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Cytoplasmic and Nuclear Binding Components for La,25-Dihydroxyvitamin D3 in Chick Parathyroid Glands (Vitamin D/Receptors/Parathyroid Hormone) PETER F

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Cytoplasmic and Nuclear Binding Components for La,25-Dihydroxyvitamin D3 in Chick Parathyroid Glands (Vitamin D/Receptors/Parathyroid Hormone) PETER F Proc. Nat. Acad. Sci. USA Vol. 72, No. 12, pp. 4871-4875, December 1975 Biochemistry Cytoplasmic and nuclear binding components for la,25-dihydroxyvitamin D3 in chick parathyroid glands (vitamin D/receptors/parathyroid hormone) PETER F. BRUMBAUGH, MARK R. HUGHES, AND MARK R. HAUSSLER Department of Biochemistry, College of Medicine, University of Arizona, Tucson, Ariz. 85724 Communicated by John H. Northrop, September 29, 1975 ABSTRACT Specific binding of la,25-dihydroxyvitamin role of 1a,25-(OH)2D3 in the homeostatic regulation of cal- D3 [la,25(OH)2D3J to macromolecular components in the cy- cium and phosphate can be elucidated. toplasm and nucleus is demonstrated in parathyroid glands Henry and Norman (14) have recently reported that of vitamin-D-deficient chicks. The interaction of la,25- (OH)WD3 with the cytoplasmic binding component is of high la,25-(OH)2[3H]Da is localized in chick parathyroid glands affinity (R4 = 3.2 X 10-10 M) and high specificity [la,25- following administration of the sterol, in vivo. In the present (OH)2D3 > 25-hydroxyvitamin D3 > la-hydroxyvitamin D3 > experiments, specific binding components for 1a,25- vitamin D3 in competing with radioactive la,25(0H)2D31. (OH)2D3 have been isolated from chick parathyroid glands Both cytoplasmic and nuclear hormone-macromolecular and characterized in vitro. Previous reports (15, 16) have complexes sediment at 3.1 S in 0.3 M KCI-sucrose gradients, demonstrated that 1la,25-(OH)2D3 interacts with the intes- and agarose gel filtration of the components indicates an ap- parent molecular weight of 58,000. The 3.1S binding mole- tine in a manner similar to the binding of steroid hormones cules are not observed in adrenal gland, testes, liver, or kid- to their respective target organs. 1a,25-(OH)2D3 enters the ney, but similar receptors for la,25-(0H)2D3 have been found intestinal cell and binds to a 3.7S cytoplasmic receptor pro- previously in intestine. tein (17, 18). The hormone receptor complex then migrates Macromolecular species with a high affinity and prefer- into the nucleus in a temperature-dependent process, where ence for 25-hydroxyvitamin D3 [25(0H)D3] are also identi- it associates with the chromatin (15, 17-19). We report here fied in parathyroid cytosol and differ from the parathyroid similar intracellular receptor proteins for la,25- la,25(OH)WD3-binding component in that: (1) they sediment that at 6 S in 0.3 M KCI-sucrose gradients, (2) they are observed in (OH)2D3 exist in chick parathyroid glands. all tissues examined, (3) they have a higher affinity for 25- (OH)D3 than la,25-(0H)2D3, and (4) they are not found in the MATERIALS AND METHODS- nucleus of the parathyroid glands, in vitro. The discovery of unique la,25.OH)2D3-binding components in the parathy- Materials. Animals used in experiments were White Leg- roid glands is consistent with the sterol hormone's action at horn cockerels (kindly donated by Demler Farms, Anaheim, this endocrine site and possible involvement in the regula- Calif.) that were raised for 6 weeks on a vitamin-D-deficient tion of parathyroid hormone synthesis and secretion. diet (20). 25-Hydroxy[26(27)-methyl-3H]vitamin D3 (6.5 Ci/ mmol) was obtained from Amersham-Searle. Vitamin D3 action to mobilize calcium and phosphate at in- Preparation of la,25-Dihydroxy[3Hjvitamin D3, In testine and bone is thought to be mediated by the metabolite Vitro. la,25-Dihydroxy[26(g7)-methyl-3H]vitamin D3 was la,25-dihydroxyvitamin D3 [la,25-(OH)2D3] (1-4). Its pro- prepared as previously described (19). Radiochemical purity duction from 25-hydroxyvitamin D3 [25-(OH)D3] by the of generated la,25-dihydroxy[3H]vitamin D3 was 98%. 25- renal la-hydroxylase appears to be regulated by calcium (5), Hydroxy[26(27)-methyl-3H]vitamin D3 substrate for the re- phosphate (6, 7), parathyroid hormone (PTH) (7, 8), and the action was purified by Celite liquid-liquid partition chro- vitamin D status of the animal (9). Evidence suggests that matography (21). The radiochemical purity of the 25-hy- hypocalcemia stimulates PTH secretion which in turn en- droxy[3H]vitamin D3 was 95%, and its specific activity was hances the production of la,25-(OH)2D3 at the kidney (7, determined by ultraviolet absorbance spectrophotometry at 8). Thus PTH, rather than calcium, may be the dominant 265 nm. modulator of the renal la-hydroxylase (10) and the finding Exposure of Chick Tissue Subfractions to Radioactive of abnormal circulating 1a,25-(OH)2D3 in humans with Sterols, In Vitro. Homogenates [300 mg wet weight (20 parathyroid disease is consistent with this concept (11, 12). parathyroid glands)/3 ml] were made in 0.25 M sucrose, DeLuca has proposed that PTH and phosphate deficiency 0.05 M Tris-HCI, pH 7.4, 0.025 M KCI, and 5 mM MgC12 may be functioning through a common intracellular mecha- (0.25 M sucrose-buffer A) with a Potter-Elvehjem homoge- nism to enhance the la-hydroxylase by lowering the phos- nizer equipped with a Teflon pestle at 00 by six passes, with phate level in the renal cell (10). Moreover, MacIntyre and 2 min cooling periods between passes. Homogenates were associates (13) have suggested that la,25-(OH)2D3 might centrifuged at 1200 X g for 10 min. Nuclear pellets were re- control its own biosynthesis directly at the kidney by a nega- moved, and the resulting supernatant was centrifuged at tive feedback mechanism involving the de novo synthesis of 100,000 X g for 1 hr at 0° to yield a final supernatant frac- the la-hydroxylase enzyme. Clearly, the fashion in which tion (cytosol). The cytosol (0.2-1.0 ml) was incubated with la,25-(OH)2D3, PTH, and phosphate deficiency interact to sterol (in 20,l ethanol) for 1 hr at 00 and then analyzed for control the formation of 1a,25-(OH)2D3 at its kidney endo- sterol binding components. crine site must be completely understood before the exact Purified nuclear extracts (chromatin) were prepared from nuclear pellets by a modification (7) of the method of Haus- Abbreviations: 25-(OH)D3, 25-hydroxyvitamin D3; la-(OH)D3, sler et al. (1) and were resuspended in 0.01 M Tris-HCl, pH la-hydroxyvitamin D3; la,25-(OH)2D3, la,25-dihydroxyvitamin 7.5, and centrifuged for 20. min at 48,000 X g. The pellet D3; PTH, parathyroid hormone. from 300 mg of tissue was reconstituted with cytosol (2.5 ml) 4871 Downloaded by guest on October 1, 2021 4872 Biochemistry: Brumbaugh et al. Proc. Nat. Acad. Sci. USA 72 (1975) and incubated for 1 hr at 25° with sterol (in 40 Al of etha- nol). Chromatin was harvested and extracted with 0.3 M KC1, 0.01 M Tris-HCl, pH 7.5, 1.5 mM EDTA, 12 mM 1- thioglycerol (0.3 M KCl-Buffer B). Extracts were centri- fuged at 48,000 X g for 20 min, and the resulting superna- tants were analyzed for sterol-binding activity. Sucrose Gradient Centrifugation. Linear gradients (5.0 ml) of 5-20% sucrose in 0.3 M KCI-Buffer B were prepared with a Buchler gradient mixer, Auto-Densi Flow, and Poly- staltic pump. Aliquots (0.3 ml) of cytosol or nuclear extracts were layered on gradients and centrifuged at 234,000 X g (average force) for 24 hr at 00 with the use of a Beckman L3-50 ultracentrifuge and an SW 50.1 rotor. The fractions (6 drops each) were counted in 5 ml of liquid scintillation mix- ture A (3% Liquifluor in toluene-Triton X-114, 3:1) in a Beckman LS-233 scintillation counter (35% efficiency). Sedi- mentation coefficients were estimated by comparison with protein markers (chymotrypsinogen, 2.5 S; ovalbumin, 3.67 S; and bovine serum albumin, 4.4 S). Agarose Gel Filtration. All chromatographic procedures were carried out at 1-3'. Agarose beads (Bio-Gel A-0.5m, 100 to 200 mesh from Bio-Rad) were equilibrated with 0.3 M KCI-Buffer B and poured into a column (1.6 X 60 cm). Samples (1.0 ml) of nuclear extracts or cytosol incubations were applied to the column and 1-ml fractions were collect- ed and counted (30% efficiency). The optical density of 20 TOP 10 fractions was measured with a Gilford 240 spectrophotome- FRACTION NUMBER ter. Column flow rates were maintained at 13-14 ml/hr FIG. 1. Sucrose gradient centrifugation of la,25-(OH)2D3 and with a Polystaltic pump. 25-(OH)D3-binding components in parathyroid glands and nontar- Filter Assay for Specific Macromolecular Binding. Sep- get organs. Incubations were carried out as follows: (A) Parathy- aration of bound from free sterol was achieved the filter roid cytosol (0.3 ml) at 00 for 1 hr with 3 nM la,25-(OH)2[3H]D3 by (6.5 Ci/mmol) alone (0), or with 0.3 gM unlabeled la,25-(OH)2D3 assay method of Santi et al. (22). Aliquots of cytosol (0.2 ml) (0), or with 6 nM nonradioactive 25-(OH)D3 (A). (B) Reconsti- containing la,25(OH)2[3H]D3 and samples containing the tuted cytosol-chromatin from parathyroid (@), adrenal (A), or same concentration of 1a,25-(OH)2[3H]Ds plus a 100-fold testes (A) was incubated with 6 nM la,25-(OH)2[3H]D3 for 1 hr at excess of unlabeled hormone were incubated at 00 for 2 hr. 250. The chromatin was then extracted with 0.3 M KCl-Buffer B. was then to DEAE-cellulose filters Parallel incubation with parathyroid cytosol-chromatin, 6 nM Cytosol (150 Al) applied lz,25-(OH)2[3H1D3, and 0.6 'M unlabeled la,25-(OH)2D3 was per- (Whatman DE 81) and washed with three 1-ml portions of formed (0).
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