Binding of Thyrotropin-Releasing Hormone to Plasma Membranes of Bovine Anterior Pituitary Gland

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1 Proc. Nat. Acad. Sci. USA Vol. 69, No. 1, pp , January 1972 Binding of Thyrotropin-Releasing Hormone to Plasma Membranes of Bovine Anterior Pituitary Gland (hormone receptor/adenylate cyclase/equilibrium constant/[3hfthyrotropin) FRNAND LABRI, NICHOLAS BARDN, GUY POIRIR, AND ANDR D LAN Laboratory of Molecular ndocrinology, Faculty of Medicine, Laval University, Quebec 1, Canada. Communicated by Alexander Rich, November 1, 1971 ABSTRACT An assay for the binding of ['Hlthyrotropin-releasing hormone ([3HJTRH) is described. Plasma membranes isolated from bovine anterior pituitary gland bind about 6 femtomoles of this hormone per mg of protein, as compared to 15 femtomoles per mg of protein in the total adenohypophyseal homogenate (4-fold purification). The equilibrium constant of membrane receptor-[3h]trh binding at C is 4.3 X 17 L- M-1, or a half-maximal binding of this hormone at 23 nm. The binding is time-dependent; addition of unlabeled hormone induces dissociation of the receptor-[3h]trh complex with a half-life of 14 min. The binding of TRH is not altered by 1 um melanocyte-stimulating hormonerelease inhibiting hormone, lysine-vasopressin, adrenocorticotropin, growth hormone, prolactin, luteinizing hormone, insulin, glucagon, L-thyroxine, or L-triiodothyronine. K+ and Mg + + increase formation of the receptor-trh complex at optimal concentrations of 5-25 mm and mm, respectively, with inhibition at higher concentrations. Ca++ inhibits binding of TRH at all concentrations tested. Abbreviation: TRH, thyrotropin-releasing hormone. 283 The secretion of thyrotropin by the anterior pituitary gland is controlled by a neurohormone synthesized in the hypothalamic area and carried to its adenohypophyseal site of action by a portal system (1-3). A major contribution in the field of neuroendocrinology has been the recent elucidation of the structure of this neurohormone (thyrotropin-releasing horrnone, TRH) as L-pyroglutamyl-ihistidyl-rproline amide (4, 5). The availability of the first synthetic hypothalamic releasing hormone in a pure form opens new possibilities for the study of the mechanism of action of this peptide in the anterior pituitary gland. There is strong evidence of a role for adenylate cyclase as a mediator of the action of the hypothalamic releasing hormones (6-11). We have found (unpublished data) that adenylate cyclase, the enzyme catalyzing the formation of cyclic AMP, is associated with the plasma membranes in anterior pituitary tissue. The possibility of a specific binding of [3HJTRH to the adenohypophyseal plasma membranes as their primary action was somewhat strengthened by studies with radio-iodinated adrenocorticotropin (12, 13), insulin (14-18), angiotensin (19), and glucagon (2-22), that indicate that the first step in the action of these polypeptide hormones is their interaction with specific recognition sites on the plasma membrane of target cells. This paper describes an assay for measurement of [3H]TRH binding and the pertinent properties of hormone binding to its receptors in the adenohypophyseal plasma membrane. MATRIALS AND MTHODS Thyrotropin-releasing hormone (L- [2,3-3H ]-Proline, 4 Ci/mol) was purchased from New- ngland Nuclear. Radiochemical purity, determined by paper chromatography on Whatman no. 1 in n-butyl alcohol- acetic acid- water 25:4:1 was more than 98% at the end of the reported experiments. Biological activity of [3H]TRH was determined before delivery by bioassay (23), and was found to be identical to that of a synthetic standard of TRH and, hence, completely biologically active. Synthetic TRH was supplied by Dr. W. F. White, Abbott Laboratories, Chicago, and by Dr. R. Guillemin, Salk Institute, La Jolla. Synthetic melanocyte-stimulating hormonerelease inhibiting hormone was a gift from Drs. A. V. Schally and J. A. Kastin, New Orleans. Porcine adrenocorticotropin was a gift from Dr. A. F. Dixon, Cambridge, ngland, Bovine growth hormone (NIH-GH-B16) and prolactin (NIH-P-B3) were supplied by the National Pituitary Agency, ndocrinology Study Section, NIH. Bovine LH was supplied by Dr. C. Courte, Laval University, Quebec. Bovine insulin (PJ-469) and crystalline porcine glucagon (GLF-599A) were gifts from Dr. M. A. Root, The Lilly Research Laboratories, Indianapolis. Synthetic lysine-vasopressin was purchased from Sigma. sters of cellulose membranes (HAWP- HA.45 um) were obtained from the Millipore Co. Isolation of Adenohypophyseal Plasma Membranes. Anterior pituitaries from adult cattle were collected in local slaughterhouses and rapidly brought to the laboratory in ice-cold Krebs-Ringer bicarbonate buffer (24) containing 11 mm D-glucose. Plasma membranes were isolated by our modification (9) of Neville's technique (25). The fraction of a 3% homogenate of bovine anterior pituitary tissue in 1 mm NaHCO3r5 mm mercaptoethanol that sediments between 122 and 2 X g is fractionated by isopycnic centrifugation (25) in a stepwise sucrose gradient of densities As evidenced by electron microscopy and assays of enzyme markers, the material sedimenting at the interfaces and consists of pure plasma membranes. Protein concentration was determined (26) with bovine serum albumin as standard. Binding of [3H]TRH to Adenohypophyseal Plasma Membranes. In the standard assay, 5 jig of plasma-membrane protein and 25 nm (27,5 cpm) [3HJTRH are incubated, in

2 284 Biochemistry: Labrie et al. a final volume of 55 1l, in buffer F (2 mm sodium phosphate buffer (ph 7.35)-7.5 mm KCl-2 mm MgCl2), at C for 4 min. The reaction is stopped by the addition of 1. ml of ice-cold buffer F, and the medium is immediately filtered with gentle suction through a Millipore filter, with three successive washes of the adsorbed material with 2 ml of the ice-cold buffer. After the filter is dried at 6C for 3 min, 1 ml of toluene-based scintillation fluid is added and the radioactivity is measured in a Packard Liquid Scintillation Spectrometer. Unless otherwise stated, all assays are done in triplicate. RSULTS Time Course of [8H]TRH-Receptor Association and Dissociation. Fig. 1 shows that half-maximal binding of [8H]TRH to the adenohypophyseal plasma membranes is obtained after 5 min of incubation at C, a plateau being reached between 2 and 3 min. No appreciable change in binding occurs when incubation is extended to 15 min (data not shown). When excess unlabeled TRH (.1 mm) is added after formation of the [3H]TRH-receptor complex has reached equilibrium, the complex dissociates, with an initial half-life of min (Fig. 2). Plasma Membrane Concentration. With 8 nm [3H]TRH, the binding is proportional to membrane concentration up to 1.6 mg/ml (Fig. 3). A concentration of 1 mg of protein per ml was used in the standard binding assay. At saturating concentrations of [3H]TRH, about 4-fold purification of the number of TRH binding sites is usually observed in the plasma membrane fraction as compared to the total adenohypophyseal homogenate. ffect of Potassium, Magnesium, Manganese, Calcium, and Chelating Agents on [8H]TRH Binding. There is a sharp 3 2, z 16 z he s Proc. Nat. Acad. Sci. USA 69 (1972) Minutes FIG. 2. Time course of dissociation of bound ['HJTRH from adenohypophyseal plasma membranes at C. 25 nm [3HJTRH and plasma membranes (1 mg of protein/ml) were incubated for 4 min at C before the addition of.1 mm unlabeled TRH and measurement of the remaining bound [3H]TRH at the indicated times after addition of the unlabeled hormone. increase in TRH binding between 2.5 and 5. mm K+, a plateau being observed between 5 and 25 mm, with a subsequent decrease reaching values below the control at 1 mm K+ (data not shown). When NaCl is added to the standard incubation medium, there is no effect of Na++ ions up to a concentration of 12 mm. Maximal stimulation by Mg++ is observed at concentrations of mm, with subsequent inhibition of binding at higher concentrations (Fig. 4). When the binding assay is performed in the presence of 1 mm Mg++, Mn++ gives a pattern similar to that of Mg++, while Ca++ is inhibitory at all concentrations (Fig. 4). quilibrium Constant of TRH-Receptor Interaction. There is a small amount of [8H]TRH that binds unspecifically to the a, *-2 8 _ a,n1 z o 6 S 4 C o4 L MINUTS OF INCUBATION FIG. 1. Time course of binding of [3H]TRH to adenohypophyseal plasma membranes. 25 nm [3H]TRH (27,5 cpm) and anterior pituitary plasma membranes (1 mg of protein/ml) were incubated at C. The bound fraction was separated by adsorption on Millipore membranes. 6 2e ,ag -membrane protein FIG. 3. ffect of protein concentration of the anterior pituitary plasma membrane fraction on [3H]TRH binding.

3 Proc. Nat. Acad. Sci. USA 69 (1972) Plasma-Membrane Binding of Thyrotropin-Releasing Hormone Concentration (mm) FIG. 4. ffect of Mg +, Mn++,and Ca++on ['H]TRH binding to adenohypophyseal plasma membranes. 1 mm Mg++ was presented during incubation with Mn++ or Ca++. *@, Mg++**,Mn +;**,Ca ++ membrane (lower curve, Fig. 5A). This nonspecific component is related linearly to the concentration of labeled TRH, and accounts for about.5% of the total radioactivity filtered through the membrane and for about 5% of the radioactivity bound in the presence of membranes. This nonspecific adsorption was subtracted from the total radioactivity bound to the filter. With increasing concentrations of [3H]TRH, the hormone binding to plasma membranes follows the equation y = STRHU/[U+(1/KTRH) 1, where STRH is the number of TRHbinding sites, U is the unbound TRH, and KTRH is the equilibrium constant of the TRH-receptor interaction. - KTRH was measured as 4.3 X 17 L M 1 and STRH as.5 nanomoles * L-1 or 6 femtomoles per mg of membrane protein (Fig. 5A and 5B). Specificity of [3H]TRH Binding. Increasing concentrations of unlabeled TRH lead, by dilution, to a progressive decrease of binding of the labeled hormone. Virtually complete inhibition of binding is observed after the addition of 1 um unlabeled TRH. 1 um lysine-vasopressin and melanocytestimulating hormone-release inhibiting hormone, two oligopeptides of hypothalamic origin, have no effect on [3H]TRH binding (Table 1). Similarly, no competition is observed when various peptide hormones (porcine adrenocorticotropin, bovine luteinizing hormone, bovine growth hormone, bovine prolactin, bovine insulin, and porcine glucagon) are added at 1 JAM, well above the physiological plasma concentration (Table 1). Coupled with the dilution experiment with unlabeled TRH, these data indicate that the site of binding of TRI is highly specific, and validate the use of the described assay for investigation of the specific binding of TRH. In view of the well-known inhibitory feedback effect of thyroid hormone on TRH action in the anterior pituitary gland (29, 3), it is interesting to note that thyroxine or triiodothyronine have no influence on the binding of TRH to plasma membranes (Table 1), thus providing evidence for an action of thyroid hormone at a site subsequent to the binding of TRH to its receptor. DISCUSSION Despite its central importance in the direct control of thyrotropin secretion, and its indirect effect on the secretion of the many hormones influenced by the concentration of circulating thyroid hormone (31, 32), little is understood about the mechanism of action of TRH in molecular terms. The availability of synthetic TRH labeled at high specific activity in its proline residue makes it possible to study the interaction of this very important molecule with its receptors in the anterior pituitary gland. Such a study avoids limitations inherent in the use of radiolabeled derivatives of peptide hormones. A high degree of specificity of the TRH receptor is suggested by the absence of competition for TRH binding by two peptide hormones of hypothalamic origin, and by six other peptide hormones. The interaction of TRH and its receptor follows standard bimolecular reaction kinetics, and the reaction is reversible. Unlabeled TRH displaces the labeled hormone in proportion to its relative concentration; virtually complete inhibition of [3H]TRH binding was observed in the presence of 1 gm unlabeled TRH. However, when [3HJTRH and receptor have reached equilibrium, excess unlabeled TRH usually fails to displace 2-4% of the bound radioactivity after 1 hr of incubation. The remaining bound radioactivity is somewhat higher than the value expected from the rate of dissociation measured in the first 2 min. Under comparable conditions, only 1-2% of glucagon was displaced from liver membranes at C in the presence of 1 mm DTA, and negligible dissociation could be measured in the absence of the chelating agent (21). About 1% of bound '25I-labeled insulin was not displaced by excess unlabeled hormone (16). There is no satisfactory explanation for these results. The concentration of TRH giving half-maximal binding to the receptor (23 nm) is in the range of concentrations found efficient in eliciting the best-known effect of this neurohormone, TSH release by the anterior pituitary gland incubated in vitro (33). It is most likely that the concentration of TRH in the portal blood supplying the TSH-secreting cells of the anterior pituitary gland is in this range of concentrations. Since calcium is required for the TRH-induced release of thyrotropin (34), it is noteworthy that addition of calcium depresses binding of the labeled hormone at all concentrations studied. It should be mentioned that physiological concentrations of Ca++ only inhibit [8H]TRH binding about 5%. These findings eliminate the TRH-receptor interaction as a possible site for the permissive action of Ca++ on thyrotropin release. Likewise, the binding of ACTH to the adrenal receptor does not require Ca++ (13) and high concentrations of Ca++ depress hormone binding. This inhibitory effect of Ca++ might be secondary to competition of Ca++ with the Mg++ sites on the hormone receptor, or to some direct interaction of Ca++ with the receptor or the hormone.

4 286 Biochemistry: Labrie et al. Proc. Nat. Acad. Sci. USA 69 (1972) IW 6 A 5 / TABL 1. ffect of unlabeled TRH, lysine-vasopressin, melanocyte-stimulating hormone-release inhibiting hormone, adrenocorticotropin, growth hormone, prolactin, luteinizing hormone, insulin, glucagon, thyroxin, and triiodothyronine on the binding of 25 nm [3H]TRH to adenohypophyseal plasma membranes* I- P- n co tr w [3H] TRH ( x let M) B 1. Added hormone Femtomoles of ['H]TRH bound/mg membrane protein Control 368 ± 14 TRH 8 MSH-release inhibiting hormone 334 ± 6 Lysine-vasopressin 344 i 12 Adrenocorticotropin 316 i 22 Growth hormone 36 i 22 Prolactin 35 i 2 Insulin Glucagon 352 +t 8 Control 37 ± 2 L-thyroxine (5 pig/ml) 376 i 38 L-thyroxine (.5 pg/ml) L-triiodothyronine (.2,ug/ml) L-triiodothyronine (.2,ug/ml) *Incubations were performed as described under "Methods", except for the presence of indicated hormones. The molecular weights of growth hormone and prolactin were taker, respectively, as 2,846 and 23,5 (27, 28) C-.4e 4. 2 YTRH (nm) FIG. 5. A. ffect of increasing concentrations of [3H]TRH on the binding of the hormone to anterior-pituitary plasma membranes. *-*, unspecific adsorption to the filter; -, binding in the presence of 1 mg/ml of plasma membrane protein, correction being made for nonspecific adsorption. B. Double-reciprocal plot of data obtained in an experiment performed as described in Fig. 5A. KTRH, from the slope of this line, is 4.3 X 17 L-M-1. There are very interesting recent data on the interaction of ACTH (12, 13), insulin (14-18), and glucagon (2-22) with receptors in their target cells. Among the striking similarities of the characteristics of binding of these relatively large peptides with those of the tripeptide TRH, there are the high equilibrium constant and specificity and, possibly more important, the location of the receptor in the plasma membrane, which is also the main site of the adenylate cyclase in mammalian tissues (35-36), including the anterior pituitary gland. This research was supported by Grant MA-3525 from the Medical Research Council of Canada. F. L. and N. B. are, respectively, Scholar and postdoctoral Fellow of the Medical Research Council of Canada. The technical assistance of A. Petitclerc and N. Lemay is gratefully acknowledged. 1. Burgus, R. & Guillemin, R. (197) Annu. Rev. Biochem. 39, McCann, S. M. & Porter, J. C. (1969) Physiol. Rev. 49, Mitnick, M. & Reichlin, S. (1971) Science 172, Boler, J., nzman, F., Folkers, K., Bowers, C. Y. & Schally, A. V. (1969) Biochem. Biophys. Res. Commun. 37, Burgus, R., Dunn, T. F., Desiderio, D. & Guillemin, R. (1969) C. R. H. Acad. Sci. 269, Labrie, F., Beraud, G., Gauthier, M. & Lemay, A. (1971) J. Biol. Chem. 246, Labrie, F., Lemaire, S. & Courte, C., J. Biol. Chem., in press. 8. Lemaire, S., Pelletier, G. & Labrie, F., J. Biol. Chem., in press. 9. Labrie, F., Poirier, G., Lemaire, S., Pelletier, G. & Boucher, R., J. Biol. Chem., in press. 1. Wilber, J., Peake, G. T. & Utiger, R. (1968) ndocrinology 84, Fleischer, H., Donald, R. A. & Butcher, R. W. (1969) Amer. J. Physiol. 217, Lefkowitz, R. J., Roth, J., Pricer, W. & Pastan, I. (197) Proc. Nat. Acad. Sci. USA 65, Lefkowitz, R. J., Roth, J. & Pastan, I. (197) Nature 228, Cuatrecasas, P. (1971) Proc. Nat. Acad. Sci. USA 68, House, P. D. R. & Weidemann, M. J. (197) Biochem. Biophys. Res. Commun. 41, Freychet, P., Roth, J. & Neville, D. M., Jr. (1971) Proc. Nat. Acad. Sci. USA 68, Freychet, P., Roth, J. & Neville, D. M., Jr. (1971) Biochem. Biophys. Res. Commun. 43, Freychet, P., Roth, J. & Neville, D. M., Jr. (1971) J. Clin. Invest. 5, 34a.

5 Proc. Nat. Acad. Sci. USA 69 (1972) Plasnma-Membrane Binding of Thyrotropin-Releasing Hormone Lin, S. Y. & Goodfriend, T. L. (197) Amer. J. Physiol. 218 (5) Tomasi, V., Koretz, S., Ray, T. K., Dunnick, J. & Marinetti, G. V. (197) Biochem. Biophys. Acta 211, Rodbell, M., Krans, H. M. J., Pohl, S. L. & Birnbaumer, L. (1971) J. Biol. Chem. 246, Rodbell, M., Krans, H. M. J., Pohl, S. L. & Birnbaumer, L. (1971) J. Biol. Chem. 246, Burgus, R., Dunn, T. F., Desiderio, D., Ward, D. N., Wale, W. & Guillemin, R. (197) Nature 226, Cohen, P. P. (1957) in Monometric Techniques, ed. Umbreit, W. W., Burris, R. H. & Stauffer, J. F. (Burgess Publishing Co., Minneapolis), p Neville, D. M., Jr. (196) J. Biophys. Biochem. Cytol. 8, Lowry,. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951) J. Biol. Chem. 193, Fellows, R.. & Rogol, A. D. (1969) J. Biol. Chem. 244, Cheever,. V. & Lewis, J. J. (1969) ndocrinology 85, Vale, W., Burgus, R. & Guillemin, R. (1968) Neuroendocrinology 3, Bowers, C. Y., Lee, K. L. & Schally, A. V. (1968) ndocrinology 82, Labrie, F., Pelletier, G., Labrie, R., Ho-Kim, M. A., Delgado, A., MacIntosh, B. & Fortier, C. (1968) Ann. ndocrinol., Paris, 29, Labrie, F., Pelletier, G., Raynaud, J. P., Ducommun, P. & Fortier, C. (1969) in Metabolisme Pgriphirique et Transport Humoral des Hormones Thyroidiennes et Stgroides (Masson & Cie, Paris), p Bowers, C. Y., Weil, A., Chang, J. K., Sievertsson, H., nzmann, F. & Folkers, K. (197) Biochem. Biophys. Res. Commun. 4, Vale, W., Burgus, R. & Guillemin, R. (1967) xperientia Sutherland,. W., Rall, T. W. & Menon, T. (1962) J. Biol. Chem., 237, Robison, G. A., Butcher, R. W. & Sutherland,. W. (1969) Annu. Rev. Biochem. 37,

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