In vitro determination of the ability of drugs to bind to adrenergic receptors. Arthur H. Neufeld and Ellen D. Page
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1 In vitro determination of the ability of drugs to bind to adrenergic receptors Arthur H. Neufeld and Ellen D. Page Alpha- and beta-adrenergic receptors were studied by measuring the binding of s H-dihydroergocryptine and s H-dihydroalprenolol, respectively, to membranes prepared from homogenized rabbit iris-ciliary bodies. The binding of s H-dihydroergocryptine appears to be specific for a-adrenergic receptors, since adrenergic agents displace this radioligand with the following order of potency: phentolamine > epinephrine > norepinephrine >> isoproterenol = propranolol. The binding of 3 H-dihydroalprenolol appears to be specific for P-adrenergic receptors, since adrenergic agents displace this radioligand with the following order of potency: propranolol >> isoproterenol > epinephrine > norepinephrine >> phentolamine. Clonidine and dopamine bind to the a-adrenergic receptor but have little activity at the P-adrenergic receptor. Timolol, d-isoproterenol, and dipivalyl epinephrine bind to the P-adrenergic receptor but have little activity at the a-adrenergic receptor. The results demonstrate that in vitro binding assays for a- and P-adrenergic receptors are useful for studying the mechanism of drug action. Key words: adrenergic receptors, catecholamines, dihydroergocryptine, dihydroalprenolol, timolol, d-isoproterenol, dipivalyl epinephrine, clonidine, iris, rabbit. Rdecently, there has been much work on developing new, or retesting available, adrenergic agents which, when applied topically to the eye, reduce intraocular pressure. Much of the interest in the use of adrenergic agonists to reduce intraocular pressure centers around their ability From the Department of Ophthalmology and Visual Sciences, Yale University School of Medicine, New Haven, Conn. Supported in part by United States Public Health Service Grant EY Arthur H. Neufeld is a recipient of a Research Career Development Award, EY Submitted for publication May 10, Reprint requests: Arthur H. Neufeld, Ph.D., Eye Research Institute of Retina Foundation, 20 Staniford St., Boston, Mass to increase the outflow of aqueous humor directly, as well as to decrease the formation of aqueous humor. Some of the recent developments in this field have included use of compounds other than the naturally occurring catecholamines. For example, timolol, apparently a /?-adrenergic antagonist, decreases intraocular pressure in rabbits and man. 1 Dipivalyl epinephrine also has marked influences on intraocular pressure, presumably after its metabolism to epinephrine. 2 d-isoproterenol, which is usually not associated with biological activity, decreases intraocular pressure in the rabbit, 3 ' 4 and compounds such as clonidine 5 ' 6 and dopamine 7 appear to reduce intraocular pressure as a result of their intrinsic sympathomimetic activity.
2 Volume 16 Number 12 Adrenergic receptors 1119 Although there is no substitute for the in vivo experiment whereby these compounds are applied topically and their influence on intraocular pressure determined, this type of investigation does not clarify the molecular mechanism of action of the drugs. Adrenergic agents may act directly, by binding to the a- or /?-adrenergic receptor, or indirectly, by causing the release of endogenous catecholamine or interfering with uptake or metabolism. In addition, although a compound such as dipivalyl epinephrine can be metabolized to epinephrine, the prodrug itself may have adrenergic activity. To test the ability of compounds of ophthalmic interest to interact directly with a- and /3-adrenergic receptors, we have used in vitro radioligand-displacement assays. 8 ' We have determined the binding activity of various compounds to the a- and /?-adrenergic receptors on membranes prepared from homogenized rabbit iris-ciliary bodies. These assays utilize 3 H-dihydroergocryptine and 3 H-dihydroalprenolol and are specific for the postjunctional a- and /8-adrenergic receptors, respectively. Methods Preparation of membranes. Either freshly enucleated eyes from 2 to 3 kg. male albino New Zealand rabbits or frozen eyes obtained from Pel-Freeze Biologicals, Inc., were used. Eyes were cut into anterior and posterior poles, and irisciliary bodies were dissected free. Tissues were pooled in groups of 5 to 20, depending upon the amount of material needed. Following described procedures, 8 the tissue was homogenized in 20 ml. of cold 0.25M sucrose, 1 mm MgCh, and 5 mm Tris-HCl, ph 7.4, in motor-driven glass/teflon homogenizers; after filtration through cheesecloth, the homogenate was centrifuged at 310 x g for 10 min. at 4 C. The supernatant obtained was centrifuged at 28,000 x g for 10 min. at 4 C. and washed twice, with rehomogenization, in 5 ml. of cold 10 mm MgCl 2 and 50 mm Tris-HCl, ph The final pellet was suspended in 2 ml. of this same solution and stored frozen for up to 4 days, with no apparent loss of activity. Immediately prior to use, this suspension was rehomogenized, and a sample was taken for protein determination by the method of Lowry et al., 10 with bovine serum albumin as standard. This membrane preparation was assayed for both PROP I I I I I0" M Fig. 1. Inhibition of 3 H-dihydroergocryptine binding by adrenergic agonists and antagonists. Membranes prepared from frozen rabbit eyes were incubated with 3 H-dihydroergocryptine in the absence and presence of the indicated agents. The ability of each compound to displace the radioligand was compared to 100 percent inhibition of binding by 5xlO~ 5 M phentolamine. Each value is the mean of duplicate determinations of at least two separate experiments. a- and /8-adrenergic receptors. Iris-ciliary bodies from normal rabbits and from frozen eyes were processed and assayed in the same manner. No differences were noted. Assay for a-adrenergic receptors. a-adrenergic receptors were assayed by determining the amount of binding to membranes of 3 H-dihydroergocryptine, at 5xlO- s M, that can be displaced by phentolamine, at 5xlO- 5 M. 8 A 50 /tg amount of membrane protein was incubated for 15 min. at 25 C. in 150 -pi of the following incubation medium: 10 mm MgCl 2, 50 mm Tris-HCl, ph 7.55, and 50 nm 3 H-dihydroergocryptine. When agents were present to displace the 3 H-dihydroergocryptine from the binding site, e.g., phentolamine or epinephrine, serial dilutions were added to the 150 pi volume to give the final molar concentration indicated. Incubation was terminated by the addition of 1.5 ml. of cold incubation medium and filtration through Whatman GF/C filters. Filters were washed twice with 10 ml. of cold incubation medium, dried for 1 hr. at 65 C, and prepared for scintillation counting by solubilization in 0.5 ml. of Protosol followed by 10 ml. of Econofluor. Nonspecific binding (that amount of 3 H-dihydroergocryptine not displaced by phentolamine) was 10 to 50 percent of the total binding and was not saturated at 10~ 7 M 3 H-dihydroergocryptine. Assay for ^-adrenergic receptors. /?-Adrenergic receptors were assayed by determining the amount of binding to membranes, prepared as described above, of 3 H-dihydroalprenolol, at 10- s M, that could be displaced by propranolol, at 5xlO- 5 M. 9 The
3 1120 Neufeld and Page Invest. Ophthalmol. Visual Sci. December 1977 Table I. Inhibition of 3 H-ligand binding 1-Epinephrine /-Norepinephrine /-Isoproterenol Phentolamine Phenoxybenzamine d, 1-Propranolol Clonidine Dopamine Dipivalyl epinephrine ^-Isoproterenol Timolol a-receptor K d ^-Receptor The dissociation constant, Kd, was calculated from the following equation: Kd = EC 3 o/(l + ( 3 H-lg)/K 3H. g) where ( 3 H lg) is the concentration of the radioligand in the assay, K3 H _ lg is the dissociation constant for the radioligand computed by Scatchard analysis, and ECoo is the concentration of the displacing compound which inhibits 50% of the binding of the radioligand. 8 procedures used for the assay of the /?-adrenergic receptor were identical to that for the a-adrenergic receptor except that the 15 min. incubation was at 37 C. Membranes were collected and washed on Whatman GF/A filters and prepared for scintillation counting as above. Nonspecific binding, or that amount of 3 H-dihydroalprenolol not displaced by propranolol, was usually 10 to 15 percent of the total binding. Materials 3 H-dihydroergocryptine (24.1 Ci./mmol.) and 3 H-dihydroalprenolol (32.6 Ci./mmol.) were purchased from New England Nuclear. Z-Epinephrine d-bitartrate, Z-arterenol d-bitartrate, /-isoproterenol d-bitartrate, dopamine, and d,z-propranolol were purchased from Sigma. The following compounds were generously supplied: phentolamine (Ciba-Geigy), phenoxybenzamine (Smith, Kline and French), clonidine (Boehringer Ingelheim), d-isoproterenol (Sterling Winthrop), timolol (Merck), dipivalyl epinephrine (Allergan). Results a-adrenergic receptor. As determined by Scatchard analysis, the K d for 3 H-dihydroergocryptine binding to sites on membranes prepared from homogenized rabbit iris-ciliary bodies is 22 nm. Fig. 1 demonstrates the specificity for adrenergic agonists and antagonists of these sites. Displacement of 3 H-dihydroergocryptine by each agent was compared to maximal displacement, or 100 percent inhibition, of the specific finding of 3 H-dihydroergocryptine by 5xlO~ 5 M phentolamine. 8 The order of potency for displacing the radioligand is phentolamine > epinephrine > norepinephrine > > isoproterenol = propranolol. This order of potency agrees with the known a-adrenergic activity of these compounds. The K d values are given in Table I and are approximately the same as that reported for membranes prepared from rabbit uteri. 8 ^ Adrenergic receptor. As determined by Scatchard analysis, the K d for 3 H-dihydroalprenolol binding to sites on membranes prepared from homogenized rabbit irisciliary bodies is 2.4 nm. Fig. 2 demonstrates the specificity for adrenergic agonists and antagonists of these sites. Displacement of 3 H-dihydroalprenolol by each agent was compared to maximal displacement, or 100 percent inhibition, of the specific binding of 3 H-dihydroalprenolol by 5xlO" 5 M propranolol. The order of potency for displacing the radioligand is propranolol > > isoproterenol > epinephrine > norepinephrine >> phentolamine. This order of potency agrees with the known ^-adrenergic activity of these compounds, such as the stimulation of adenylate cyclase. The K d values are given in Table I and are in reasonable agreement with other reported values for frog erythrocytes 9 and rat pineal gland. 11 Adrenergic compounds tvhich influence intraocular pressure. Fig. 3 demonstrates the ability of clonidine, dopamine, and epinephrine to displace 3 H-dihydroergocryptine from the a-adrenergic receptor. Clonidine is very potent, at least five times more active than epinephrine, and is the most potent agonist that we have studied. Dopamine is about one-fifth as active as epinephrine, but this is still considerable potency for a compound not usually associated with much a-adrenergic activity. Table I lists the dissociation constants for these compounds at the a- and ^-adrenergic receptors. Dopamine is not active at the /?-adrenergic receptor.
4 Volume 16 Number 12 Adrenergic receptors 1121? 80 x Fig. 2. Inhibition of 3 H-dihydroalprenolol binding by adrenergic agonists and antagonists. Membranes prepared from frozen rabbit eyes were incubated with 3 H-dihydroalprenolol in the absence. and presence of the indicated agents. The ability of each compound to displace the radioligand was compared to 100 percent inhibition of binding by 5xlO~ 5 M propranolol. Each value is the mean of duplicate determinations of at least two separate experiments. Fig. 4 demonstrates the ability of timolol, epinephrine, <2-isoproterenol, and dipivalyl epinephrine to displace 3 H-dihydroalprenolol from the /?-adrenergic receptor. Timolol is very potent, approximately two orders of magnitude more active than epinephrine and equipotent to propranolol. d-isoproterenol, which is usually not associated with biological activity, is as potent as norepinephrine and only four times less active than epinephrine at the /?-adrenergic receptor. Dipivalyl epinephrine also has the ability to bind to the ^-adrenergic receptor with about one-fifteenth the potency of epinephrine. Table I lists the dissociation constants for these compounds at the a- and /3-adrenergic receptors. Timolol, d-isoproterenol, or dipivalyl epinephrine is not active at the a-adrenergic receptor. Discussion Our findings confirm and extend the work by Lefkowitz and colleagues 8 ' 9 to a densely adrenergically innervated smooth muscle containing both a- and /?-adrenergic receptors. The tissue that we have referred to as rabbit iris-ciliary body and used for the preparation of membranes in these lo" 6 M Fig. 3. Inhibition of 3 H-dihydroergocryptine binding by clonidine, epinephrine, and dopamine. The determinations were similar to those described in Fig o t z 100 z S 20 I0" 9 I0" 8 I0" 7 I0" 6 I0" 5 I0" 4 I0" 3 Fig. 4. Inhibition of 3 H-dihydroalprenolol binding by timolol, epinephrine, d-isoproterenol, and dipivalyl epinephrine. The determinations were similar to those described in Fig. 2. studies is actually composed of several different, adrenergically innervated smooth muscles, including ciliary muscle, vascular smooth muscle, iris sphincter, and iris dilator. Thus our findings generalize to include adrenergic receptors in several types of smooth muscle. Our observations with 3 H-dihydroergocryptine support the hypothesis that this compound binds to the a-adrenergic receptor. 8 We find at least threefold more binding sites for 3 H-dihydroergocryptine in membranes prepared from the rabbit irisciliary body than that reported previously for the rabbit uterus, 8 a sparsely, ad- M I I
5 1122 Neufeld and Page Invest. Ophthalmol. Visual Sci. December 1977 renergically innervated tissue. The phentolamine-sensitive binding of 3 H-dihydroergocryptine is displaced by adrenergic agonists with the order of potency characteristic of interaction at an a-adrenergic receptor: epinephrine > norepinephrine > isoproterenol. In addition, dopamine, which has a-adrenergic activity demonstrated by its ability to dilate the pupil when applied topically to the rabbit eye, 7 potently displaces 3 H-dihydroergocryptine. Our observations with 3 H-dihydroalprenolol support the hypothesis that this compound binds to the /?-adrenergic receptor. 9 Although there are no values in the literature to compare the density of /?-adrenergic receptors in the iris-ciliary body with other smooth muscles, the value that we have obtained is similar to that reported for frog erythrocytes, 9 rat pineal gland, 11 and rat cerebral cortex with the use of a different ligand. 12 Propranololsensitive binding of 3 H-dihydroalprenolol is displaced by adrenergic agonists with the expected order of potency characteristic of interaction at a /?-adrenergic receptor: isoproterenol > epinephrine > norepinephrine. The /3-adrenergic receptor in this tissue is presumably associated with adenylate cyclase because stimulation in vitro with adrenergic agents causes the synthesis of cyclic AMP 13 as in other tissues. Studies comparing the binding of the radioligands to membranes prepared from normal and denervated iris-ciliary bodies indicate that for membranes prepared from innervated tissue, 80 to 90 percent of the specific binding of 3 H-dihydroergocryptine is to the true, postjunctional a-adrenergic receptors associated with the contraction of smooth muscle. 14 Similarly, most and probably all of the 3 H-dihydroalprenolol binds to the postjunctional ^-adrenergic receptors associated with relaxation of smooth muscle. Also, competitive inhibitors of monoamine oxidase and catechol-omethyl transferase do not alter binding of either radioligand. 14 Clonidine is a sympathomimetic drug which reduces the intraocular pressure of the rabbit, monkey, and man. 5 - G - 15 Although clonidine does not have a specific effect on outflow faciliy in primates but rather influences regional blood flow, 15 many investigators have suggested that this compound may be useful clinically. Recently, Allen and Langham 6 used clonidine topically in conscious rabbits and concluded that this drug is only weakly active peripherally, compared to the naturally occurring catecholamines, and primarily influences intraocular pressure through a mechanism involving the central nervous system. Our findings clearly show that clonidine can bind to peripheral a-adrenergic receptors and can do so more potently than epinephrine or norepinephrine. Differences in the in vivo potency must therefore be accounted for by differences in absorption, uptake, or metabolism. Dopamine, administered topically or intravitreally, decreases intraocular pressure and dilates the pupil. Shannon et al. 7 suggest that dopamine is capable of stimulating the a-adrenergic receptor but not the /?-adrenergic receptor. Our findings support these conclusions in that dopamine displaces 3 H-dihydroergocryptine from the a-adrenergic receptor, although less potently than epinephrine, and has virtually no activity at the ^-adrenergic receptor. cz-isoproterenol has somewhat surprising activity in the eye. Although the compound does not decrease the intraocular pressure of the rhesus monkey or man, 4 the drug is effective when administered topically to the rabbit. 3 ' 4 Our present findings indicate that ^-isoproterenol binds to the /?-adrenergic receptor. This observation, together with a previous finding that ^-isoproterenol does not increase the concentration of cyclic AMP in the aqueous humor, 4 indicates that this drug must be acting as a ^-adrenergic antagonist in the eye. Its inability to reduce intraocular pressure in primates is probably due to its weak potency.
6 Volume 16 Number 12 Adrenergic receptors 1123 Timolol is a /?-adrenergic antagonist which reduces intraocular pressure in the rabbit and man. 1 From our experiments, the ability of this drug to displace 3 H-dihydroalprenolol from the /?-adrenergic receptor indicates that this compound has extremely high potency. Timolol applied topically to the rabbit eye does not increase the concentration of cyclic AMP in the aqueous humor (authors' unpublished observations); therefore its effect on intraocular pressure is not due to intrinsic /?-adrenergic agonistic activity. Thus timolol acts as a potent, true ys-adrenergic antagonist to reduce intraocular pressure at a locus within the eye that has yet to be identified. Dipivalyl epinephrine is a prodrug which, when applied topically to the rabbit and man, reduces intraocular pressure. 2 The prodrug is highly permeable, entering the eye readily where it is hydrolyzed to epinephrine by the esterases found in ocular tissues. 16 Although much of the activity of dipivalyl epinephrine is clearly related to its metabolism to catecholamine, our observations indicate that the prodrug itself is active at the /?-adrenergic receptor. This activity is not due to breakdown of the prodrug during in vitro incubation, since there is essentially no activity at the a-adrenergic receptor, the compound is relatively stable in solution at neutral ph for several hours (A. Hussain, personal communication), and esterase activity is not associated with the washed membrane fraction that we use for the incubation. 1 " The displacement of radioligands from adrenergic receptors assayed in vitro provides a simple, supplementary model system for studying the potency and site of action of drugs of interest. The method allows the investigation of these parameters in the absence of interfering variables such as neuronal and extraneuronal uptake, release of endogenous catecholamines, or metabolism and the accumulation of metabolites. Studying the displacement of the radioligahds appears to give an accurate description of binding at the a- and /3-adrenergic receptors and is a useful technique for investigating interactions at these receptors. REFERENCES 1. Katz, I. M., Hubbard, W. A., Getson, A. J., and Gould, A. L.: Intraocular pressure decrease in normal volunteers following timolol ophthalmic solution, INVEST. OPHTHALMOL. 15:489, Kaback, M. B., Podos, S. M., Harbin, T. S., Jr., Mandell, A., and Becker, B.: The effects of dipivalyl epinephrine on the eye, Am. J. Ophthalmol. 81:768, Seidehamel, R. J., Dungan, K. W., and Hickey, T. E.: Specific hypotensive and antihypertensive ocular effects of cz-isoproterenol in rabbits, Am. J. Ophthalmol. 79:1018, Kass, M. A., Reid, T. W., Neufeld, A. H., Bausher, L. P., and Sears, M. L.: The effect of d-isoproterenol on intraocular pressure of the rabbit, monkey, and man, INVEST. OPH- THALMOL. 15:113, Heilman, K.: Untersuchungen iiber die Wirkung von Catapresan auf den intraokularen Druck. 1. Mitteilung, Klin. Monatsbl. Augenheilkd. 157:182, Allen, R. C., and Langham, M. E. : The intraocular pressure response of conscious rabbits to clonidine, INVEST. OPHTHALMOL. 15:815, Shannon, R. P., Mead, A., and Sears, M. L.: The effect of dopamine on the intraocular pressure and pupil of the rabbit eye, INVEST. OPHTHALMOL. 15:371, Williams, L. T., Mullikin, D., and Lefkowitz, R. J.: Identification of a-adrenergic receptors in uterine smooth muscle membranes by ( 3 H) dihydroergocryptine binding, J. Biol. Chem. 251:6915, Mukherjee, C., Caron, M. G., Coverstone, M., and Lefkowitz, R. J.: Identification of adenylate cyclase-coupled /3-adrenergic receptors in frog erythrocytes with (-)-( 3 H)- alprenolol, J. Biol. Chem. 250:4869, Lowry, O. H., Rosenbrough, N. H., Farr, A. L., and Randall, R.: Protein measurement with the Folin phenol reagent, J. Biol. Chem. 193:265, Kebabian, J. W., Zatz, M., Romero, J. A., and Axelrod, J.: Rapid changes in rat pineal P- adrenergic receptor: alterations in 1-( 3 H)- alprenolol binding and adenylate cyclase, Proc. Natl. Acad. Sci. U.S.A. 72:3735, Sporn, J. R., Harden, T. K., Wolfe, B. B., and Molinoff, P. B.: /?-adrenergic receptor involvement in 6-hydroxydopamine-induced
7 1124 Neufeld and Page Invest. Ophthalmol. Visual Set. December 1977 supersensitivity in cat cerebral cortex, Science 194:624, Neufeld, A. H., and Sears, M. L.: Cyclic- AMP in ocular tissues of the rabbit, monkey, and human, INVEST. OPHTHALMOL. 13:475, Page, E. D., and Neufeld, A. H.: Characterization of ot- and /3-adrenergic receptors ih membranes prepared from the rabbit iris before and after development of supersensitivity. Submitted to Biochemical Pharmacol- 15. Bill, A., and Heilman, K.: Ocular effects of clonidine in cats and monkeys (Macaca irus), Exp. Eye Res. 21:481, Hussain, A., and Truelove, J. E.: Prodrug approaches to enhancement of physicochemical properties of drugs. IV. Novel epinephrine prodrug, J. Pharm. Sci. 65:1510, 1976.
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