PROGESTERONE RECEPTORS IN HUMAN UTERINE CYTOSOL
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1 Br. J. lin. Pharma. (1983), 15, THE INTERACTION OF CANRENONE WITH OESTROGEN AND PROGESTERONE RECEPTORS IN HUMAN UTERINE CYTOSOL M. DOLORES FERNANDEZ1, GRAHAM D. CARTER' & T. NORMAN PALMER2 Departments of 'Chemial Pathology and 2Biohemistry, Charing Cross Hospital, Fulham Palae Road, London W6 8RF 1 Canrenone, the major ative metabolite of spironolatone, dereased [3H]-progesterone binding to isolated uterine ytosoli progesterone reeptors. The inhibition was onentration-dependent. 2 Canrenone did not alter [3H]-oestradiol binding to isolated uterine ytosoli oestrogen reeptors. 3 Canrenone inhibition of progesterone binding to isolated ytosoli reeptors was stritly ompetitive: Kd (apparent dissoiation onstant for progesterone binding) was inreased in a onentrationdependent manner by anrenone, whereas Bmax (maximal number of progesterone binding sites/mg ytosoli protein) was unaltered. There was marked ooperativity in progesterone binding at high anrenone and low progesterone onentrations. The impliation is that anrenone alters the subunit interation of the reeptor protein. 4 Kd for progesterone was 3.2 x 1-9 M. K, (the inhibition onstant for anrenone with respet to progesterone binding) was 3 x 1-9M. Reports in the literature suggest that, following spironolatone administration, anrenone may rise to onentrations suffiiently high to inhibit progesterone binding. This ation may ontribute to the effet of spironolatone in induing menstrual disturbanes in female patients. Introdution Spironolatone, a syntheti steroid latone (spirolatone) ats as a speifi ompetitive mineraloortioid antagonist (Kagawa, 196; Drill, 1962). It is used linially as a potassium-sparing diureti and as an antihypertensive agent (Ohs et al., 1978). Reent reports have indiated that the drug may also benefit some patients with hirsutism due to benign androgen exess (Shapiro et al., 198; Boisselle & Tremblay, 1979; Ober et al., 1978). The primary ative metabolite of spironolatone is the de-thioaetylated derivative anrenone (17,8 hydroxy-3-oxo-pregna-4, 6-diene-21-arboxyli aid -y-latone) (Gohman & Gantt, 1962; Karim et al., 1976; Karim, 1978). It is reported (Ramsay et al., 1977) that more than 7% of the renal antialdosterone ativity of spironolatone may be speifially attributed to anrenone. The metabolism and exretion of anrenone is biphasi and slow (Karim et al., 1976). Animal studies suggest that the pharmaologial effets of spironolatone as an antimineraloortioid are due to the speifi inhibition of the binding of aldosterone to ytoplasmi reeptors (Fanestil, 1968; Funder et al., 1974). Other authors have reported spironolatone inhibition of the binding of androgens (Raynaud et al., 1975; Corvol et al., 1975; Boiselle et al., 1979) to their reeptors. There is also a report ,83,1-95 $2.() (Levy et al., 198a) that spironolatone inhibits oestradiol binding to its ytosoli reeptor in rat uterus but this only applies at high onentrations and is of doubtful physiologial signifiane. The inhibition of testosterone binding oupled to inhibition of androgenesis (Menard et al., 1974) may aount for the gynaeomastia reported as a sideeffet of spironolatone therapy (Clark, 1965; Rose et al., 1977; Hufffman etal., 1978). This is not the only side-effet. Menstrual disturbanes are reported in female patients (Levitt, 197; Loriaux et al., 1976). Following a reent study arried out in our Endorine Unit in whih 7 out of 12 hirsute women reeiving spironolatone developed menstrual irregularities, it was deided to investigate the effet of anrenone on the binding of oestrogen and progesterone to reeptors in human uterine ytosol. Methods Materials [2, 4, 6, 7-3H]-Oestradiol (speifi ativity: Ci/mmol) and [1, 2, 6, 7-3H]-progesterone (speifi ativity: 8-11 Ci/mmol) were supplied by Amersham International. For some investigations, [3H] Blakwell Sientifi Publiations
2 96 M. DOLORES FERNANDEZ, GRAHAM D. CARTER & T. NORMAN PALMER progesterone was purified on a 5 m olumn of Sephadex LH-2 (Pharmaia) using the solvent system benzene:methanol (17:3). The fration ontaining peak radioativity was used. Canrenone was a gift of Searle laboratories. Cortisol, diethylstilboestrol and norethisterone were purhased from Sigma Chemial Company. Ativated haroal was supplied by Sigma Chemial Company. Fines were removed by repeated washings with distilled water. Tissue preparation Uterine tissue (myometrium) from eight premenopausal women undergoing hysteretomy was pulverized in a morodismembrator (Braun Instruments Ltd, W. Germany) and the powder resuspended in buffer (1mM phosphate, 1.5 mm dik EDTA, 1 mm monothioglyerol; ph = 7.4, ontaining 3% glyerol) to a onentration of 1:8 w/v. All subsequent proedures were arried out at 4 C. The suspension was stirred for 1 min followed by entrifugation at 2 g for 15 min. The supernatant ('rude' ytosol) was used in preliminary investigations into the binding of [3H]-oestradiol and [3H]-progesterone to their reeptors in the presene or absene of anrenone. A 'pure' ytosol was prepared aording to the method desribed by Ogle (1981). The 'rude' ytosol desribed previously was inubated with a suspension of.5% haroal/.5% dextran to strip it of endogenous steroid. After inubating for 1 min, the mixture was entrifuged at 154 g for 5 min and the supernatant used to haraterise the inhibitory effet of anrenone on the binding of [3H]- progesterone to its reeptors. Cytoplasmi oestrogen reeptor assay The method used is based on that of King et al. (1979). Dupliate aliquots (2 Ml) of 'rude' ytosol were inubated overnight with 4.2 nm [3H]-oestradiol in the presene or absene of a 2 fold exess of diethylstilboestrol in a final volume of 24 ul. The unbound oestradiol was removed by inubating for 1 min with 24 ul of.5% haroal/.5% dextran T-7 in 1 mm Tris/1 mm EDTA buffer; ph = 7.4. After entrifuging for 1 min at 2 g, 25 MAI of supernatant were ounted in 2 ml sintillation fluid (Pio- Fluor 3, Pakard). Speifi binding sites were estimated from the differenes in radioativity between inubations with and without diethylstilboestrol. Although stritly a measure of [3H]- oestradiol binding at 4.2 nm, results are expressed as the onentration of oestrogen reeptors. Cytoplasmi progesterone reeptor assay The method used is based on that of King et al. (1979). Dupliate aliquots (2 1,u) of 'rude' ytosol were inubated overnight with 7.7 nm [3H]- progesterone/1,mm ortisol in the presene or absene of a 1 fold exess of norethisterone in a final volume of 26,ul. The unbound [3H]-progesterone was separated and ounted as in the ytoplasmi oestrogen reeptor assay but the inubation with dextranoated haroal was shortened to 5 min. The results are shown as progesterone reeptor onentration although stritly this expression is a measure of [3H]- progesterone binding at 7.7 nm. Effet of anrenone on [3H]-oestradiol binding to reeptors in uterine ytosol Canrenone was added to dupliate aliquots (2,ul) of a 'rude' uterine ytosol preparation to give final onentrations ranging between nm and inubated with 4.2 nm [3H]-oestradiol in the presene or absene of a 2-fold exess of diethylstilboestrol (total volume of 24,ul). All subsequent proedures were arried out as desribed for the ytoplasmi oestrogen reeptor assay. Canrenone inhibition of [3H]-oestradiol binding to uterine reeptors was investigated in a total of three 'rude' ytosol preparations. Effet of anrenone on [3H]-progesterone binding to reeptors in uterine ytosol Canrenone was added to dupliate aliquots (2,ul) of a 'rude' uterine ytosol preparation to give final onentrations ranging between nm. They were inubated with 7.7 nm [3H]-progesterone/1 Mm ortisol in the presene or absene of a 1 fold exess of norethisterone (total volume of 26,l). All subsequent proedures were arried out as desribed for the ytoplasmi progesterone reeptor assay. Canrenone inhibition of [3H]-progesterone binding to uterine reeptors was investigated in a total of four 'rude' ytosol preparations. Charaterization of the inhibition by anrenone of [3H]-progesterone binding to uterine reeptors Dupliate aliquots (2 Ml) of 'pure' uterine ytosol were added to six onentrations of purified [3H]- progesterone, ranging between nm in the presene or absene of a 1 fold exess of unlabelled progesterone. Cortisol was added to all tubes to give a onentration of 1,UM in a final volume of 26 Ml. Additionally, eah onentration of progesterone was inubated in the presene of different amounts of anrenone (range -125 nm). After overnight inubation, all tubes were treated as desribed for the ytoplasmi progesterone reeptor assay.
3 INTERACITION OF CANRENONE WITH HUMAN UTERINE RECEPITORS 97 Protein estimation Cytosol protein was estimated using the Lowry tehnique (Lowry et al., 1951). Results Canrenone interation with [3H]-oestradiol and [3JH]- progesterone binding to uterine reeptors The initial objetive was to establish whether anrenone inhibits the binding of [3H]-oestradiol and/or [3H]-progesterone to their respetive ytosoli reeptors. The binding of [3H]-oestradiol (4.2 nm) to its speifi reeptor in one representative ytosoli preparation (oestrogen reeptor onentration = 66 fmol/mg ytosoli protein) at varying anrenone onentrations (-2515 nm) is shown in Figure la. Regardless of the anrenone onentration, the binding of [3H]-oestradiol was onstant; binding was 96.6% (expressed as the perentage of the total [3H]-oestradiol bound in the absene of anrenone ± s.e. mean). Other experiments showed similar results. The orresponding effet of anrenone (-4666 nm) on the binding of [3H]-progesterone (7.7 rm) to its speifi ytosoli reeptor is shown in Figure lb. These ombined data (+ s.e. mean) are from experiments arried out with four premenopausal uterine ytosols. The progesterone reeptor onentrations were 729, 481, 1168 and 497 fmol/mg ytosol protein. As the anrenone onentration inreased, the binding of [3H]-progesterone (expressed as the perentage of the total [3H]-progesterone bound in the absene of anrenone ± s.e. mean) dereased: 5% apparent inhibition of progesterone binding by anrenone was at nm (mean + s.e. mean). Nature of the inhibition of progesterone binding by anrenone To eluidate the type of inhibition by anrenone, [3H]-progesterone (.54;.65,.79, 1.39, 5.95 and 1.8 nm) binding to uterine reeptors at various anrenone onentrations (, 15.4, 84.6, 154, 846, and 3384 nm) was investigated. Plots of [3H]- progesterone bound (pmol/mg ytosoli protein) v. total [3H]-progesterone onentration are shown in Figure 2a. At low anrenone onentrations these plots were onsistently hyperboli. Thus, the interation of progesterone with its ytosoli reeptor learly omplies with a Mihaelis-Menten-type equation: b Bmax [P] Kd + [P] where b = the amount of progesterone bound to reeptor at progesterone onentration [P]. Kd = apparent dissoiation onstant of the reeptor for progesterone. Bmax = the maximum number of progesterone binding sites per mg ytosoli protein. At high anrenone onentration, the plot [3H]- progesterone bound v total [3H]-progesterone showed evidene of sigmoidiity. To haraterise and quantify the inhibition, double reiproal (i/progesterone bound v 1/progesterone onentration) Lineweaver-Burk plots were onstruted (Figure 2b). The plots at anrenone onen- 12 F a 12 b '. ~ Co U) a) 1 I 8 F a 1 'a 8, 6 OD CD 4 ) 2 2 L I' I I 1 1 1, 1, 1, 1 1 1, 1, Canrenone (nm) Canrenone (nm) Figure 1 Effet of inreasing onentrations of anrenone on the binding of (a) 4.2 nm [3H]-oestradiol (expressed as a perentage of the binding in the absene of anrenone, n = 1) and (b) 7.7 nm [3H]-progesterone (expressed as a perentage of the binding in the absene of anrenone + s.e. mean, n = 4) to uterine ytosol reeptors.
4 98 M. DOLORES FERNANDEZ, GRAHAM D. CARTER & T. NORMAN PALMER a b a.5.6 E E QL *.4. ",.2.._ E -. Ez- C 3. C ~ Progesterone (nm) 1/[Progesterone] Figure 2 Effet of anrenone on progesterone binding to isolated uterine reeptors. The binding of progesterone to reeptors was determined at zero (), 15.4 (h), 84.6 (), 154 (), 846 (A) and 3384 (U) nm anrenone. Results are shown as (a) a plot of progesterone bound (pmol/mg protein) v progesterone onentration (nm) (primary plot) and (b) a double reiproal plot of 1/progesterone bound (pmol/mg protein) v liprogesterone onentration (Lineweaver-Burk plot). The inset () shows in detail the double reiproal plot of the uninhibited reation. trations of, 15.4, 84.6 and 154 nm were fitted by linear regression analysis whereas those at onentrations of 846 and 3384 nm were fitted by hand. The resultant six lines interepted the y axis at a ommon point. This is onsistent with a stritly ompetitive inhibition. At anrenone onentrations of 846 and 3384 nm the plots were upward-infleting urves, as would be predited from the sigmoidiity of the orresponding primary plots. Figure 2 shows in detail the double reiproal plot of progesterone binding in the absene of anrenone. The omputed Kd (taken from the interept with the x axis) is 3.2 x 1-9 M. Bmax (taken from the interept with the y axis) is 99 fnol/mg ytosoli protein. Quantitative aspets ofbinding inhibition by anrenone Figure 3a shows the derived Dixon plot (1/progesterone bound v anrenone onentration). Ki (the inhibition onstant) was alulated from the point of intersetion of the plots on the negative side of the x axis (interept = -K*). K; was approximately 3 x 19M. The degree of ooperativity of the progesterone/ anrenone interation was evaluated using the Hill plot (Figure 3b. This plot is of log (b/bmax -b) (log of the ratio of oupied: unoupied binding sites) v log [P] (log progesterone onentration). The slope of the lines gives the Hill oeffiient (n), a measure of ooperativity. The oeffiients approximated to unity exept at high anrenone and low progesterone onentrations. Values of 2.1 and 2.4 were obtained at anrenone onentrations of 846 and 3384 nm respetively. Disussion The present study was prompted by observations made during a linial trial of spironolatone in the treatment of hirsutism. Of the twelve women who reeived the drug, seven developed side effets whih suggested interferene with the hormonal ontrol of menstruation. Although other workers have investigated the interaition between spironolatone and oestrogen (Raynaud et al., 1975; Rifka et al., 1978; Levy et al., 198a,b) and progesterone (Raynaud et al., 1975) reeptors, the signifiane of their results in man is questionable sine most of the investigations were arried out in animals. Another limitation has been the almost exlusive use of spironolatone itself. Sine up to approximately 8%
5 INTERACTION OF CANRENONE WITH HUMAN UTERINE RECEPTORS g9 a b.- Ix ne I o Canrenone (PM) 1 Log [Progesterone] (nm) Figure 3 Type of inhibition by anrenone of progesterone binding. The results from Figure 2 were used to onstrut (a) a Dixon plot (i.e. I/progesterone bound (pmol/mg protein) vs. anrenone onentration (Mm). (b) shows the derived Hill plot i.e. log [b/bm.,-b] v log [progesterone] (nm). The slope of the lines gives the Hill oeffiient, n. Values of n were onsistently approximately unity exept with 846 nm (A) and 3384 nm (-) where at low progesterone onentrations below.65 and.79 nm respetively, n was 2.1 and 2.4 respetively. The symbols are those used in Figure 2. of drug is known to be onverted to the biologially ative derivative anrenone (Karim, 1978), this important metabolite was hosen for the present study. In ontrast to the negative results obtained with oestradiol, there was unequivoal inhibition of progesterone binding by anrenone. Uterine ytosol preparations from four premenopausal women with widely different reeptor onentrations exhibited a remarkably onsistent pattern of inhibition. Double reiproal plots showed this inhibition to be stritly ompetitive in nature; viz. Kd was inreased by anrenone in a onentration-dependent manner, whereas Bmax was unhanged. Thus, it appears that anrenone and progesterone ompete for a ommon binding site(s) on the ytosol reeptor. Under onditions of low progesterone/high anrenone onentrations, there appears to be signifiant positive ooperativity in progesterone binding. This is implied by the sigmoidiity of primary plots (Figure 2a), and the upward infletion of the Lineweaver-Burk replots (Figure 2b). The degree of ooperativity is evident from the Hill oeffiient (n) whih assumes values signifiantly greater than unity at the two highest anrenone levels when progesterone onentration falls to below.65 and.79 rm respetively. These findings (albeit based on limited data) are onsistent with an allosteri model. whih proposes that the progesterone reeptor onsists of two protomeri subunits (see review by Mainwaring, 198). Presumably anrenone modifies the interation of these subunits. Of the various approahes to the determination of Ki, the Dixon plot appeared to be the most satisfatory. The determined Ki of 3 x 1-9M (f. Kd = 3.2 x 1-9 M) indiates that anrenone is a poor inhibitor of progesterone binding, its affinity for the reeptor being approximately one hundred times lower than that of progesterone. Nevertheless, this figure falls within the published range for plasma anrenone whih an reah values of 12 nm following 1-2 mg doses of spironolatone (Karim, 1978). There are no published data speifially giving onentrations in human uterus but studies in rats suggest that anrenone levels in most tissues exeed that of plasma (Karim, 1978), although some may be extraellular and protein bound. Sine spironolatone an be given in doses of up to 4 mg, it seems reasonable to suppose that therapeuti amounts of the drug would result in at least partial inhibition of progesterone binding to uterine ytosol reeptors. The degree to whih this inhibition ontributes to the menstrual problems assoiated with spironolatone therapy is diffiult to assess. Interpretation is
6 1 M. DOLORES FERNANDEZ, GRAHAM D. CARTER & T. NORMAN PALMER further ompliated by our use of myometrium rather than endometrium whih we were unable to Qbtain in adequate quantities. There is some evidene that progesterone reeptors in the two tissues are not struturally idential (Verma & Laumas, 1973). These differenes notwithstanding, the linial onsequenes of reeptor binding of anrenone will depend on the interplay of several fators. Not least in importane is the possibility that the anrenonereeptor omplex might itself be ative. Although Kagawa (196) and Kagawa et al. (1964) failed to demonstrate a progestational or antiprogestational effet in animals, a more reent report (Shane & Potts, 1978) indiates that spironolatone delays withdrawal bleeding in oestrogenised monkeys. The latter report taken in onjuntion with linial findings of menstrual irregularities and our own in vitro studies leads us to speulate that spironolatone may at both as a progestogen and an anti-progestogen. If so, this may aount for the finding of polymenorrhoea in some women and oligomenorrhoea in others. Referenes BOISSELLE, A. & TREMBLAY, R.R. (1979). New therapeuti approah to the hirsute patient. Fert. Ster., 32, BOISSELLE, A., DIONNE, F.T. & TREMBLAY, R.R. (1979). Interation of spironolatone with rat skin androgen reeptor. Can. J. Biohem., 57, CLARK, E. (1965). Spironolatone therapy and gyneomastia. J. Am. med. Ass., 193, CORVOL, P., MICHAUD, A., MENARD. J., FRIEFELD, M. & MAHOUDEAU, J. (1975). Antiandrogeni effet of spirolatones: Mehanism of ation. Endorinology, 97, DRILL, V.A. (1962). The aldosterone bloking effets of spirolatones. Jap. J. Pharma., 11, FANESTIL, D.D. (1968). Mode of spinolatone ation: ompetitive inhibition of aldosterone binding to kidney mineraloortioid reeptors. Biohem. Pharma., 17, FUNDER, J.W., FELDMAN, D., HIGHLAND, E. & EDELMAN, I.S. (1974). Moleular modifiations of anti-aldosterone ompounds: effets on affinity of spirolatones for renal aldosterone reeptors. Biohem. Pharma., 23, GOCHMAN, N. & GANTT, C.L. (1962). A fluorimetri method for the determination of a major spironolatone (Aldatone) metabolite in human plasma. J. Pharma. exp. Ther., 135, HUFFMAN, D.H., KAMPMANN, J.P., HIGNITE, C.E. & AZARNOFF, D.L. (1978). Gyneomastia indued in normal males by spironolatone. Clin. Pharma. Ther., 24, KAGAWA, C.M. (196). Bloking the renal eletrolyte effets of mineraloortioids with an orally ative steroidal spirolatone. Endorinology, 67, KAGAWA, C.M., BOUSKA, D.J., ANDERSON, M.L. & KROL, W.F. (1974). Pharmaologial properties of a mineraloortioid antagonist (SC-14266). Arh. int. Pharmaodyn., 149, KARIM, A. (1978). Spironolatone: Disposition, metabolism, pharmaodynamis and bioavailability. Drug Metab. Rev., 8, KARIM, A., ZAGARELLA, J., HRIBAR, J. & DOOLEY, M. (1976). Spironolatone. I. Disposition and metabolism. Clin. Pharma. Ther., 19, KING, R.J.B., REDGRAVE, S., HAYWARD, J.L., MILLIS, R.R. & RUBENS, R.D. (1979). The measurement of reeptors for oestradiol and progesterone in human breast tumours. In Steroid reeptors assays in human breast tumours: Methodologial and linial aspets, ed. King, R.J.B., pp Cardiff: Alpha Omega Alpha. LEvrrr, JI. (197). Spironolatone therapy and amenorrhea. J. Am. med. Ass., 211, LEVY, J., BURSHELL, A., MARBACH, M., AFLLALO, L. & GLICK, S.M. (198a). Interation of spironolatone with oestradiol reeptors in ytosol. J. Endorinol., 84, LEVY, J., BURSHELL, A., MARBACH, M., AFLLALO, L. & GLICK, S.M. (198b). Estrogeni ativity of drugs known to ause gyneomastia. In Pharmaologial modulation of steroid ation, ed. Genazzani, E. et al., pp New York: Raven Press. LORIAUX, D.L., MENARD, R., TAYLOR, A., PITA, J.C. & SANTEN, R. (1976). Spironolatone and endorine dysfuntion. Ann. int. Med., 85, LOWRY, O.H., ROSEBROUGH, N.J., FARR, A.L. & RANDALL, R.J. (1951). Protein measurement with the folin phenol reagent. J. biol. Chem., 193, MAINWARING, W.I.P. (198). Steroid reeptors. In Cellular reeptors for hormones and neurotransmitters, eds Shulster, D. & Levitzki, A., pp Chihester, New York, Brisbane & Toronto: John Wiley & Sons Ltd. MENARD, R.H., STRIPP, B. & GILLETTE, J.R. (1974). Spironolatone and testiular ytohrome P-45: dereased testosterone formation in several speies and hanges in hepati drug metabolism. Endorinology, 94, OBER, K.P. & HENNESSY, J.F. (1978). Spironolatone therapy for hirsutism in a hyperandrogeni woman. Ann. int. Med., 89, OCHS, H.R., GREENBLA1T, D.J., BODEM, G. & SMITH, T.W. (1978). Spironolatone. Am. Heart J., 96, OGLE, T.F. (1981). Kineti and physiohemial harateristis of an endogenous inhibitor to progesteronereeptor binding in rat plaental ytosol. Biohem. J., 199, RAMSAY, L., ASBURY, M., SHELTON, J. & HARRISON, I. (1977). Spironolatone and anrenoate-k: relative poteny at steady-state. Clin. Pharma. Ther., 21, RAYNAUD, J.P., BONNE, C., BOUTON, M.M., MOG- VILEWSKY, M., PHILIBERT, D. & AZADIAN- BOULANGER, G. (1975). 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7 INTERACTION OF CANRENONE WITH HUMAN UTERINE RECEPTORS 11 LORIAUX, D.L. (1978). Interation of digitalis and spironolatone with human sex steroid reeptors. J. lin. Endorinol. Metab., 46, ROSE, L.I., UNDERWOOD, R.H., NEWMARK, S.R., KISCH, E.S. & WILLIAMS, G.H. (1977). Pathophysiology of spironolatone indued gyneomastia. Ann. int. Med., 87, SHAPIRO, G. & EVRON, S. (198). A novel use of spironolatone: Treatment of hirsutism. J. lin. Endorinol. Metab., 51, SCHANE, H.P. & POTTS, G.O. (1978). Oral progestational ativity of spironolatone. J. lin. Endorinol. Metab., 47, (3), VERMA, U. & LAUMAS, K.R. (1973). In vitro binding of progesterone to reeptors in the human endometrium and the myometrium. Biohim. biophys. Ata., 317, (Reeived June 9, 1982 aepted September27, 1982)
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