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Tumor Types Derived from Epithelial and Myoepithelial Cell Lines of R3230AC Rat Mammary Carcinoma1

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Tumor Types Derived from Epithelial and Myoepithelial Cell Lines of R3230AC Rat Mammary Carcinoma1 (CANCER RESEARCH 52, 1553-1560, March 15, 1992] Tumor Types Derived from Epithelial and Myoepithelial Cell Lines of R3230AC Rat Mammary Carcinoma1 Anna Sapino, Mauro Papotti, Brunella Sanfìlippo,Patrizia Gugliotta, and Gianni Bussola!i Department of Biomedicai Sciences and Human Oncology, University of Turin, Via Santena 7, Turin, 1-10126, Italy ABSTRACT MATERIALS AND METHODS Epithelial and myoepithelial cells coexist in the rat R3230AC mam Tumor. R3230AC transplantable mammary tumor was obtained mary tumor. To test the hypothesis that these two cell types constitute from Biomeasure (Hopkinton, MA) and maintained by serial s.c. trans interactive but independent neoplastic populations, we obtained in vitro plantations into the dorsal region of female Fischer 344 inbred rats (100-120 g body weight; Nossan, Correzzana, Milan, Italy). cell lines with epithelial or myoepithelial patterns and transplanted them in syngeneic animals. One stabilized line (EPI) and four cloned lines (A, Tumor fragments were obtained from nonnecrotic areas of the donor rat, mechanically dispersed in a Potter homogenizer and suspended in C, D, E) with epithelial characteristics, confirmed by positive reactions RPMI. Approximately 1 mm3 of tumor (or 1-3 x IO6neoplastic cells) for keratins in immunocytochemical and immunoblot tests, constantly gave rise in vivo to carcinomas, which, however, lacked structural and was used for monthly transplantations. The tumor consistently grew to a 2-em mass within 20 days. Animals were killed by decapitation every functional patterns typical of the original tumor. A fusiform shape and 25-35 days; tumor tissue was in part inoculated in recipient rats as immunocytochemical characteristics of myoepithelial cells were observed described above, in part fixed in absolute ethanol or methacarn for in three clones (H, I, L), which in vivo gave rise to sarcomatous and histology and immunohistochemistry (antibodies listed in Table 1), and mixed carcinosarcomatous neoplasms. These data are consistent with the in part processed for cell culture lines (see below). above hypothesis and indicate that breast carcinomas derive from epithe In order to evaluate the response to estrogen stimulation, tumor- lial cells, while sarcomatous and carcinosarcomatous neoplasms can bearing animals were given for 1 month weekly s.c. injections of originate from myoepithelial cell proliferation. This study provides data estradici valerate (20 mg/kg body weight) according to the method of suggesting myoepithelial cell involvement in the development of patho Hilf (14). logical entities occurring in the human breast and displaying mixed Establishment of Primary Stabilized and Cloned Cultures. The tumor epithelial and stromal neoplastic components, i.e.. cystosarcoma phyl- tissue, removed aseptically, was minced into small pieces (~1 mm3) loides and sarcomatous metaplasia in carcinomas. with scalpels and digested with 125 units/mg collagenase (type II) (Worthington Biochemical Corp., Freehold, NJ) in RPMI (GIBCO- Island Biological Co., Grand Island, NY), 10% PCS3 (GIBCO), 200 INTRODUCTION units/ml penicillin, 200 Mg/ml streptomycin (EUROBIO), and 2.5 mg/ ml Fungizone (GIBCO) for 2 h at 37*C. The R3230AC mammary carcinoma, transplantable in Single cell suspensions and several small tumor fragments were Fischer rats, was originally described by Hilf et al. (1) as a milk- washed twice in RPMI supplemented with 10% FCS without collagen producing adenocarcinoma. Under estrogen stimulation, it dis ase and plated in T25 flasks (Falcon Plastics, Los Angeles, CA) at a plays marked increase of milk protein production and cellular concentration of about 3 x 10s cells/flask. Incubation of the flasks for 24 h at 37'C in a 5% CO2 humidified vacuolation. The biochemical properties and hormone depend ency of this tumor have been investigated by several authors atmosphere allowed most of the fragments and free cells to attach. In (2-12). order to obtain an epithelial cell line (EPI) from the primary culture, elongated cells were removed following trypsin-EDTA treatment (15) We observed that the peculiar functional secretory similarity with a minor modification proposed by Kuzumaki et al. (16). Briefly of this carcinoma to the normal mammary gland is matched by the mixed cell sheet was rinsed once with Ca2+-and Mg2+-free PBS and a parallel similarity in structure; both epithelial and basally incubated for 3 min at 37*C in the presence of fresh trypsin-EDTA. located myoepithelial cells are present, outlining neoplastic The less rapidly detaching cells, mostly islands of epithelium-like cells, pseudoglandular structures and showing the typical immuno were rinsed and supplied with fresh medium. This procedure was cytochemical and ultrastructural characteristics of these cells in repeated every 3 days until epithelial like cells covered more than 90% the normal breast (13). of the culture surface. The R3230AC mammary carcinoma therefore represents an The stabilized EPI cells are presently at the 100th passage. Subcul tures were routinely carried out in RPMI, 10% FCS, and antibiotic. experimental model with unique morphological and functional Cell Cloning. The mixed population obtained from primary cultures properties. We have established and cloned in vitro cell lines (of R3230AC tumor) as well as the stabilized (EPI) epithelial cells were from this tumor and studied their morphology, immunocyto- cloned following the dilution plating technique proposed by Sato et al. chemistry, and function. These cell lines were further investi (17). A single cell suspension was appropriately diluted and 96-well gated by transplanting them back into syngeneic rats, where microtest plates (Falcon) were seeded; each well was inoculated with a they gave rise to carcinomas, sarcomas, and mixed carcinosar- cell suspension yielding an average of 1 cell/well. Those wells contain comas. This experimental model provides data that help to ing only one cell as ascertained by microscope inspection were consid understand the significance and genesis of peculiar and still ered available for clone establishment; the others were discarded. unexplained pathological entities occurring in the human Conditioned media were prepared by adding to the routine medium 10% of the supernatant obtained from confluent cultures of epithelial breast, i.e., cystosarcoma phylloides and sarcomatous meta cells filtered through 0.22-/im Millipore filters and stored at 4*C before plasia in carcinomas. use. We obtained 3 clones (I, H, L) from the mixed population of primary culture and 4 clones (A, C, D, E) from the EPI cell line. Received 7/22/91; accepted 1/8/92. The costs of publication of this article were defrayed in part by the payment The cell lines, at early passages, were reinjected into syngeneic of page charges. This article must therefore be hereby marked advertisement in animals and subcultured until passage 80. accordance with 18 U.S.C. Section 1734 solely to indicate this fact. 1This work was supported by grants from the CNR (Rome), AIRC (Milan), 3The abbreviations used are: FCS, fetal calf serum; PBS, phosphate-buffered saline; NTEN, 50 miviTris, pH 7.4-0.15 M NaCI-2 mM EDTA-0.1% Nonidet P- and the Ministry of the University. 2To whom requests for reprints should be addressed. 40; sm, smooth muscle. 1553 Downloaded from cancerres.aacrjournals.org on October 2, 2021. © 1992 American Association for Cancer Research. MAMMARY CARCINOMA CELL LINES In Vitro Hormonal Stimulation. Primary cultures, stabilized EPI cells, routinely stained with hematoxylin and eosin and processed for im- and clones D and E were cultured in Petri dishes and on glass coverslips munocytochemical characterization using the antibodies listed in Table for 9 days in a basal medium containing 10 * M 17/3-estradiol (Merck, 1. To detect immunological binding, the avidin-biotinylated peroxidase Darmstadt, Germany) and 10% of charcoal-adsorbed PCS (18). complex procedure (21) was used, after treatment of the sections with The medium was changed every 3 days. the appropriate biotinylated secondary antisemiti (Vector, Burlingame, a-Lactalbumin production was estimated immunocytochemically. CA). Light Microscopy. The morphological appearance of living cultures In Vivo Hormonal Stimulation. Animals bearing palpable tumors in flasks was observed on a Leitz Labovert inverted microscope fitted obtained from EPI, D, E, H, and I cells were treated with estrogen with phase contrast. Mixed cells from primary cultures, EPI cells, and following the protocol used in R3230AC-bearing animals (see above). clones were also grown on glass coverslips; fixed in methanol; and stained by the Papanicolaou method for cytological examination. For immunohistochemical tests, cells were grown on glass coverslips, RESULTS fixed in methanol for 5 min at -20'C, permeabilized in acetone for 5 s at —¿20*C,andréhydratée!withpig normal serum (diluted 1:5(1in PBS Serially Transplanted R3230AC Tumors. The gross and mi for 20 min). Cells were incubated at 37'C for 60 min with the primary croscopic appearances of the R3230AC mammary tumor, de antibodies listed in Table 1 and then with the appropriate fluorescein- scribed in detail elsewhere (13), were examined at each labeled secondary antisera (Sera-Lab, Ltd., Sussex, England) diluted transplantation. 1:10 in PBS for 30 min at room temperature, following a standard The tumors were mostly well delimited, but focal invasion of indirect immunofluorescence procedure. the adjacent muscular layers was observed in some cases. Dis Electron
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