BILE SALTS MODULATE CHRONIC ETHANOL-INDUCED HEPATOTOXICITY

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1 Alcohol & Alcoholism Vol. 37, No. 1, pp , 2002 BILE SALTS MODULATE CHRONIC ETHANOL-INDUCED HEPATOTOXICITY ANNE-MARIE MONTET, LAURENCE OLIVA, FRANÇOISE BEAUGÉ 1 nd JEAN-CLAUDE MONTET* Lbortoire de Physiopthologie Héptique, INSERM, 46 Boulevrd de l Gye, 13009, Mrseille nd 1 Centre de Recherche Pernod-Ricrd, Créteil, Frnce (Received 2 Mrch 2001; in revised form 28 July 2001; ccepted 6 August 2001) Abstrct This study tested the hypothesis tht chronic ethnol-induced injury in rts my be modified by the hydrophobicity of the bile cid pool. The supplementtion to chronic ethnol feeding (28 dys) with chenodeoxycholte, hydrophobic bile slt, ggrvted stetosis (ccumultion of tricylglycerols nd cholesterol esters), lipoperoxidtion nd cytolysis (expressed s elevtions of ctivities of sprtte minotrnsferse nd glutmte dehydrogense), while the ddition of ursodeoxycholic cid, hydrophilic bile slt, llevited ethnol-induced heptic ltertions. Furthermore, our dt show tht ursodeoxycholic cid still exerts its beneficil effects in model of more severe heptic intoxiction induced by the co-dministrtion of ethnol nd chenodeoxycholic cid. The hepto-protective effect observed ppers to be independent of the choleretic properties of ursodeoxycholic cid nd my be due prtly to the cpcity of the bile cid to preserve mitochondri. INTRODUCTION Bile slts re polr mphiphilic molecules which ply crucil role in bile formtion. Vritions in the conjugtion nd in the number, position, nd orienttion of hydroxyl groups, led to lrge vritions in the hydrophilic hydrophobic blnce between different bile slts (Armstrong nd Crey, 1982; Heumn, 1989). The more hydrophobic bile slts my be cytotoxic when present in bnormlly high concentrtions. Thus, deoxycholic cid nd chenodeoxycholic cid (CDC), which re the mjor bile cids in humn bile, hve high ffinity for phospholipids nd my disrupt cell membrne integrity. In contrst, the hydrophilic bile cid, ursodeoxycholic cid (UDC), is essentilly non-toxic nd hs even been shown to prevent or reduce heptocyte injury nd cholestsis induced by high concentrtions of hydrophobic bile slts (Heumn et l., 1991,b). UDC s beneficil effects hve been demonstrted in the tretment of cholesttic diseses (Leuschner et l., 1989; Poupon et l., 1991; Colombo et l., 1992; Glbert et l., 1992) nd of drug-induced cholestsis (Zho nd Montet, 1990; Queneu et l., 1993, 1994). On the other hnd, UDC hs been shown to improve liverfunction tests in ptients with lcoholic cirrhosis nd cholestsis who still continue to consume ethnol (Plevris et l., 1991). Moreover, UDC protects Hep G2 cells from ethnol-induced cytotoxicity (Neumn et l., 1995) nd, similrly, turoursodeoxycholte (TUDC) countercts the inhibitory effect of ethnol on bile secretion nd vesiculr exocytosis in the isolted perfused rt liver (Alvro et l., 1995). We hve recently demonstrted tht UDC ws ble to reduce stetosis nd lipid peroxidtion induced by chronic ethnol feeding in rts (Oliv et l., 1998; Tbouy et l., 1998). However, the role of bile slts in modulting chronic ethnol cytotoxicity hs not yet been explored. The beneficil effect of UDC on stetosis might not occur in the presence of hydrophobic bile slt pool. The im of this study ws therefore to compre the effects of CDC nd UDC on chronic ethnol heptotoxicity in rts nd to determine whether UDC could be effective in preventing liver dmge in rts co-dministered ethnol nd CDC. *Author to whom correspondence should be ddressed. MATERIALS AND METHODS Chemicls A nutritionlly dequte diet ws purchsed from UAR Villemoisson, Frnce. UDC ws from Sigm Chemicl Corportion (St Louis, MO, USA). CDC nd turine were from Clbiochem (Los Angeles, CA, USA). The bile slts used were >98% pure. 3α-Hydroxysteroid dehydrogense ws from Worthington Biochemicl Corportion (Freehold, NJ, USA). Cholylglycine hydrolse ws obtined from Sigm. Kits for enzyme ctivity [sprtte minotrnsferse (AST), lnine minotrnsferse (ALT), glutmte dehydrogense (GLDH), nd lctte dehydrogense (LDH)] mesurements were obtined from Boehringer (Boehringer Mnnheim, Germny). Triglycerides (tricylglycerols) nd totl nd free cholesterol contents were determined by enzymtic procedure with commercil kits from Boehringer (Boehringer Mnnheim, Germny). Lipid peroxidtion ws mesured using the LPO-586 ssy from Boehringer Ingelheim (Bioproducts, Ggny, Frnce). Experimentl design Mle Sprgue Dwley rts (Iff-Credo, l Arbresle, Frnce) weighing 250 ± 5 g (men ± SEM) were housed t 25 C with 12 h/12 h light/drk cycles. They received humne cre nd the studies were pproved by the Service Vétérinire de l Snté et de l Protection Animle (no ). Thirty rts were pir-fed liquid diets contining 18% of energy s protein, 35% s ft, 11% s crbohydrte nd 36% s either ethnol (ethnol diet) or s n isocloric mltose dextrin mixture (control diet), ccording to Lieber nd De Crli (1989). Rts were rndomly distributed into five groups of six rts ech nd received vrious tretments for 28 dys: control liquid diet, ethnol diet, ethnol diet + UDC (100 mg/kg/dy), ethnol diet + CDC (80 mg/kg/dy), ethnol diet + UDC (100 mg/kg/dy) + CDC (80 mg/kg/dy). The selected UDC dose (100 mg/kg/dy) is rther similr to tht previously used to prevent heptotoxicity induced by vrious drugs, including ethnol (Zho nd Montet, 1990; Queneu et l., 1994; Tbouy et l., 1998). Vrious doses of CDC ( mg/kg/dy) dded to the control liquid diet were tested in order to select the CDC dose tht meet two conditions: (1) to mrkedly enrich the bile cid pool with CDC; (2) to obtin CDC biliry output lower thn the mximum biliry secretion of CDC in the rt (Kitni et l., Medicl Council on Alcohol

2 26 A.-M. MONTET et l. 1994). The CDC dose we selected (80 mg/kg/dy) did not induce cholestsis or cytolysis. All diets were supplemented with 0.25% turine in order to fvour turoconjugtion of bile slts. At the end of the tretment, rts were nesthetized with pentobrbitl. Cnnultions of the common bile duct nd of the femorl vein were performed. Animls were plced in restrining cges. After 30 min equilibrtion, bile ws collected for 1 h to determine bile slt, phospholipid, cholesterol nd LDH biliry secretion. An intrvenous infusion of 0.9% (w/v) NCl ws mintined t 1.5 ml/h to replenish body fluids. Blood smples were tken for further GLDH, AST nd ALT nlyses. The peritonel cvity ws then opened, nd the liver ws perfused through the portl vein with ice-cold lctte physiologicl serum until most of the blood content of the liver ws wshed out. The liver ws quickly removed nd weighed. A smple of ~1 g ws homogenized in Tris HCl buffer (20 mm, ph 7.4) t 4 C with Potter-Elvehjem homogenizer, in order to determine the rte of lipid peroxidtion. Another liquot of liver ws quickly frozen nd stored t 25 C until lipid nlysis. Heptic lipids nd peroxidtion products Totl liver lipids were extrcted from homogenized liver with chloroform/methnol (2/1; v/v) ccording to Tbouy et l. (1998). Triglyceride, free cholesterol nd cholesterol ester concentrtions were determined by enzymtic procedure with commercilly vilble test kits. To ssess the extent of heptic lipid peroxidtion, the concentrtions of mlondildehyde (MDA) nd 4-hydroxynonenl (4-HNE) in the liver were mesured using the LPO-586 kit. This procedure is bsed on the rection of chromogenic regent with MDA nd 4-HNE to yield stble chromophore with mximl bsorbnce t 586 nm. Biliry lipid secretion Phospholipid nd cholesterol concentrtions in bile were nlysed s previously described (Zho nd Montet, 1990). Totl biliry bile slts were determined enzymticlly using the 3α-hydroxysteroid dehydrogense method (Turley nd Dietschy, 1978). Individul moleculr species of bile slts were determined by gs liquid chromtogrphy fter deconjugtion by cholylglycine hydrolse (Zho nd Montet, 1990). The rtios turine/glycine-conjugted bile slts were obtined fter thin-lyer chromtogrphic seprtion using butnol/ethyl cette/cetic cid (50/40/10, by vol) s solvent system, nd scnner densitometry. The hydrophobicity index of the bile cid pool ws clculted ccording to Heumn (1989). Plsm nd bile enzymtic ctivities The ctivity of biliry LDH ws determined immeditely fter bile collection. Serum ws seprted from whole blood by centrifugtion (4 C for 10 min t 800 g) nd stored t 20 C. GLDH ctivity ws determined by following the oxidtion of NADH t 340 nm. AST nd ALT ctivities were mesured t 37 C by conventionl enzymtic methods with Boehringer kits. Sttistics Results re expressed s mens ± SEM. Sttisticl differences between groups were ssessed by the Kruskl Wllis test, nd the Mnn Whitney test ws used for group-by-group comprisons. Differences were regrded s sttisticlly significnt if P < RESULTS Liver weight nd liver lipid concentrtions Tble 1 shows tht ethnol-fed rts hd significnt 30% increse in liver weight, when compred with control rts. Bile slt feeding modulted liver weight, which ws decresed by 17% by UDC supplementtion to the ethnol diet, but incresed by 10% by CDC supplementtion, both in comprison with the liver weight of ethnol-treted rts. When UDC ws dded to the ethnol + CDC diet, the rise in liver weight ws reduced by 15%. Tble 1 lso shows the influence of ethnol nd ethnol plus UDC nd/or CDC dministrtion on liver lipid ccumultion. Ethnol feeding led to mjor increse in liver triglycerides nd in cholesterol esters. When UDC ws co-dministered with ethnol, stetosis ws prtly prevented: liver triglyceride nd cholesterol ester levels were decresed by 33% nd 31% respectively. By contrst, CDC supplementtion to the ethnol diet led to n increse in triglyceride nd cholesterol ester contents (+53% nd +31% respectively). When UDC ws dded to the ethnol + CDC diet, stetosis ws prtly prevented ( 47% for triglycerides nd 46% for cholesterol esters). Liver lipid concentrtions were similr to those of rts receiving the ethnol + UDC diet. Heptic lipid peroxidtion As shown in Tble 2, ethnol promoted lipid peroxidtion. Concomitnt tretment with UDC during ethnol dministrtion ws ssocited with significnt decrese in lipid peroxidtion: 16% for MDA nd 20% for MDA + 4-HNE. Tble 1. Influence of ursodeoxycholic cid (UDC) nd/or chenodeoxycholic cid (CDC) dministrtion on ethnol-induced chnges in liver weight nd lipids Liver weight Triglycerides Cholesterol esters Groups (g) (mg/g of liver) (mg/g of liver) Control ± 0.15 cd ± 1.46 bcd 3.10 ± 0.17 bcd Ethnol ± ± ± 1.02 Ethnol + UDC ± 0.49 cd ± 5.67 c 8.41 ± 1.06 c Ethnol + CDC ± 0.50 d ± d ± 0.81 d Ethnol + UDC + CDC ± ± ± 1.28 Vlues re mens ± SEM for six rts per group. Different from the ethnol group (P < 0.05); b different from the ethnol + UDC group (P < 0.05); c different from the ethnol + CDC group (P < 0.05); d different from the ethnol + UDC + CDC group (P < 0.05).

3 BILE ACIDS IN ETHANOL-INDUCED HEPATOTOXICITY 27 Tble 2. Ursodeoxycholic cid (UDC) nd chenodeoxycholic cid (CDC) effects on ethnol-induced lipoperoxidtion MDA MDA + 4-HNE Groups (nmol/g of liver) (nmol/g of liver) Control ± 1.10 bcd ± 4.86 bcd Ethnol ± ± 4.00 Ethnol + UDC ± ± 4.98 Ethnol + CDC ± 1.64 b ± 4.39 b Ethnol + UDC + CDC ± 1.91 c ± 5.81 c Vlues re mens ± SEM for six rts per group. Different from the ethnol group (P < 0.05); b different from the ethnol + UDC group (P < 0.05); c different from the ethnol + CDC group (P < 0.05); d different from the ethnol + UDC + CDC group (P < 0.05). MDA, mlondildehyde; 4-HNE, 4-hydroxynonenl. In contrst, when CDC ws co-dministered with ethnol, lipid peroxidtion ws significntly incresed by 18% nd 16% for MDA nd MDA + 4-HNE respectively bove the ethnolonly levels. Lipid peroxidtion ws prtilly prevented by UDC dministrtion when the ethnol diet ws supplemented with CDC. The levels of MDA + 4-HNE were identicl with those obtined with the ethnol + UDC diet. Biliry lipid secretion nd biliry LDH output Bile flow ws unffected by the different tretments (Tble 3). Biliry lipid secretion of control rts ws not significntly modified by ethnol nd ethnol + UDC tretment, but ws enhnced by CDC feeding. In the ethnol + UDC + CDC group, secretion of bile slts, phospholipid, nd cholesterol ws significntly higher thn in the ethnol nd ethnol + UDC groups. No differences on biliry LDH levels were found between the different groups of rts (Tble 3). Bile cid composition nd hydrophobicity indices Turine supplementtion exclusively led to turoconjugted bile slts. Tble 4 displys the proportions of the different moleculr species of bile slts in ech group of rts. Chronic ethnol dministrtion did not ffect the biliry bile cid profile of control rts. For the groups supplemented with bile slts, the dministered bile slt becme the predominnt biliry bile slt. UDC proportions were 47% for the ethnol + UDC group nd 33.8% for the ethnol + UDC + CDC group, wheres the CDC proportions were 49% nd 31% for ethnol + CDC nd ethnol + UDC + CDC groups, respectively. The hydrophobicity index of ech bile cid pool, s estimted by reverse-phse high-performnce liquid chromtogrphy (Heumn, 1989), is lso shown in Tble 4. Control rts nd ethnol-treted rts hd very similr hydrophobicity indices. UDC supplementtion led to decresed index, wheres CDC feeding led to positive index. In rts co-dministered UDC nd CDC, the net hydrophobicity index ws slightly negtive ( 0.09). Serum prmeters Tble 5 reports the effect of the ddition of UDC nd/or CDC on ethnol-induced cytotoxicity. Ethnol lone incresed ALT, AST nd GLDH ctivities. When ethnol ws given concomitntly with UDC, the GLDH ctivity decresed significntly (by 42%). In contrst, 2-fold increse in GLDH ctivity (over the ethnol vlue) ws induced by CDC supplementtion to the ethnol diet. This effect ws significntly blocked when UDC ws dded to the ethnol + CDC diet (by 44%). GLDH Tble 3. Bile flow, biliry secretion of lipids nd biliry lctte dehydrogense Biliry secretion of lipids (µmol/h/kg) Bile flow Lctte dehydrogense Groups (ml/h/kg) Bile slts Phospholipids Cholesterol (mu/h/kg) Control 4.48 ± ± 5.28 cd ± 1.22 cd 1.50 ± 0.55 d ± Ethnol 4.95 ± ± ± ± ± Ethnol + UDC 4.77 ± ± ± ± ± 6.26 Ethnol + CDC 4.93 ± ± ± 1.50 b 1.70 ± ± Ethnol + UDC + CDC 4.98 ± ± bc ± 1.01 b 2.18 ± 0.16 b ± Vlues re mens ± SEM for six rts per group. Different from the ethnol group (P < 0.05); b different from the ethnol + UDC group (P < 0.05); c different from the ethnol + CDC group (P < 0.05); d different from the ethnol + UDC + CDC group (P < 0.05). Tble 4. Bile cid profile nd hydrophobicity index C βmc UDC DC CDC Hydrophobicity Groups (%) (%) (%) (%) (%) index Control 40.9 ± 3.6 bcd 41.7 ± 3.1 bcd 2.5 ± 0.5 bd 7.0 ± 0.9 d 7.9 ± 1.1 bcd 0.26 ± 0.03 bcd Ethnol 39.8 ± ± ± ± ± ± 0.03 Ethnol + UDC 18.0 ± ± ± ± ± ± 0.02 Ethnol + CDC 26.2 ± ± ± 1.1 b 6.3 ± ± 3.9 b ± 0.03 b Ethnol + UDC + CDC 21.6 ± ± 2.7 b 33.8 ± 2.1 bc 2.4 ± ± 3.2 bc 0.09 ± 0.03 bc Vlues re mens ± SEM for six rts per group. Different from the ethnol group (P < 0.05); b different from the ethnol + UDC group (P < 0.05); c different from the ethnol + CDC group (P < 0.05); d different from the ethnol + UDC + CDC group (P < 0.05). C, cholic cid; βmc, β-muricholic cid; UDC, ursodeoxycholic cid; DC, deoxycholic cid; CDC, chenodeoxycholic cid.

4 28 A.-M. MONTET et l. Tble 5. Ursodeoxycholic cid (UDC) nd chenodeoxycholic cid (CDC) effects on serum enzymes ALT AST GLDH Groups (IU/l) (IU/l) (IU/l) Control ± 4.61 cd ± 9.10 cd ± 1.32 bcd Ethnol ± ± ± 3.06 Ethnol + UDC ± ± ± 2.28 Ethnol + CDC ± 2.90 b ± 7.90 b ± 5.83 b Ethnol + UDC + CDC ± 2.03 b ± 2.95 bc ± 7.82 c Vlues re mens ± SEM for six rts per group. Different from the ethnol group (P < 0.05); b different from the ethnol + UDC group (P < 0.05); c different from the ethnol + CDC group (P < 0.05); d different from the ethnol + UDC + CDC group (P < 0.05). ALT, lnine minotrnsferse; AST, sprtte minotrnsferse; GLDH, glutmte dehydrogense. level ws lrger in the ethnol + CDC + UDC group thn in the ethnol + UDC group, but the difference did not rech sttisticl significnce. CDC dministrtion tended to increse serum AST nd ALT ctivities. When UDC ws dded to the ethnol nd the ethnol + CDC diets, ALT tended to diminish, but AST ws significntly decresed. DISCUSSION The results of the present investigtion indicte tht bile slts modulte heptic disorders induced by chronic ethnol feeding in rts. Supplementtion with the hydrophobic bile slt CDC ggrvtes ethnol-induced dmge, wheres the dministrtion of the hydrophilic bile slt UDC hs protective effect. Interestingly, UDC lso meliortes heptocellulr injuries ssocited with lcohol nd CDC co-tretment. Thus, the beneficil ction of UDC is mintined when the bile cid pool contins lrge frction of hydrophobic bile slts, sitution which occurs in humn bile. Our results lso demonstrte tht UDC hs the cpcity to protect heptocytes in the bsence of cholestsis. This is novel spect of the positive effect of UDC becuse, to dte, the min trget of UDC tretment is cholestsis. Our observtions show tht CDC supplementtion to the ethnol diet enriched the bile cid pool with CDC without inducing cholestsis. However, this tretment induced heptic lipid metbolic dysfunctions more severe thn those observed with ethnol lone: stetosis ws significntly incresed (by 53% for triglycerides nd 31% for cholesterol ester concentrtion) nd lipid peroxidtion level ws lso incresed (by 17%). The dditionl toxic effects induced by CDC could result from the gret cpcity of this hydrophobic bile slt to bind to lipid bilyers (Güldütun et l., 1993; Ben Mouz et l., 2001). CDC, t millimolr concentrtions, hs been shown to increse the fluidity of the polr core of liver plsm membrnes (Güldütun et l., 1993), fluidizing effect lso observed with ethnol (Beugé et l., 1996; Oliv et l., 1998). In the presence of ethnol, the toxic threshold of CDC could be lowered nd thus both molecules my lter membrne structure under in vivo conditions. On the other hnd, the relese of the specific mitochondril enzyme GLDH ws significntly incresed by CDC supplementtion, thus reflecting n ltertion of the inner mitochondril membrne permebility. This is consistent with the studies of Krähenbühl et l. (1994), who found tht hydrophobic bile slts cn ffect the function of enzyme complexes in the mitochondril electron trnsport chin. Also, Spivey et l. (1993) showed tht lethl heptocellulr injury by glycochenodeoxycholte ws ssocited with rpid nd significnt depletion of cellulr ATP followed by sustined increse in [C 2+ ]. Glycochenodeoxycholte impired stte 3, but not stte 4, mitochondril respirtion. Similrly, we reported (Tbouy et l., 1998) tht mitochondri from rts chroniclly fed ethnol demonstrted n impired bility to produce energy with decrese in the ADP-stimulted respirtion (V3). Such mitochondril ltertions cused by CDC nd/or ethnol my contribute to the development of the stetosis we observed in the present study. In contrst to the deleterious effect of ethnol + CDC tretment, we showed tht exogenous supplementtion of the hydrophilic bile slt UDC to ethnol feeding improved ethnol-induced heptic dysfunction. This UDC beneficil effect my be due to the slightly decresed hydrophobicity index of the bile slt pool, nd more specificlly to the greter cpcity of UDC to protect heptocytes, thn the other two hydrophilic bile cids, cholic nd βmc. Our dt confirm nd extend previous findings (Alvro et l., 1995; Neumn et l., 1995; Oliv et l., 1998) on the heptoprotective effect of UDC. A key point of the present study is tht UDC ttenutes cytotoxicity of ethnol plus CDC co-dministrtion. Indeed, UDC supplementtion reduced heptomegly (by 15%), stetosis (by 47% for triglycerides nd 46% for cholesterol esters) nd lipid peroxidtion (by 30%). Moreover, the preventive effect of UDC included n ttenution of the incresed serum vlues of ALT, AST nd GLDH produced by ethnol + CDC feeding with greter effect on those enzymes tht reside either prtilly (AST) or totlly (GLDH) in mitochondri. It is noteworthy tht in spite of the presence of high percentge of CDC nd of hydrophobicity index lrger thn tht observed in the ethnol group, UDC dministrtion still exerted beneficil effects when compred with the ethnol group. The therpeutic effect of UDC in cholesttic diseses hs been prtly ttributed to its bility to induce choleresis nd to displce more hydrophobic bile slts from the heptocyte. In our intoxiction model, these mechnisms cnnot explin the protective ction of UDC, becuse no bile flow impirment, nd consequently no retention of toxic bile cids in heptocytes, occurred. Indeed, our dt indicte tht the biliry output of CDC ws rther similr in the ethnol + CDC nd ethnol + CDC + UDC groups. Therefore, the efficcy of UDC my be due to its cytoprotective properties. In order to explin this beneficil effect, direct interction of UDC with liver membrnes hs been suggested. First, ccording to Güldütun et l. (1993) the mechnism of UDC hepto-protection ginst hydrophobic bile slts my be linked with its cpcity to stbilize plsm membrnes. We lso found tht UDC ws n efficient plsm membrne stbilizer ginst ethnol (Beugé et l., 1996; Oliv et l., 1998). Second, recent dt indicte direct protection of liver mitochondril membrnes by UDC both ginst hydrophobic bile slts (Krähenbühl et l., 1994b; Botl et l., 1995; Benz et l., 1998; Rodrigues et l., 1998; Güldütun et l., 1999) nd ethnol-induced injury (Neumn et l., 1995; Tbouy et l., 1998). These two mechnisms re not mutully exclusive. The present results on GLDH relese

5 BILE ACIDS IN ETHANOL-INDUCED HEPATOTOXICITY 29 provide dditionl insights regrding the protective effect of UDC on mitochondri. In conclusion, the mjor finding of the current study is tht UDC prtilly protects the liver ginst the intoxiction induced by the co-dministrtion of ethnol nd CDC. This beneficil effect ppers to be independent of the choleretic properties of UDC nd my be ttributed, t lest in prt, to UDC cytoprotection on mitochondri. REFERENCES Alvro, D., Benedetti, A., Gigliozzi, A., Bini, A., Dell Grdi, P., L Ros, T., Jezequel, A. M. nd Cpoccci, L. (1995) Functionl nd ultrstructurl fetures of ethnol/bile slts interction in the isolted perfused rt liver. Heptology 21, Armstrong, M. J. nd Crey, M. C. (1982) The hydrophobic hydrophilic blnce of bile slts. Inverse correltion between reverse-phse high performnce liquid chromtogrphic mobilities nd micellr cholesterol-solubilizing cpcities. Journl of Lipid Reserch 23, Beugé, F., Choqurt, D., Oliv, L. nd Montet, J.-C. (1996) Allevition by ursodeoxycholte of liver plsm membrne disorders induced by lcohol intke in rts. Alcoholism: Clinicl nd Experimentl Reserch 20, 123A. Ben Mouz, A., Lindheimer, M., Montet, J.-C., Zjc, J. nd Lgerge, S. (2001) A study of the dsorption of bile slts onto model lecithin membrnes. Colloids nd Surfces B: Biointerfces 20, Benz, C., Angermüller, S., Töx, U., Klöters-Plchky, P., Rieder, H. D., Suer, P., Stremmel, W. nd Stiehl, A. (1998) Effect of turoursodeoxycholic cid on bile-cid-induced poptosis nd cytolysis in rt heptocytes. Journl of Heptology 28, Botl, R., Spivey, J. R., Aguilr, H., Bronk, S. F. nd Gores, G. J. (1995) Ursodeoxycholte (UDCA) inhibits the mitochondril membrne permebility trnsition induced by glycochenodeoxycholte: mechnism of UDCA cytoprotection. Journl of Phrmcology nd Experimentl Therpeutics 272, Colombo, C., Crosignni, A., Assisso, M., Bttzzti, P. M., Podd, M., Giunt, A., Zimmer-Nechemis, L. nd Setchell, K. D. R. (1992) Ursodeoxycholic cid therpy in cystic fibrosis-ssocited liver disese: dose response study. Heptology 16, Glbert, C., Montet, J. C., Lengrnd, D., Lecuire, A., Sott, C., Figrell, C. nd Chzlette, J. P. (1992) Effects of ursodeoxycholic cid on liver function in ptients with cystic fibrosis nd chronic cholestsis. Journl of Pedritrics 121, Güldütun, S., Zimmer, G., Imhof, M., Bhtti, S., You, T. nd Leuschner, U. (1993) Moleculr spects of membrne stbiliztion by ursodeoxycholte. Gstroenterology 104, Güldütun, S., Zimmer, G., Leuschner, M., Bhtti, S., Elze, A., Deisinger, B., Hofmnn, M. nd Leuschner, U. (1999) The effect of bile slts nd clcium on isolted rt liver mitochondri. Biochimic et Biophysic Act 1453, Heumn, D. M. (1989) Quntittive estimtion of the hydrophilic hydrophobic blnce of mixed bile slt solutions. Journl of Lipid Reserch 30, Heumn, D. M., Mills, A. S., McCll, J., Hylemon, P. B., Pndk, W. M. nd Vlhcevic, Z. R. (1991) Conjugtes of ursodeoxycholte protect ginst cholestsis nd heptocellulr necrosis cused by more hydrophobic bile slts. Gstroenterology 100, Heumn, D. M., Pndk, W. M., Hylemon, P. B. nd Vlhcevic, Z. R. (1991b) Conjugtes of ursodeoxycholte protect ginst cytotoxicity of more hydrophobic bile slts: in vitro studies in rt heptocytes nd humn erythrocytes. Heptology 14, Kitni, K., Kni, S., Sto, Y. nd Oht, M. (1994) Turo α-muricholte is s effective s turo β-muricholte nd turoursodeoxycholte in preventing turochenodeoxycholte-induced liver dmge in the rt. Heptology 19, Krähenbühl, S., Tlos, C., Fischer, S. nd Reichen, J. (1994) Toxicity of bile cids on the electron trnsport chin of isolted rt liver mitochondri. Heptology 19, Krähenbühl, S., Fischer, S., Tlos, C. nd Reichen, J. (1994b) Ursodeoxycholte protects oxidtive mitochondril metbolism from bile cid toxicity: dose response study in isolted rt liver mitochondri. Heptology 20, Leuschner, U., Fischer, H., Kurtz, W., Güldütun, S., Hübner, K., Hellstern, A., Gtzen, M. nd Leuschner, M. (1989) Ursodeoxycholic cid in primry biliry cirrhosis: results of controlled double-blind tril. Gstroenterology 97, Lieber, C. S. nd DeCrli, L. M. (1989) Liquid diet technique of ethnol dministrtion: 1989 updte. Alcohol nd Alcoholism 24, Neumn, M. G., Cmeron, R. G., Sher, N. H., Bellentni, S. nd Tiribelli, C. (1995) Effect of turoursodeoxycholic nd ursodeoxycholic cid on ethnol-induced cell injuries in the humn Hep G2 cell line. Gstroenterology 109, Oliv, L., Beugé, F., Choqurt, D., Montet, A.-M., Guitoui, M. nd Montet, J.-C. (1998) Ursodeoxycholte llevites lcoholic ftty liver dmge in rts. Alcoholism: Clinicl nd Experimentl Reserch 22, Plevris, J. N., Hyes, P. C. nd Bouchier, I. A. D. (1991) Ursodeoxycholic cid in the tretment of lcoholic liver disese. Europen Journl of Gstroenterology nd Heptology 3, Poupon, R. E., Blku, B., Eschwège, E., Poupon, R. nd the UDCA- PBC study group (1991) A multicenter, controlled tril of ursodiol for the tretment of primry biliry cirrhosis. New Englnd Journl of Medicine 324, Queneu, P. E., Bertult-Peres, P., Mesdjin, E., Durnd, A. nd Montet, J.-C. (1993) Diminution of n cute cyclosporin-induced cholestsis by turoursodeoxycholte in the rt. Trnsplnttion 56, Queneu, P. E., Bertult-Peres, P., Guitoui, M., Mesdjin, E., Durnd, A. nd Montet, J.-C. (1994) Improvement of cyclosporin A-induced cholestsis by turoursodeoxycholte in long-term study in the rt. Digestive Diseses nd Sciences 39, Rodrigues, C., Fn, G., M, X., Kren, B. nd Steer, C. (1998) A novel role for ursodeoxycholic cid in inhibiting poptosis by modulting mitochondril membrne perturbtion. Journl of Clinicl Investigtion 101, Spivey, J. R., Bronk, S. F. nd Gores, G. J. (1993) Glycochenodeoxycholte-induced lethl heptocellulr injury in rt heptocytes. Journl of Clinicl Investigtion 92, Tbouy, L., Zmor, A., Oliv, L., Montet, A.-M., Beugé, F. nd Montet, J.-C. (1998) Ursodeoxycholte protects ginst ethnolinduced liver mitochondril injury. Life Sciences 63, Turley, S. D. nd Dietschy, J. M. (1978) Reevlution of the 3 α-hydroxysteroid dehydrogense ssy for totl bile cids. Journl of Lipid Reserch 19, Zho, X. M. nd Montet, J.-C. (1990) Effects of bile slt supplementtion on biliry secretion in estrogen-treted rts. Journl of Nutritionl Biochemistry 1,

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