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Direct Action of 17/3-Estradiol on Mouse Mammary Ducts Analyzed by Sustained Release Implants and Steroid Autoradiography1

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Direct Action of 17/3-Estradiol on Mouse Mammary Ducts Analyzed by Sustained Release Implants and Steroid Autoradiography1 [CANCER RESEARCH 47, 6052-6057, November 15. 1987] Direct Action of 17/3-Estradiol on Mouse Mammary Ducts Analyzed by Sustained Release Implants and Steroid Autoradiography1 Charles W. Daniel,2 Gary B. Silberstein, and Phyllis Strickland Department of Biology, Thimann Laboratories, University of California, Santa Cruz, California 95064 ABSTRACT association of stroma, and indeed the stroma might be the site of initial action by the hormone. 17,M .stradini is a recognized mammary mitogen, but uncertainty exists A different approach to the problem of estradiol action has as to whether its normal action is mediated exclusively through the been the direct application of steroid to the gland in vivo. By pituitary or whether in addition direct effects of estradiol on mammary applying estrone to the skin in the nipple area of male monkeys tissue may play a role in mammary growth and development. To further investigate the action of estradiol on the developing mammary ductal (10,11), rabbits (12), and guinea pigs ( 13) lobuloalveolar growth system of young mice, implants of biocompatible ethylene vinyl acetate was stimulated in the treated compared with the untreated copolymer, which deliver small amounts of steroid locally to the target glands. Implantation of estrogens in cholesterol pellets into the tissue, were implanted into the mammary glands of castrated females in mammary glands of ovariectomized virgin mice did not produce which the ductal system was static and end buds had regressed. Within local glandular growth (14). 3 days end buds appeared in the vicinity of the implants but not elsewhere An improved technique for local administration of hormones in the gland and not in other glands of the animal, indicating direct and growth factors has recently become available in which small stimulation. The new end buds were histologically normal, displaying a plastic EVAc implants capable of the slow release of nondena- visible cap (stem) cell layer with high levels of DNA synthesis. The tured bioactive molecules are placed directly into the gland (15). antiestrogen keoxifene, which competes with estrogen for its receptors, inhibited end bud formation in the estradiol-implanted gland but failed EVAc pellets may be implanted to any area of interest with to inhibit growth when implanted into the glands of intact, 5-week-old local effects of released molecules readily distinguishable from females. Time course and dose-response studies of estradiol stimulation systemic influences. This technique allows both qualitative and were carried out in ovariectomized animals and were consistent with a quantitative assessments of hormone effects. direct action for estrogen. Steroid autoradiography revealed estrogen In this communication we report that implanted estrogen can receptors in the lumenal cells of the end bud, in ductal epithelium, and directly stimulate mammary ductal growth in castrated female in stroma adjacent to ducts, but none was detected in the rapidly prolif mice without causing systemic stimulation and that this effect erating cap cells. We conclude that estrogen, perhaps acting on nonepi- can be blocked by a competitive inhibitor of estradiol binding. thelial target cells and probably in conjunction with extramammary Steroid autography revealed a gradient of estradiol receptors in factors, directly stimulates mammary ductal growth. the mammary ducts and the presence of receptors in the stroma of the developing gland. INTRODUCTION In vivo, estradiol3 is known to play a critical role in stimulat MATERIALS AND METHODS ing growth of the mouse mammary gland during the ductal Materials. EVAc (Elvax 40P) was a gift of DuPont Chemical Com phase of development (1). Administered systemically to cas pany, Universal City, CA. Steroid hormones and tatnoxifen were ob trated female mice, it has the specific effect of restoring the tained from Sigma Chemical Company, St. Louis, MO. The antiestro mammary end buds, the growth points for ductal elongation. gen keoxifene (LY 156758) was a gift of Eli Lilly Company, Indian These restored end buds display normally high levels of DNA apolis, IN (16). synthesis (2). Because estradiol is ineffective in restoring mam Animals and Surgical Procedures. Virgin C57/BL/crl mice were mary growth in ovariectomized-hypophysectomized animals, castrated at 5 wk of age and were used for implant experiments 6 wk its action on the gland is considered to be indirect,4 through or more after surgery. Preparation of Implants. EVAc implants were prepared as described stimulation of pituitary prolactin secretion (3, 4). Further evi by Rhine et al. (17). EVAc was washed for 1 wk prior to use in several dence supporting an indirect role for the steroid is found in changes of 95% ethanol with continuous stirring and dissolved in several in vitro studies in which estradiol added to culture méthylènechlorideto give a 20% w/v solution. Steroids were dissolved medium failed to stimulate proliferation in primary cultures of directly in the EVAc solution, and the solution was quick frozen in an mouse mammary epithelial cells (5-7). acetone-dry ice bath for 10 min. The frozen pellet was stored for 2 days An additional, more direct role for estrogen in mammary at -20°C,after which it was placed under a mild vacuum for another 2 growth and development is indicated by recent in vitro studies days at room temperature. The dried pellet was cut into approximately 1.0-mm2 pieces and weighed. of mixed cultures of mammary epithelial and mammary stromal cells, in which epithelial proliferation was enhanced by the Release of Estradiol from EVAc. The release kinetics of estrogen was studied in vitro. Pellets prepared with 86 ng/mg EVAc. and containing addition of estradiol to the culture medium (8, 9). These exper 9 x 10" cpm/mg EVAc 17/3-[3H]estradiol (NEN), were cut into implant- iments suggest that estradiol action may require the close sized pieces, weighed, and sealed in porous nylon mesh bags (Nitex) which were then placed in 1.5 ml normal saline at 37°Con a rotator (1 Received 5/18/87: revised 8/11/87; accepted 8/18/87. The costs of publication of this article were defrayed in part by the payment rpm). At 24-h intervals, the bags were removed and 0.5 ml of the saline of page charges. This article must therefore be hereby marked advertisement in was counted in Biofluor (NEN). Bags were then rinsed and replaced in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. ' Supported by NSF Grant PCM83-0814. fresh saline. 2To whom requests for reprints should be addressed. Implantation of EVAc. Recipient mice were anesthetized with Nem- 3The abbreviations used are: estradiol. 170-estradiol; EVAc, ethylene vinyl butal (60 ¿ig/gbodyweight) and the third and fourth mammary glands acetate copolymer (Elvax 40P; DuPont Chemical Company). 4Our use of the terms "direct" and "local" throughout this paper do not imply were exposed by reflecting the abdominal skin. A small pocket was made in the mammary fat pad using Dumont forceps which were then a particular mode of action at the cellular level; estradiol could act either as a primary mitogen or. as suggested by these and other results, as a means of used to insert the implant. In the case of double implants, both were sensitizing the gland to systemic factors. inserted into the same pocket. The abdominal skin was closed with 6052 Downloaded from cancerres.aacrjournals.org on September 28, 2021. © 1987 American Association for Cancer Research. DIRECT STIMULATION OF MAMMARY DUCTS BY ESTRADIOL wound clips and the animals were allowed to recover in an atmosphere virgin mice at 5 wk of age is arborated and fills approximately of95%O2-5%CO2. 50% of the available fatty stroma. In hormonal h intact animals Steroid Autoradiography. Virgin female C57/BL mice were ovariec- the tips of most branches display large end buds (19). Ovariec tomized at 5 wk of age, 2 days prior to treatment, to reduce the levels tomy resulted in an approximately linear decline in end bud of endogenous estrogen. Each of three experimental animals received an injection of 200 //C ['HJestradiol in 40 ^1 100% ethanol with 0.2 ml number, end bud size, and ductal caliber. After 2 wk ducts were balanced salt solution and 2 UKBSA. Control animals also received a thin, no end buds were seen (Figs. 1 and 2), and there was no second injection containing 200-fold excess estradiol or testosterone DNA synthesis in the regressed gland (Fig. ID). propionate in the same vehicle, and animals in the experimental group The time course of the estrogen response was investigated. received a second injection consisting of vehicle only. Mice, ovariectomized for at least 6 wk, were implanted with a Animals were sacrificed by cervical dislocation 2 h after injection. single EVAc pellet containing 25 ng estradiol, a dose which Strips of mammary' glands were taken in the end bud region and near produced a maximal local response. Whole mount preparations the nipple. Control tissues included uterus, bladder, and mammary fat of glands were scored for numbers of end buds after which pad from an area of the gland not occupied by mammary ducts. Tissue representative areas were excised and processed for [3H]thymi- was flattened on strips of cardboard, flash frozen in liquid propane, and stored at -70°C. Sections of 5 pm were cut on a Tissue Tek II dine autoradiography from which labeling indices were deter cryostat at —30°C.Inthe dark, frozen sections were transferred to mined. Fig. 3 shows that end buds appeared on Day 3, were slides predipped in Kodak NTB-2 photographic emulsion diluted 1:1 most numerous on Day 4, and decreased in number and size with water by the method of Stumpf and Sar (18).
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