Resistance of rat hepatocytes against bile acid-induced apoptosis in cholestatic liver injury is due to nuclear factor-kappa B activation

Journal of Hepatology

Volumn 39, Issue 2, 2003, Pages 153-161

  Schoemaker, Marieke H ^a,d   Gommans, Willemijn M ^a   Conde De La Rosa, Laura ^a   Homan, Manon ^a   Klok, Pieter ^b   Trautwein, Christian ^c   Van Goor, Harry ^b   Poelstra, Klaas ^a   Haisma, Hidde J ^b   Jansen, Peter L M ^a   Moshage, Han ^a  

^a Ctr for Liver Digest/Metab Dis   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

Author keywords

Apoptosis; Bile acids; Caspases; Cholestasis; cIAP2; Hepatocytes; Inflammation; Nuclear factor kappa B

Indexed keywords

BILE ACID; CASPASE 3; CASPASE 8; CASPASE 9; CYTOKINE; GLYCOCHENODEOXYCHOLIC ACID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR OF APOPTOSIS PROTEIN; PROTEIN BCL 2; TAUROCHENODEOXYCHOLIC ACID; TAUROURSODEOXYCHOLIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BILE DUCT LIGATION; CELL CULTURE; CHOLESTATIC HEPATITIS; CONTROLLED STUDY; ENZYME ACTIVATION; GENE ACTIVATION; GENE CONTROL; GENE EXPRESSION; IN VITRO STUDY; LIVER CELL DAMAGE; LIVER MITOCHONDRION; MALE; NICK END LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STAINING; UPREGULATION;

EID: 10744225137     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0168-8278(03)00214-9     Document Type: Article

References (42)

1. Popper H. Cholestasis. Annu Rev Med 1968;19:39-56.
2. Greim H, Trülzsch D, Roboz J, Dressler K, Czygan P, Hutterer F, et al. Mechanisms of cholestasis 5. Bile acids in normal rat livers and in those after bile duct ligation. Gastroenterology 1972;63:837-45.
3. Schölmerich J, Becher MS, Schmidt K, Schubert R, Kremer B, Feldhaus S, et al. Influence of hydroxylation and conjugation of bile salts on their membrane-damaging properties-studies on isolated hepatocytes and lipid membrane vesicles. Hepatology 1984;4:661-6.
4. Rodrigues CMP, Fan G, Ma X, Kren BT, Steer CJ. A novel role for ursodeoxycholic acid in inhibiting apoptosis by modulating mitochondrial membrane perturbation. J Clin Invest 1998;101:2790-9.
5. Patel T, Bronk SF, Gores GJ. Increases of intracellular magnesium promote glycodeoxycholate-induced apoptosis in rat hepatocytes. J Clin Invest 1994;94:2183-92.
6. Gonzalez B, Fisher C, Rosser BG. Glycochenodeoxycholic acid (GCDC) induced hepatocyte apoptosis is associated with early modulation of intracellular PKC activity. Mol Cell Biochem 2000;207:19-27.
7. Faubion WA, Guicciardi ME, Miyoshi H, Bronk SF, Roberts PJ, Svingen PA, et al. Toxic bile salts induce rodent hepatocyte apoptosis via direct activation of Fas. J Clin Invest 1999;103:137-45.
8. Qiao L, Studer E, Leach K, McKinstry R, Gupta S, Decker R, et al. Deoxycholic acid (DCA) causes ligand-independent activation of epidermal growth factor receptor (EGFR) and Fas receptor in primary hepatocytes: inhibition of EGFR/mitogen-activated protein kinase-signaling module enhanced DCA-induced apoptosis. Mol Biol Cell 2001;12:2609-45.
9. Botla R, Spivey JR, Aguilar H, Bronk SF, Gores GJ. Ursodeoxycholate (UDCA) inhibits the mitochondrial membrane permeability transition induced by glycochenodeoxycholate: a mechanism of UDCA cytoprotection. J Pharmacol Exp Ther 1995;272:930-8.
10. Rodrigues CMP, Ma X, Linehan-Stieers C, Fan G, Kren BT, Steer CJ. Ursodeoxycholic acid prevents cytochrome c release in apoptosis by inhibiting mitochondrial membrane depolarization and channel formation. Cell Death Diff 1999;6:842-54.
11. Yerushalmi B, Dahl R, Devereaux MWE, Gumpricht E, Sokol RJ. Bile acid-induced rat hepatocyte apoptosis is inhibited by antioxidants and blockers of the mitochondrial permeability transition. Hepatology 2001;33:616-26.
12. Rust C, Karnitz LM, Paya CV, Moscat J, Simari RD, Gores GJ. The bile acid taurochenodeoxycholate activates a phosphatidylinositol 3-kinase-dependent survival signaling cascade. J Biol Chem 2000;275:20210-6.
13. Rubin RA, Kowalski TE, Khadelwal M, Malet PF. Ursodiol for hepatobiliary disorders. Ann Intern Med 1994;121:207-18.
14. Benz C, Angermüller S, Otto G, Sauer P, Stremmel W, Stiehl A. Effect of tauroursodeoxycholic acid on bile acid-induced apoptosis in primary human hepatocytes. Eur J Clin Invest 2000;30:203-9.
15. Schoemaker MH, Ros JE, Homan M, Trautwein C, Liston P, Poelstra K, et al. Cytokine regulation of pro- and anti-apoptotic genes in rat hepatocytes: NF-κB-regulated inhibitor of apoptosis protein-2 (cIAP2) prevents apoptosis. J Hepatol 2002;36:742-50.
16. Hatano E, Bennett BL, Manning AM, Qian T, Lemasters JJ, Brenner DA. NF-κB stimulates inducible nitric oxide synthase to protect mouse hepatocytes from TNF-α- and Fas-mediated apoptosis. Gastroenterology 2001;120:1251-62.
17. Kountouras J, Billing BH, Scheurer PJ. Prolonged bile duct obstruction: a new experimental model for cirrhosis in the rat. Br J Exp Pathol 1984;65:305-11.
18. Moshage H, Casini A, Lieber CS. Acetaldehyde selectively stimulates collagen production in cultured rat liver fat-storing cells but not in hepatocytes. Hepatology 1990;12:511-8.
19. Iimuro Y, Nishiura T, Hellerbrand C, Behrns KE, Schoonhoven R, Grisham JW, et al. NF-κB prevents apoptosis and liver dysfunction during liver regeneration. J Clin Invest 1998;101:802-11.
20. Perrelet D, Ferri A, Mackenzie AE, Smith GM, Korneluk RG, Liston P, et al. IAP family proteins delay motoneuron cell death in vivo. Eur J Neurosci 2000;12:2059-67.
21. Hatano E, Bradham CA, Stark A, Iimuro Y, Lemasters JJ, Brenner DA. The mitochondrial permeability transition augments Fas-induced apoptosis in mouse hepatocytes. J Biol Chem 2000;275:11814-23.
22. Vos TA, van Goor H, Tuyt LML, de Jager-Krikken A, Leuvenink R, Kuipers F, et al. Expression of inducible nitric oxide synthase in endotoxemic rat hepatocytes is dependent on the cellular glutathione status. Hepatology 1999;29:421-6.
23. Jaeschke H, Fisher MA, Lawson JA, Simmons CA, Farhood A, Jones DA. Activation of caspase 3 (CPP32)-like proteases is essential for TNF-alpha-induced hepatic parenchymal cell apoptosis and neutrophil-mediated necrosis in a routine endotoxin shock model. J Immunol 1998;160:3480-6.
24. Van der Woude CJ, Jansen PL, Tiebosch AT, Beuving A, Homan M, Kleibeuker JH, et al. Expression of apoptosis-related proteins in Barrett's metaplasia-dysplasia-carinoma sequence: a switch to a more resistant phenotype. Hum Patrol 2002;33:686-92.
25. Miyoshi H, Rust C, Roberts PJ, Burgar LJ, Gores GJ. Hepatocyte apoptosis after bile duct ligation in the mouse involves Fas. Gastroenterology 1999;117:669-77.
26. Grasl-Kraupp B, Ruttkay-Nedecky B, Koudelka H, Bukowska K, Bursch W, Schulte-Hermann R. In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note. Hepatology 1995;21:1465-5.
27. Miyoshi H. Rust C, Guicciardi ME, Gores GJ. NF-kappaB is activated in cholestasis and functions to reduce liver injury. Am J Pathol 2001;158:967-975.
28. Graf D, Kurz AK, Reinehr R, Fischer R, Kircheis G, Häussinger D. Prevention of bile acid-induced apoptosis by betaine in rat liver. Hepatology 2002;36:829-39.
29. Grinko I, Geerts A, Wisse E. Experimental biliary fibrosis correlates with increased numbers of fat-storing and Kupffer cells, and portal endotoxemia. J Hepatol 1995;23:449-58.
30. Sewnath ME, Van Der Poll T, Ten Kate FJ, Van Noorden CJ, Gouma DJ. Interleukin-1 receptor type 1 gene-deficient bile duct-ligated mice are partially protected against endotoxin. Hepatology 2002;35:149-58.
31. Kurosawa H, Que FG, Robert LR, Fesmier PJ, Gores GJ. Hepatocytes in the bile duct-ligated rat express Bcl-2. Am J Physiol 1997;272:G1587-93.
32. Nakopoulou L, Stefanaki K, Vourlakou CH, Manolaki N, Gakiopoulou H, Michalopoulos G. Bcl-2 protein expression in acute and chronic hepatitis, cirrhosis and hepatocellular carcinoma. Pathol Res Pract 1999;195:19-24.
33. Iwata M, Harada K, Kono N, Kaneko S, Kobayashi K, Nakanuma Y. Expression of Bcl-2 familial proteins is reduced in small bile duct lesions of primary biliary cirrhosis. Hum Patrol 2000;31:179-84.
34. Takikawa Y, Miyoshi H, Rust C, Roberts P, Siegel R, Mandal PK, et al. The bile acid-activated phosphatidylinositol 3-kinase pathway inhibits Fas apoptosis upstream of Bid in rodent hepatocytes. Gastroenterology 2001;120:1810-17.
35. Schrantz N, Bourgeade M, Mouhamad S, Leca G, Sharma S, Vazquez A. p38-mediated regulation of an Fas-associated Death Domain protein independent pathway leading to caspase-8 activation during TGF-β-induced apoptosis in human Burkitt Lymphoma B cells BL41. Mol Biol Cell 2001;12:3139-315.
36. Varghese J, Sade H, Vandenabeele P, Sarin A. Head Involution Defective (Hid)-triggered apoptosis requires caspase-8 but not FADD (Fas-associated Death Domain) and is regulated by Erk in mammalian cells. J Biol Chem 2002;277:35097-104.
37. Imai Y, Kimura T, Murakami A, Yajima N, Sakamaki K, Yonehara S. The CED-4-homologous protein FLASH is involved in Fas-mediated activation of caspase-8 during apoptosis. Nature 1999;398:777-85.
38. Scaffidi C, Fulda S, Srinivasan A, Friesen C, Li F, Tomaselli KJ, et al. Two CD95 (APO-1/Fas) signaling pathways. EMBO J 1998;17:1675-87.
39. Cowling V, Downward J. Caspase-6 is the direct activator of caspase-8 in the cytochrome c-induced apoptosis pathway: absolute requirement for removal of caspase-6 prodomain. Cell Death Diff 2002;9:1046-56.
40. Bajt ML, Lawson JA, Vonderfecht SL, Gujral JS, Jaeschke H. Protection against Fas receptor-mediated apoptosis in hepatocytes and non-parenchymal cells by a caspase-8 inhibitor in vivo: evidence for a postmitochondrial processing of caspase-8. Toxicol Sci 2000;58:109-17.
41. Slee EA, Adrain C, Martin SJ. Serial killers: ordering caspase activation events in apoptosis. Cell Death Differ 1999;6:1067-74.
42. Rodrigues CM, Steer CJ. Mitochondrial membrane perturbations in cholestasis. J Hepatol 2000;32:135-41.