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1 Vol. 39, No. 6, August ] 996 Pages CYTOCHROME P-450 AND FREE RADICAL GENERATION IN RAT LIVER MICROSOMES UNDER THE INFLUENCE OF PROSTAGLANDIN El. V.U. Buko, V.V. Sadovnichy, Institute of Biochemistry, Belamssian Academy of Sciences, Grodno, Belams Received June 10, 1996 SUMMARY There is evidence to suggest that the mechanism of antioxidant effect of prostaglandin El. (PGE1) is due to decrease of radical species generation by cytochrome P-450 in rat liver mlcrosomes. Chronic alcohol intoxication increased NADPH oxidation, cytochrome P-450 content and NADPH-stimulated chemolunfiniscense of microsomes. Ethanol also raised superoxide dismutase (SOD) activity in microsomes. PGE 1 decreased cytochrome P-450 content, normalized NADPH oxidation, NADPH-induced chemoluminiscence and SOD activity in the liver of alcohol-treated rats. PGE developed the similar effect after microsomal induction by both acetone combined with starvation and phenobarbital normalizing all the above parameters. Therefore, PGE1 affects on both, ethanol-inducible I1E1 and phenobarbital-inducible IIB1 isoforms. Key words: INTRODUCTION antioxidant, prostaglandin, cytochrome P-450, chronic alcohol intoxication, SOD High reactive free oxygen radicals participate in a development of liver damage caused by ethanol, carbone tetrachloride and other hepatotoxins. The cytochrome P-450 system is a major contributor of superoxide anion and hydrogen peroxide generation induced by ethanol, acetone (1), carbone tetrachloride (2) and other toxic compounds. Both cytochrome P-450 and NADPH-cytochrome P-450 reductase are responsible for the free radical and hydrogen peroxide generation by liver cells. Free oxygen radicals are being constantly produced by different isoforms of cytochrome P-450. The isoform cytochrome P-450IIE1 is responsible for ethanol oxidation in liver microsomes and induced by ethanol and other organic solvents, such as acetone. This isofonn that exists in a high spine form develops a high oxidase activity and plays most important role in superoxide radical formation (3).The phenobarbital- inducible isoforms, cytochrome P-450IIB1 and IIB2, also activated oxygen that is subsequently eliminated as superoxide or peroxide anions that resulted in the disnmtation to hydrogen peroxide. The phenobarbital-inducible isoforms of cytochrome P-450 can be also induced by acetone (4). ABBREVIATION S PGE1 - prostaglandin El; PGE2 - prostaglandin E2; SOD - superoxide dismutase /96/061177M /0 Copyright 1996 by Academic" Press Australia. All rights t~f reproduction in any form reserved.
2 Cytochrome gene subfamily II represents about % of total cytochrome P-450 in liver microsomes (5).The ethanol-inducible form P-450IIE1 presents of % and phenobarbital-inducible forms P-450IIB 1 and P-450IIB2 of 25%, but other authors evaluated the percentage of the latter forms as of 45% (6). Thus, contribution of cytochrome P-450II gene subfamily in microsomal free radical formation is quite significant. The electron transfer from NADPH to NADPH-cytochrome P-450 reductase is also accompanied by free radical formation but the role of the flavoprotein as the reactive oxygen source in microsomes was doubted (2). Previously we were shown that prostaglandins E (PGE) having hepatoprotective properties acts as antioxidant decreasing lipid hydroperoxides and malondialdehyde in rat liver after chronic alcohol intoxication (7). We are assumed that tiffs effect can be connected with free radical generation in microsomes. Therefore the aim of this work is to study the PGE1 effect on cytochrome P-450 dependent system, NADPH-stimulated free radical formation and antiradical defense system in rat liver microsomes after an induction by ethanol, acetone in combination with starvation or phenobarbital. MATERIALS AND METHODS Male rats from Rappolovo colony weighing g were used. All animals had free access to stock pellet diets (Skidel, Belarus) and drinking water ad libitum. Chronic alcohol intoxication was performed by ethanol intragasral intubation in dosage 5 g/kg of body weight during 30 days. PGE1 was administered during the 10 last days of the ethanol treatment (4 mg/kg b.w., intraperitoneally) in this experiment. Acetone was treated during 3 days (5 ml/kg b.w., intragastrally, during 3 days). All animals treated with acetone were fasted during 48 hours before decapitation. PGE1 in this experiment was used intraperitoneally (4 mg/kg b.w.) during all the 3 days of the experiment. Induction of microsomes by phenobarbital was performed by intraperitoneal injection (80 mg/kg b.w., 2 days). PGE1 in this case was treated during 2 days intraperitoneally (4 mg/kg b.w.). Each group consists of 8 animals. Hemoglobin and other blood proteins were removed from the liver by the liver perfusion using 1.15% solution of potassium chloride. Liver was removed and homogenized using Potter-Elveheim homogenizer with a teflon pestle. Microsomal fraction was isolated by differential centrifugation of postmitochondrial supematant at g using centrifuge VAC-602 (Janetzki, Germany) accordingly by Karusina and Archakov (8).The microsomal pellet was resuspended in 0.1 M Tris-HC1 buffer (ph 7.4). Microsomal protein was determined according by Lowry et al. (9). The cytochrome P-450 content in microsomes was determined from the carbon monoxide difference spectrum upon dithionite reduction according to Omura and Sato (10). NADPH-cytochrome P-450 reductase activity was measured as described by Dallner (11). NADPH-oxidase activity was determined by a registration of the decrease in absorbance at 340 nm (12). Microsomal ethanol oxidizing system (MEOS) activity was measured by following the decrease in absorbance of NADPH at 340 nm according to Lieber and De Carli (13). Superoxide dismutase (SOD) activity was measured as performed by Beauchamp and Fridovich (14). The ferrous thiocyanate method was used for a determination of hydrogen peroxide formation as described by Hildebrandt (15). NADPH-dependent 1178
3 microsomal free radical generation was evaluated by chemoluminometric method with amplification by luminol using chemiluminometer "KhLM-063" (Russia). Data presented in this paper represent mean + S.E.M. of at least 8 experiments. Statistical significance was assessed by Student' s t test. RESULTS AND DISCUSSION Long term ethanol administration leads to an increase of cytochrome P-450 contem in liver microsomes, whereas NADPH-cytochrome P-450 reductase activity being unchanged (Table 1). Alcohol treatment activates microsomal oxidation of NADPH and ethanol. At the same time NADPH-dependent chemiluminescence amplificated by luminol and SOD activity were significantly increased. Hydrogen peroxide formation in liver microsomes of the ethanol-treated group was unchanged. The treatment of ethanol-intoxicated rats with PGE1 decreased the cytochrome P-450 level and MEOS activity below the control level. PGEI normalized the NADPH-dependent chemolunfiniscence of microsomes and SOD activity and increased the NADPH-oxidase activity. The combination of an acetone treatment with starvation activated NADPH-oxidation and NADPH-cytochrome P-450 reductase (Table 2). Cytochrome P-450 content in liver microsomes was increased. Acetone treatment and starvation significantly increased NADPH-dependent chemoluminiscence of microsomes, SOD activity and hydrogen peroxide formation. PGE I normalized most of parameters changing by acetone treatment combined with 48 hours starvation. PGE 1 decreased cytochrome P-450 and hydrogen peroxide formation, NADPH-oxidation, NADPH-cytochrome P-450 reductase activity and NADPH-dependent chemoluminiscence. The decrease of SOD activity after PGE 1 treatment was not significant. Phenobarbital that is a very strong inductor of microsomal oxidizing system (16) leads to a near two-fold increase NADPH-oxidase and NADPH-cytochrome P-450 reductase activities (Table 3). Activities of MEOS, SOD and NADH-oxidase were also increased after phenobarbital treatment. Content of cytochrome P-450 was elevated more than 2-fotd. Hydrogen peroxide formation was also enhanced in this group. PGE1 normalized NADPHoxidase, NADPH-cytochrome P-450 reductase and MEOS activities in phenobarbital-treated rats and decreased cytochrome P-450 content and SOD activity. At the same time PGE 1 treatment did not change NADPH-dependent chemoluminiscence amplificated by luminol and hydrogen peroxide production. The significant increase of cytochrome P-450 content under the influence of chronic alcohol intoxication, the treatment with acetone combined with starvation or phenobarbital treatment as well as the elevation of NADPH-cytochrome P-450 reductase (in two last groups) and NADPH oxidase activities suggest on an induction of microsomal cytochrome 1179
4 Table 1 Effect of PGE~ on rat liver monooxygenase and antioxidative system parameters of rat liver microsomes in chronic alcohol intoxication Control Ethanol Ethanol+ PGE~ Parameters CytochromeP-450& * *# NADH-cytochrome P " " "# Hydrogen peroxide Superoxide dismutase, % of blocked activite " # NADPH-dependent chemoluminescence, c.p.m./s per mg of protein * - expressed as nmol/min per mg of protein & - expressed as nmol per mg of protein * - p<0.05 compared to the control group # - p<0.05 compared to the ethanol-treated group P-450 dependent oxidation system in all the three experiments. Acetone and ethanol induce rat liver proteins related to two different isoforms of cytochrolne P-450: acetone alone or in combination with starvation induced mainly cytochrome P-450 B gene subfamily and, to a less extent, cytochrome P-450IIE 1 whereas under ethanol intoxication take place a reverse situation (17). These authors indicated that phenobarbital decreased cytochrome P-450IIE1 content and dramatically increased amounts of cytochrome P-450 related to B gene 1180
5 BIOCHEMISTRYond MOLECULAR BIOLOGY INTERNATIONAL Table 2. Effect of PGE~ on monooxigenase and antioxidative system parameters in liver microsomes from either acetone-treated and starved 48 h rats. Parameters Control Acetone + starvation Acetone + starvation + PGE~ Cytochrome P-450& " NADH-cytochrome P * * # Hydrogen peroxide production & " "# Superoxide dismutase, % of blocked activity " # NADPH-dependent chemoluminescence, c.p.m./s per mg of protein * - expressed as nmol/min per mg of protein & - expressed as nmol per mg of protein * - p<o.05 compared to the control group # - p<o.05 compared to the acetone-treated and starved group subfamily (IIBI,IIB4). We can assmne that in our experiments chronic alcohol intoxication increased cytochrome P-450IIE 1 content whereas the induction of microsomal oxidation system by phenobarbital or by acetone with starvation is realized mainly via an increase of cytochrome P-450IIB isoforms. An elevation of hemoprotein content in microsomes is probably a main factor leading to changes of other parameters of NADPH-dependent microsomal oxidation system. 1181
6 Table 3 Effect of PGEt on of rat liver monooxygenase and antioxidative system parametrs after the induction of rat liver microsomes by phenobarbital. Parameters Control Phenobarbital Phenobarbital+ PGE, Cytochrome P-450 & * *# NADH-cytochrome P * # * # * # Hydrogen peroxide produc " * Superoxide dismutase, * *# % of blocked activity NADPH-dependent chemoluminescence, c.p.m./s per mg of protein * - expressed as nmol/min per mg of protein & - expressed as nmol per mg of protein * - P< 0.05 compared to the control group # - P< 0.05 compared to the phenobarbital- treated group PGE1 decreased or completely normalized all investigated parameters of this systcnl increased under an influence of ethanol, acetone with starvation or phenobarbital. The decrease of a total cytochrome P-450 content by PGE1 in liver mierosomes of rats treated with ethanol as well as with acetone or phenobarbital suggest that PGE1 affects on both induced forms of cytochrome P-450, IIE1 and IIB1. Hepatoprotective effect of syuthetic derivative of PGE2, 16,16-dimethyl PGE2 was observed after intoxication of mouses with brombenzene (18). Moreover, PGE2 normalized cytochrome P-450 content ill the liver decreasing by brombenzene. 16,16-Dimethyl-PGE2 improved the maintenance of 1182
7 cytochrome P-450 content, NADPH-eytochrome c reduetase and the mixed function oxidases in the hepatocyte culture from Hooded-Lister strain changing during incubation (19). Thus, PGE and its derivatives normalized cytochrome P-450 functions in different physiological and pathological conditions. It is known that PGE interacts with cytochrome P-450 from liver changed his spectral parameters (20). Earlier we were shown that PGE, containing a carbonyl group are able to form covalent and non-covalent bounds with human serum albumin (21) and prostaglandin receptors of liver plasma membranes (22). Carbonyl group of PGE interact with T-amino group of lysine residue of these proteins. It is also possible an interaction of PGE with sulfhydryl groups of proteins forming semimercaptals. Modification of cytochrome P-450 by as well as NADPH-cytochrome c reductase having lysine residue (23) in the active center can lead to a decreasing of cytochrome P-450 dependent system activity. The antiradical activity of PGE 1 clearly showed in all experimental groups. The decrease of NADPH-induced chemoluminiscence and SOD activity increased by all the three microsomal inducers indicate on this effect. PGEI also decreased hydrogen peroxide formation in acetone- and phenobarbital-treated groups. Thus, antiradical effect of PGE is developed by a decrease of free radical concentration that in turn leads to a decrease or to normalization of other parameters related to free radical dependent processes. We suggest that this effect of PGE1 is connected with a decrease of cytochrome P-450 content and, probably, NADPH-cytochrome P-450 reductase activity that are very important sources of free oxygen radicals in the liver. We can also postulate that one of the mechanisms of the PGE 1 hepatoprotective action is related to antiradical activity of this compound. REFERENCES 1. Ekstrom G. and Ingelman-Sunberg M. (1989) Biochem. Phamlacol. 38, Persson J.O., Terelius Y. and Ingelman-Sundberg M. (1990) Xenobiotica, 20, Tindberg N. and Ingelman-Sundberg M.(1989) Biochem. 28, Ronis M.J. and Ingehnan-Sundberg M. (1989) Xenobiotica, 19, Schenkman J.B., Thummel K.E. and Favrean L.V. (1989) Drug Metab. Rev. 20, hnaoka. S., Terano Y. and Funae Y. (1987) Biochem. Biophys. Acta, 916, Buko V. (1991) Zeitschrift ffir Gastroenterology, 29, Karnzina I.I., Archakov A.I. (1977) in Modern Techniques in Biochemistry (Orekhovich, Ed.) pp , Meditsina Publishers, Moscow. 9. Lowry O.N., Rosebrough N.G., Farr A.L. at al. (1951) J.Biol.Chem. 193, Omura T., Sato R. and Cooper D.G. (1965) Fed. Proc., 24, Dallner G.(1963) Acta pathol, microbiol, scand., 166, Gillette I.R., Brodie B.B. and La Du N. (1957)J. Pharmacol. Exp. Ther. 119, Lieber C.S., De Carli L.M. (1970) J. Biol. Chem. 245, Beauchamp C. and Fridovich I. (1971) Anal. Biochem. 44,
8 15. Hildebrandt A.G., Roots I., Tjoe M. et al. (1978) Methods Enzymol. 52, Guengerich G.A., Wlight S.T., Martin M.V. et al. (1982) Biochem. 21, Johansson I., Eliasson E., Norsten C. et al. (1986) FEBS Lett. 196, Funck-Brentano C., Tinel M., Degott C. et al. (1984) Biochem. Pharmacol. 33, Grant M.H., Smith S.J., and Burke M.D. (1986) Biochem. J., 239, Kupfer D., Jansson I., Favreau L.V. et al. (1988) Arch. Biochem. Biophys., 261, Buko V.U., Zavodnik I.B. and Lapshina E.A. (1990) Biokhimia (Eng. Tr.) 55, Buko V.U. and Zavodnik I.B. (1990)Alcohol and Alcoholism, 25, Slepneva I.A. and Weiner L.M. (1988) Biochem. Biophis. Res. Commun. 155,
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