-alpha status and hepatic d-galactosamine-induced apoptosis in rats J Gastroenterol Hepatol 13 1998 197 207
39. O. Briz, R.I. Macias, M. Vallejo, A. Silva, M.A. Serrano, and J.J. Marin Usefulness of liposomes loaded with cytostatic bile acid derivatives to circumvent chemotherapy resistance of enterohepatic tumors Mol Pharmacol 63 2003 742 750
40. H. Sawai, S. Kawai, and N. Domae Reduced expression of Bax in ceramide-resistant HL-60 subline Biochem Biophys Res Commun 319 2004 46 49
41. G.S. Salvesen, and V.M. Dixit Caspase activation: the induced-proximity model Proc Natl Acad Sci USA 96 1999 10964 10967
42. S. Singh, G. Shackleton, E. Ah-Sing, J. Chakraborty, and M.E. Bailey Antioxidant defenses in the bile duct-ligated rat Gastroenterology 103 1992 1625 1629
43. E. Purucker, R. Winograd, E. Roeb, and S. Matern Glutathione status in liver and plasma during development of biliary cirrhosis after bile duct ligation Res Exp Med (Berl) 198 1998 167 174
44. G. Zollner, P. Fickert, A. Fuchsbichler, D. Silbert, M. Wagner, and S. Arbeiter Role of nuclear bile acid receptor, FXR, in adaptive ABC transporter regulation by cholic and ursodeoxycholic acid in mouse liver, kidney and intestine J Hepatol 39 2003 480 488
45. G.I. Henderson, J.J. Chen, and S. Schenker Ethanol, oxidative stress, reactive aldehydes, and the fetus Front Biosci 4 1999 D541 D550
46. T. Yoshioka, Y. Takehara, M. Shimatani, K. Abe, and K. Utsumi Lipid peroxidation and antioxidants in rat liver during development Tohoku J Exp Med 137 1982 391 400
47. J. Sastre, M. Asensi, F. Rodrigo, F.V. Pallardo, M. Vento, and J. Vina Antioxidant administration to the mother prevents oxidative stress associated with birth in the neonatal rat Life Sci 54 1994 2055 2059
48. M.M. Gonzalez, R. Madrid, and R.M. Arahuetes Physiological changes in antioxidant defences in fetal and neonatal rat liver Reprod Fertil Dev 7 1995 1375 1380
49. Macias RIR, Serrano MA, Monte MJ, Jimenez S, Hernandez B, Marin JJG. Long-term effect of treating pregnant rats with ursodeoxycholic acid on the congenital impairment of bile secretion induced in the pups by maternal cholestasis. J Pharmacol Exp Ther 2005;312:751-758.
50. M.H. Schoemaker, W.M. Gommans, L.C. de la Rosa, M. Homan, P. Klok, and C. Trautwein Resistance of rat hepatocytes against bile acid-induced apoptosis in cholestatic liver injury is due to nuclear factor-kappa B activation J Hepatol 39 2003 153 161
51. H. Kurosawa, F.G. Que, L.R. Roberts, P.J. Fesmier, and G.J. Gores Hepatocytes in the bile duct-ligated rat express Bcl-2 Am J Physiol 272 1997 G1587 G1593