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Mesenchyme-Mediated Effect of Testosterone on Embryonic Mammary Epithelium1

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Mesenchyme-Mediated Effect of Testosterone on Embryonic Mammary Epithelium1 [CANCER RESEARCH 38, 4066-4070. November 1978) 0008-5472/78/0038-OOOOS02.00 Mesenchyme-mediated Effect of Testosterone on Embryonic Mammary Epithelium1 Heidelinde Dürnberger,Barbara Heuberger, Peter Schwartz,2 Gertraud Wasner, and Klaus Kratochwil Institut fürMolekularbiologie der österreichischen Akademie der Wissenchaften, Billrothstr. 11, A-5020 Salzburg, Austria Abstract possible endocrine therapy of breast cancer. The embryonic mammary rudiment of the mouse re Extensive information is available on intracellular events that take place after steroid application. The action of the sponds to testosterone with the formation of a condensa tion of mesenchymal cells around the gland bud and hormone is mediated by specific cytoplasmic receptors and involves the translocation of the hormone:receptor complex subsequent necrosis of the gland epithelium. Experimen into the nucleus with subsequent modification of transcrip- tal combinations of epithelium and mesenchyme of this tional activity (7). In our laboratory we are concerned with rudiment, by taking advantage of the androgen-insensi- tive mutant (Tfm, "testicular feminization"), have shown the intercellular processes that occur within the mammary gland in response to androgenic hormones. The model that the hormone acts directly on the mesenchyme, its system is the embryonic rudiment of the gland in the effect on the epithelium being indirect and mediated by mouse, which has long been known to develop differently the surrounding mesenchyme. Only the mesenchymal in female and male fetuses (22, 25). Experiments in vivo cells at the epithelial surface are capable of initiating this have implied that fetal testicular hormones are the causative reaction, and there is no oriented migration of specialized agents for this sexual dimorphism (20, 21), and we have mesenchymal cells to the gland bud in response to the shown in organ cultures of mammary rudiments that the hormone. The mesenchyme forms this condensation only gland responds directly to androgenic hormones with high around mammary epithelium; in experimental association specificity (9, 10). the epithelia of the embryonic lung, pancreas, or salivary The androgen-induced processes in the mammary gland gland remain unaffected. The experiments suggest fur ther that association of mammary epithelium with "mam take place on Day 14 of gestation, i.e., at a time when the mary" mesenchyme must exist for some time before rudiment consists only of a small epithelial bud attached to the epidermis by a somewhat thinner "stalk." The first sign hormone action to allow a response. of the reaction is the appearance of a conspicuous conden The finding that the destructive action of testosterone sation of mesenchymal cells around the epithelial bud. As on mammary epithelium is mediated by the surrounding this condensation progresses the stalk of the epithelial mesenchyme and requires organ-specific tissue interac rudiment becomes stretched and finally ruptures, separat tion is discussed in regard to its possible significance for ing the mammary epithelium from the epidermis. This an androgen therapy of metastatic breast cancer (i.e., detached piece of gland epithelium, as well as the portion mammary epithelium in nonmammary mesenchyme). of the stalk connected to the epidermis, then undergoes massive necrosis (22). A more detailed description of the Introduction cellular events in response to androgenic hormones will be given elsewhere.3-4 The presence of receptors for androgenic hormones has From histological observations it is obvious that both been demonstrated in samples of human breast cancer (4, tissues, gland epithelium and surrounding mesenchyme, 14, 17) and in mammary carcinoma cell lines of human are involved in the androgen-induced reaction (Fig. 1). (MCF-7; Refs. 6 and 13) and mouse (Shionogi 115; Refs. 2 However, the fact that testosterone was shown to act and 23) origin. Responsiveness to androgens was found in directly on the rudiment (in culture) does not necessarily some cases of human breast cancer (1), in human (13) and imply that it also acts directly on both of its tissues. The mouse (2, 23) cell lines, as well as in dimethylbenzanthra- cene-induced mammary carcinomas of the rat (19, 24). gland could only have one target tissue for the hormone, which then influences the other component through proc Whereas the response of the rat tissue involved regression esses referred to as "tissue interaction." The availability of of the tumor, the mouse and human cell lines were found to an androgen-insensitive mutant of the mouse [Tfm for be stimulated by and even dependent on androgens for "testicular feminization" (16)] makes it possible to identify their growth and maintenance in culture. the tissue responding to the hormone. Since androgenic hormones have been used with some success in the treatment of human breast cancer (1), an Materials and Methods understanding of the mechanism of action of androgens on Normal mouse embryos were hybrids of BALB/c x C3Hf mammary tissue would appear to be highly relevant for a matings. The propagation of the X-chromosome carrying 1 Presented at the John E. Fogarty International Center Conference on 3 P. Schwartz. Die Entwicklung der embryonalen Milchdrüsenanlageder Hormones and Cancer, March 29 to 31, 1978, Bethesda. Md. Supported by Maus, eine elektronenmikroskopische Untersuchung speziell der androgen- National Cancer Institute Contract N01-CB-33883. bedingten Rückbildungder Drusenanlage mannlicher Embryonen, submit 2 Present address: Anatomisches Institut der UniversitätGöttingen,West ted for publication. Germany. 4 P. Schwartz, and K. Kratochwil, Manuscript in preparation. 4066 CANCER RESEARCH VOL. 38 Downloaded from cancerres.aacrjournals.org on September 27, 2021. © 1978 American Association for Cancer Research. Tissue Interaction in Androgen Response of Mammary Gland the Tfm mutation in a separate mouse colony (derived from Table 1 3 pairs donated by Mary F. Lyon) has been described (12). The androgen response of 4 types of epitheliomesenchymal Only X'''""/Y hemizygous embryos are androgen-insensitive, combinations and these were distinguished from normal X'/Y males by The X""7Y tissues are androgen-insensitive. All other tissues [X'/Y or wild type - (wt)] are normal with regard to the Tfm locus. testing 3 mammary rudiments of each embryo for androgen Only combination type ¿,containing androgen-insensitive mesen sensitivity. X'^/X" heterozygous female embryos (derived chyme, did not yield a single responsive gland. from the same carrier females as X'""/Y embryos) could be Androgen response observed distinguished from X /X' littermates by the incomplete Combination type a.X7'"'7Y-epithelium 33/49" response of their mammary glands to testosterone. wt-mesenchyme Dating of embryos and the organ culture of mammary b. wt-epithelium 0/49 rudiments has previously been described in detail (8), as X '•»'/Y-mesenchyme well as the androgen response of intact glands in vitro. For c. X'/Y-epithelium 13/21 the recombination technique see Ref. 12. Clean separation wt-mesenchyme" of epithelium from mesenchyme was carried out after 30 d. wt-epithelium 26/30 min incubation in a solution of 2.25% trypsin (1:250) plus X'/Y-mesenchyme 0.75% pancreatin (N. F., both Difco Laboratories, Detroit, " Number of respondings glands/total number of successful Mich.). Mammary epithelia with few adhering mesenchymal combinations. cells were obtained by careful peeling of the skin of 12- or 13-day embryos (without previous enzymatic treatment). chyme and that the genotype of the epithelium is irrelevant. Mesenchyme-free epithelia of 11-day pancreas, 11-day We assume also that, in the intact gland, testosterone acts lung, and 13-day submandibular salivary gland were ob only on the glandular mesenchyme, which then, in a yet tained after a 5- to 10-min incubation in the same trypsin: unknown fashion, causes epithelial necrosis (12). pancreatin solution (5). Origin of the Mesenchymal Cells Involved in the Andro The androgen response of mammary rudiments as well gen Response. Virtually none of the mesenchymal cells as of experimental tissue combinations was observed in exhibiting the condensation characteristic of the early living expiants and further documented in histological sec stages in the androgen response showed thymidine incor tions after glutaraldehyde fixation and embedding in Epon. poration in radioautographs. The mesenchymal condensa tion therefore arises by accumulation of cells rather than by Results localized proliferation. We wondered whether this accumu lation was a strictly local phenomenon or whether some Identification of the Target Tissue for Testosterone. type of specialized mesenchymal cell would migrate from Explanted mammary rudiments (epithelium with surround more distant sites to the gland bud in response to testoster ing mesenchyme) of normal mouse embryos respond to 1 one. nw testosterone in the medium (9). Histologically, this To test the latter possibility, we combined androgen- response in vitro is identical to the appearance of affected sensitive (wild type) glands containing only a thin coat (2 to mammary rudiments in male fetuses. In contrast, glands of 3 cell layers) of equally androgen-sensitive mesenchymal androgen-insensitive (X'""/Y) embryos remain entirely un cells with a large mass of androgen-insensitive (Tfm) mes affected even with 10 ¿xMtestosterone. enchyme. All 62 of these combinations responded normally Experimental tissue combinations consisted of either (a) to
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