Effects of progesterone, progestogens, and danazol on the specific cortisol binding in human plasma*
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1 FERTUTY AND STERUTY Copyright Q 1985 The American Fertility Society Vol. 43, No. 6, June 1985 Printed in U.S A. Effects of progesterone, progestogens, and danazol on the specific cortisol binding in human plasma* Ulla-Britt Ottosson, M.D.t Bo Nilsson, M.D. Ragnar SOdergard, M.D. Bo von Schoultz, M.D. Department of Obstetrics and Gynecology, University Hospital, Umea, Sweden The interaction of medroxyprogesterone acetate (MPA) with cortisol binding to corticosteroid-binding globulin (CBG) was studied with the use of an aqueous two phase system with polyethylene glycol and dextran for equilibrium partition. Competitive binding analyses were also performed for progesterone (P), levonorgestrel, norethisterone, danazol, and tamoxifen. P and danazol were found to exert cortisol displacing activity, whereas MPA and the other tested compounds had no such effect. The glucocorticoid effects reported for MPA could not be explained by displacement. n general, P serum concentrations are lower than those of cortisol, and most binding sites on CBG are occupied by the glucocorticoid. At high P levels displacement and an increase in free cortisol may occur. Danazol displacement of cortisol is hampered by its pronounced albumin binding. n conclusion, none of the tested compounds should increase free and biologically active cortisol during normal clinical treatment. Fertil Steril 43:856, The interaction between steroids and circulat ing specific binding proteins may interfere with the clinical effects of hormonal therapy. Among the various synthetic progestogens that are used to mimic the effects of natural progesterone (P), the 19-nor steroids, like levonorgestrel and nor ethisterone, are known to compete with testoster one (T) for the binding to sex-hormone-binding globulin (SHBG). 1 2 Danazol, which is another T derivative and frequently used in the treatment Received August 28, 1984; revised and accepted February 7, *Supported by grants from the Swedish Medical Research Countil (5982) and the Medical Faculty, University of Umea. treprint requests: Dr. Ulla-Britt Ottosson, Department of Obstetrics and Gynecology, University Hospital, S Umea, Sweden. 856 Ottosson et al. Progestogens and cortisol binding of endometriosis, has also been found to bind to SHBG with high affinity.3 These compounds, by competitive binding and displacement, may in crease the amounts of unbound and biologically active T.3 4 The increased tissue availability of T could be responsible for certain androgenic side effects, such as acne, hirsutism and reduced se rum concentrations of high-density lipoprotein cholesterol, which are observed in some women during treatment.3 4 The lack of an orally active preparation has hampered the clinical use of natural P. Recently, significant absorption and increased serum con centrations were obtained after oral administra tion of micronized P, which might offer an alter native with metabolic advantages. 5 6 P itself has no glucocorticoid properties but has been reported to have antiinflammatory effects and to reduce
2 cell-mediated immune reactivity. 7 8 These obser vations have been difficult to comprehend be cause circulating T-lymphocytes, although they possess cortisol receptors, apparently have no re ceptors for P. 9 Medroxyprogesterone acetate (MPA), a 17 -hy droxyprogesterone derivative, is another proges togen that does not bind to SHBG. 2 MPA is devoid of androgenic properties, but glucocorticoid side effects have been reported with its use Whereas T is bound to SHBG, the specific car rier protein for cortisol and P is corticosteroid binding globulin (CBG), or transcortinp The present competitive binding analyses were per formed in order to elucidate whether reported glucocorticoid effects of P and MPA could be ex plained by displacement of cortisol from CBG. The binding of danazol, two 19-nor steroids, and tamoxifen was also investigated. TWO-PHASE SYSTEM An aqueous two-phase system composed of two water-soluble polymers, polyethylene glycol (up per phase, 7% wt/wt) and dextran (lower phase, 12% wt/wt), was used for equilibrium partition. 16 A.2 M K-phosphate buffer containing. 1 M K-thiocyanate with a ph of 7.4 was used. n this system, serum proteins are exclusively confined to the lower dextran-containing phase, while ste roids distribute more equally between the two phases in a well-defined manner, depending on the particular steroid used. The partition coeffi cient is determined with the use of labeled ste roids in serum-free separation experiments. With serum included in the system, it is possible, from the specific radioactivity in the upper phase of the system, to calculate the amounts of free and pro tein-bound steroid in the lower phase. All exper iments were performed at room temperature (2 C). MATERALS AND METHODS CORTSOL, PROGESTERONE, AND REAGENTS MEDROXYPROGESTERONE ACETATE BNDNG TO The labeled steroids 1, 2, 6, 7-3H-progesterone and 6a- 1, 2-3 H-medroxyprogesterone acetate (New England Nuclear Corporation, Boston, MA) were purified by chromatography with the Bush B3 system 13 and 1, 2, 6, 7-3H-cortisol (New En gland Nuclear Corporation) was purified by chro matography on a Celite microcolumn. 14 Unla beled P, cortisol, norethisterone, 5a-dihydrotes tosterone (DHT), activated charcoal (Norit A), dextran (mol wt 17,5), and polyethylene glycol (mol wt 8) were purchased from Sigma Chem ical Company, St. Louis, MO. Unlabeled MPA was obtained from L vens Kemiske Fabrik, Bal lerup, Denmark, danazol from Sterling-Winthrop AB, Stockholm, Sweden, levonorgestrel from KAB AB, Stockholm, Sweden, and tamoxifen from mperial Chemical ndustries, Ltd., Maccles field, England. All salts were of analytical grade, and the water was twice distilled in quartz. CORTCOSTEROD-BNDNG GLOBULN SERUM Venous blood samples were drawn from men treated with high doses of estrogen for carcinoma of the prostate. After coagulation, all sera were. decanted, and the endogenous steroids were re moved by treatment with activated charcoal ac cording to Heyns et al. 15 The pooled serum sam ples were stored at - 2 C until used. Vol. 43, No. 6, June Pooled serum fro m estrogen-treated men known to have a high CBG concentration was used. One hundred microliters of serum was incu bated for 15 minutes in glass tubes with 5 cpm 3H-cortisol and increasing amounts of unlabeled cortisol. Likewise, 5 cpm 3H-P and 3H-MPA were incubated with increasing amounts of the corresponding unlabeled steroid. Thereafter, 2.4 gm of the homogenized phase system was added. After 3 minutes' equilibration and centrifuga tion of 1 x g for 1 minutes, 8 J.l of the upper phase was withdrawn and analyzed in a liquid scintillation counter. The protein-bound and free fractions of labeled steroid were calcu lated. Scatchard analyses were performed for the ratio of bound and free steroid plotted as a func tion of bound steroid. 1 7 CBG binding of the ste roid was calculated by subtraction of the nonspe cific albumin binding from the total binding ac cording to Rosenthal. 1 8 The albumin binding was determined by the addition of excess amounts of unlabeled steroid. DSPLACEMENT STUDES One-hundred-microliter portions of pooled se rum were incubated for 15 minutes with 5 cpm 3H-cortisol or 5. cpm 3H-P and increasing Ottosson et al. Progestogens and cortisol binding 857
3 amounts of the competitors to be tested. n some experiments 1 g of DHT was added for exclusion of any possible interference due to steroid binding to SHBG. The further experimental operations were identical to the binding studies described above. Cortisol, P, MPA, danazol, levonorgestrel, norethisterone, and tamoxifen in amounts of 11, 12, 13, and 14 ng were used as test substances. The percentage of bound 3H-steroid was calcu lated, and the results were plotted as a function of the amount of unlabeled competitor added. Each displacement experiment was repeated on three different occasions, and all gave similar results. For the competitors cortisol, P, and danazol, an added amount of 1 ng to the system would ap proximately correspond to a concentration of 1 nm. RESULTS CORTSOL, PROGESTERONE, AND MEDROXYPROGESTERONE ACETATE BNDNG TO CORTCOSTEROD-BNDNG GLOBULN Both cortisol and P bound to CBG with high affinity. The association constants (KA) were 4.75 x 17 and 6.48 x 17 M - 1, respectively. No spe cific binding of MPA to CBG could be recorded. The concentration of CBG, calculated with P used as ligand, was found to be around 2 M. DSPLACEMENT STUDES The displacement of l abeled cortisol and P caused by the substances tested are shown in Figures 1 and 2. Cortisol, P, and danazol had a marked displacing effect, while MPA, levonorges trel, norethisterone, and tamoxifen showed very little or no displacement at the concentrations used. The "relative affinity" of danazol to CBG, i.e., the relative amount of danazol needed to re duce the binding of radioactive cortisol or P to 5% of the initial binding as compared with the amount of unlabeled cortisol that gives the same effect was graphically estimated from the figures to be approximately 1 :4. 5 (Figs. 1 and 2). The absence or presence of 1 g of 5a-DHT did not affect the results of the displacement experi ments. DSCUSSON The present study confirms that P and cortisol compete for the same specific binding in human 858 Ottosson et al. Progestogens and cortisol binding Cortisol Danazol Proges terone Medrox yprogesterone acetate Levonorgestrel.A. Norethisterone x,... 1 '6 :c :5 1P- :! 5 :z:.., "tl :.c <!l ll 1 9 Tamoxifen Amount competitor added (ng) Figure 1 Displacement of 3H-cortisol from CBG by different steroids and tamoxifen. The amount of competitor necessary to reduce bound cortisol to 5% is indicated by Nonspecific al bumin binding was subtracted before the figure was drawn. The specific binding represents around 25% of the total amount of 3H-cortisol in the test system. serum. The serum concentrations of cortisol re main virtually stable throughout life and average 96 to 5 nm in nonpregnant women. n compari son, midluteal-phase values of P in fertile women are only about 21 to nm. 19 Therefore, in spite of the fact that P is bound with a somewhat high er affinity, most binding sites on CBG will be occupied by the glucocorticoid. After oral and in tramuscular administration of 1 mg of natural P, peak values for the serum concentration of about 75 and 25 nm were recorded.7 Even if doses higher than 1 mg are necessary to ac complish complete secretory transformation of the endometrium during estrogen replacement therapy, 2 it seems unlikely that P levels during clinical treatment will be high enough to cause displacement and glucocorticoid side effects. However, during the first trimester of preg nancy an increase in the plasma concentration of free cortisol is apparent.21 n individual pregnant women a rapid increase of P, followed by dis placement of cortisol, might explain some mani festations of glucocorticoid excess such as an al tered glucose tolerance. P has been suggested as
4 Cortisol Danazol Medrox yprogestrone A N o rethisterone e Progesterone acetate x... 1 : :c :s l1- Q) Cii Ui Q) 1 c. :r.., "C "'.Q Cl m lj. Levonorgestrel 1 Tamo x ifen roo 1 ooo 1 oooo Amount competitor added (ng) Figure 2 Displacement of 3H-P from CBG by different steroids and tamoxifen. The amount of competitor necessary to reduce CBG-bound P to 5% is indicated by Nonspecific al bumin binding was subtracted before the figure was drawn. The specific binding represents around 2 5 % of the total amount of 3H-P in the test system. "nature's immunosuppressant" and to depress cell-mediated immune reactivity during preg nancy.8 Extremely high concentrations of P-in the 1-5 M range-within the trophoqlastic tis sue8 should cause local displacement of cortisol. Although T-lymphocytes apparently lack P recep tors,9 this mechanism could tentatively explain the immunosuppressive effects reported for the sex steroid. MPA has been reported to suppress the synthe sis and release of adrenocorticotropic hormone and to cause adrenal atrophy in experimental animals n man, significant hyperglycemic and eosinopenic activity has been observed. 1 However, the present competitive binding analy ses gave no evidence that these cortisol-like ef fects of MPA could be explained by an interaction with the cortisol binding to CBG. The MPA bind ing to CBG was found to be weak and less than. 1 : 1 to that of cortisol. Furthermore, serum lev els of MPA even during cancer treatment with high doses are lower ( < 1 nm) than normal cortisol concentrations. 2 3 Therefore, mechanisms Vol. 43, No. 6, June 1985 other than displacement, i. e., a direct action in target organs should be responsible for the gluco corticoid-like effects of MPA. Danazol was found to bind to CBG with a "rela tive affinity" of about 1 :4.5, compared with corti sol. Therapeutic serum levels of danazol are high er (about 2 nm) than normal cortisol concen trations. 2 4 However, corticosteroid-like s ide effects have not been reported during danazol treatment. Thi s should be exp l ained by the marked albumin binding of danazol. n compari son, the KA values for the albumin binding of cortisol and danazol are. 3 x 14 M - 1 and X 14 M - 1, respectively With the use ofthe KA values and data from the literature on normal levels of cortisol, serum albumin, and CBG bind ing capacity, the effect on free cortisol levels of the presence of varying concentrations of danazol was calculated by the use of a computer. 2 5 t was calculated that > 95% of danazol was albumin bound, and only 2% to 5% was bound to CBG; whereas for cortisol 7% to 8% was CBG-bound, and only 1% to 2% was bound to albumin. n conclusion, when given in doses commonly used during clinical treatment, neither MPA nor any of the other tested synthetic steroids should increase the levels of free and biologically active cortisol. Acknowledgments. Skillful technical assistance was pro vided by Mrs. M. lsak.sson and Mrs. M. Wallen, and excellent secretarial help was given by Mrs. M. Holmberg. REFERENCES 1. Jenkins N, Fotherby K : Binding of the contraceptive ste roids norgestrel and norethisterone in human plasma. J Steroid Biochem 1 1 :5 2 1, 198 Nilsson B, Sodergard R, Damber M-G, von Schoultz B: Danazol and gestagen displacement of testosterone and in1luence on sex-hormone-binding globulin capacity. Fer til Steril 38:48, 1982 Nilsson B, Siidergard R, Damber M-G, Damber J-E, von Schoultz B: Free testosterone levels during danazol ther apy. Fertil Steril 39:55, 1983 Meldrum DR, Pardridge WM, Karow WG, Rivier J, Vale W, Judd HL: Hormonal effects of danazol and medical oophorectomy in endometriosis. Obstet Gynecol 62:48, 1983 Whitehead M, Townsend PT, Gill D K, Collins WP, Campbell S: Absorption and metabolism of oral proges terone. Br Med J 28:825, 1 98 Ottosson U-B, Carlstrom K, Damber J-E, von Schoultz B: Serum levels of progesterone and some of its metabolites including deoxycorticosterone after oral and parenteral administration. Br J Obstet Gynaecol 9 1 : , 1984 Ottosson et al. Progestogens and cortisol binding 859
5 7. Carter J: The effect of progesterone, oestradiol and HCG on cell-mediated immunity in pregnant mice. J Reprod Fertil 46:211, Siiteri PK, Febres F, Clemens LE, Chang RJ, Gondos B, Stites D: Progesterone and maintenance of pregnancy: is progesterone nature's immunosuppressant? Ann NY Acad Sci 286:384, Neifeld JP, Lippman ME, Tormey DC: Steroid hormone receptors in normal human lymphocytes. J Biol Chern 252:2972, Briggs MH, Briggs M: Glucocorticoid properties ofprogestogens. Steroids 22:555, Jones JR, Del Rosario L, Soriero AA: Adrenal function in patients receiving medroxyprogesterone acetate. Contraception 1:1, Westphal U: Steroid-Protein nteractions. New York, Springer-Verlag, 1971, pp 113, Bush E: Methods of paper chromatography of steroids applicable to the study of steroids in mammalian blood and tissues. Biochem J 5:37, Brenner PF, Guerrero R, Cekan Z, Diczfalusy E: Radioimmunoassay method for six steroids in human plasma. Steroids 22:775, Heyns W, van Baelen H, de Moor P: Study of steroid-protein binding by means of competitive adsorption: application to cortisol binding in plasma. Clin Chim Acta 18:361, Shanbhag VP, SOdergard R, Carstensen H, Albertsson P-A: A new method for the determination of testosteroneestradiol-binding globulin in human plasma. J Steroid Biochem 4:537, Scatchard G: The attractions of proteins for small molecules and ions. Ann NY Acad Sci 51:66, Rosenthal HE: A graphic method for the determination and presentation of binding parameters in a complex system. Anal Biochem 2:525, Gurpide E, Holinka C: Pregnancy-related changes in the metabolism of hormones. n Maternal-Fetal Endocrinology, Edited by D Tulchinsky, KJ Ryan. Philadelphia, W. B. Saunders, 198, p Lane G, Siddle NC, Ryder TA, Pryse-Davies J, King RJB, Whitehead M: Dose dependent effects of oral progesterone on the oestrogenised postmenopausal endometrium. Br Med J 287:1241, Rosenthal HE, Slaunwhite WR Jr, Sandberg AA: Transcortin: a corticosteroid-binding protein of plasma. X. Cortisol and progesterone interplay and unbound levels of these steroids in pregnancy. J Clin Endocrinol Metab 29:352, Edgren RH, Hambourger WE, Calhoun DW: Production of adrenal atrophy by 6-methyl-17-acetoxyprogesterone with remarks on the adrenal effects of other progestational agents. Endocrinology 65:55, Salimtschik M, Mouridsen JT, Lfllber J, Johansson E: Comparative chemo kinetics of MPA, administration by oral and intramuscular route. Cancer Chemother Pharmacal 4:267, Lloyd-Jones JG, Labross A, William-Ross T, Ross RW, Edelson J, Davidsson C: Danazol plasma concentration in man. J nt Med Res (Suppl 3) 5:18, Sodergard R, Backstrom T, Shanbhag V, Carstensen H: Calculation of free and bound fractions of testosterone and estradiol-17 to human plasma proteins at body temperature. J Steroid Biochem 16:8 1, Ottosson et al. Progestogens and cortisol binding
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