NOTE- HUMAN BREAST CANCER SERIALLY TRANSPLANTABLE IN NUDE MICE IN ASCITES FORM*1

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1 NOTE- HUMAN BREAST CANCER SERIALLY TRANSPLANTABLE IN NUDE MICE IN ASCITES FORM*1 Setsuo HIROHASHI,*2 Yukio SHIMOSATO, Kanji NAGAI,*3 Tsutomu KOIDE, and Toru KAMEYA Pathology Division, National Cancer Center Research Institute*4 Cell suspension of a human breast cancer cell line (Hattori line) was injected intraperitoneally into an athymic nude mouse to produce ascites form breast cancer (peritoneal carcinomatosis). Subsequent serial transfers of cancer cells in as- tumor cells died of accumulation of ascites after a latency period averaging 4 weeks, with one exception which died of a wasting disease. Multiple lung metastases were observed in some mice. The tumor cells retained cytological characteristics of the original cell line, and histology of the infiltrating tumor in the peritoneum and omentum was that of poorly differentiated adenocarcinoma. Differentiation not only toward acinar or duct lining cells but also toward myoepithelial cells was observed by histochemistry, immunohistochemistry, and electron microscopy. Ascites form cancer is a good experimental model that bears advantages of cultured cells in vitro as well as those of solid tumors in vivo. Studies on cancer chemotherapy have been greatly accelerated by the use of animal cancers which proliferate in ascites form. Thus, we attempted to establish ascites form human cancers in athymic nude mice, which were successfully used for the subcutaneous transplantation of some human neoplasms.6, 10) The present report deals with our prelimi - nary results on biological and morphological characteristics of a human breast cancer in ascites form serially transplantable in nude mice (BALB/c nu/nu), which was designated as Br-13 and is now in the fifth passage. Materials and Methods Tumor Cells The tumor cells used were cells maintained in vitro which were derived from cells in pleural fluid of a 28-year-old Japanese female with advanced breast cancer. The strain (Hattori line) was established in December, 1973, by 106 at 86th passage were inoculated into a mouse. Animals Athymic nude mice, male and female, 4 to 8 weeks old, with the genetic background of BALB/c were used for the experiments. These mice were supplied from the Central Laboratory for Experimental Animals (Kawasaki), and bred and maintained in a specific pathogen-free condition.8) The experiments were carried out in the flexible film vinyl isolators under the same condition. Method of Transplantation Initially, cultured tumor cells in RPMI-1640 medium were injected intraperitoneally. Serial transfers were carried out similarly by injecting tumor cells in ascites directly or those washed and suspended in the *1 This work was supported in part by a Grant-in-Aid for Cancer Research from the Ministry of Health and Welfare, and from the Ministry of Education, Science and Culture. This paper constitutes Part IV of a series on transplantable human cancers in nude mice. 431

2 S. HIROHASHI, ET AL. same culture medium. The number of tumor cells was counted at the time of transfer. Morphological Observations (1) For light microscopy, smears of ascites were rapidly dried and fixed with 100% methanol for I min, and solid tumors and organs were fixed with 10% Formalin. Staining methods used were Giemsa stain, Hematoxylin and Eosin stain, periodic acid-schiff (PAS) reaction, PAS reaction after digestion with amylase, Alcian Blue stain, and phosphotungstic acid-hematoxylin (PTAH) stain. Enzyme histochemical studies were also carried out on acid and alkaline phosphatases,1,3) and non-specific esterase.2) (2) Tumor cells were examined for the presence of actomyosin in the cytoplasm by using the indirect immunofluorescence method. Air-dried smears were fixed with 95% ethanol for 10min. Immunostainings were made as usual, using antihuman uterine actomyosin rabbit serum as the 1st antibody, and FITC-labeled anti-rabbit r-globulin goat serum (Miles Lab., Inc., Kankakee, Ill.) as the 2nd antibody. The following controls were used: (a) Normal rabbit serum followed by the 2nd conjugated antibody, (b) rabbit anti-human chorionic gonadotropin serum4) (unrelated antibody), followed by the 2nd conjugated antibody, (c) anti-actomyosin, followed by the non-labeled 2nd antibody, and then by the 2nd conjugated antibody (inhibition test). Extraction and purification of actomyosin from the human uterus (surgical material) and preparation made according to Knieriem.5) of antisera were (3) For electron microscopy, fixed in 1.25%glutaraldehyde, cell blocks were postfixed with 1.0% OsO4, dehydrated in graded ethanol, and embedded in Epon 812 through QY-1. Ultrathin sections were double-stained with uranium and lead. Chromosomal Analysis The cells were treated for 4 hr with Colcemid (10-6M), swollen by hypotonic solution, fixed in Carnoy's solution, and stained with Giemsa solution. Results and Discussion passage suspended in culture medium were injected intraperitoneally into a female nude mouse. Marked abdominal distension due to retention of ascites was noticed 65 days after inoculation (Photo 1). The ascites was blood- The minimum number of tumor cells required for successful serial transfer was determined by inoculating graded number of culture medium only to female mice. Each group consisted of 3 mice. All the mice 90 days after transplantation, with no detectable tumor cells in the peritoneal cavity. On the other hand, all the female and 2 of 3 of excessive accumulation of blooded ascites. The interval between inoculation and death was about 4 weeks (21 to 39 days) and 10ml or less of ascites containing more than 107 tumor cells/ml could be obtained from each dead mouse. One male mouse inoculated no tumor cells were found in the small amount of ascites. Smears of the ascites consisted almost entirely of tumor cells and rare mononuclear cells probably of the mouse origin. Tumor cells were floating free in the ascites, with little tendency to form cell aggregates, which were spherical and large, and moderately variable in size. They had a large finely reticular nucleus and a few nucleoli. A good number of cells possessed clear perinuclear halo and strongly basophilic peripheral cytoplasmic rim by Giemsa stain (Photo 2). PASpositive fine granules were present in the cytoplasm, which were digested by amylase, being glycogen. Epithelial mucin, positively stained with Alcian Blue and PAS, was found in the cytoplasm of some cells. These cytological characteristics were similar to those of cultured tumor cells.7,9) Actomyosin was positively stained in the area corresponding to the perinuclear halo by the indirect immunofluorescence method (Photo 3). Tumor cells were negative for alkaline phosphatase, negative or faintly positive for acid phosphatase, and positive for non-specific esterase activities. Electron microscopically tumor cells possessed microvilli, secretory granules, and occasional intracellular lumina equipped with microvilli (Photos 5 and 6). The cytoplasm 432 Gann

3 TRANSPLANTABLE HUMAN BREAST CANCER of some tumor cells was divided into three zones; the inner perinuclear zone with frequent mitochondria, the mid zone with a large number of fibrils of about 10nm thick arranged in coarse bundles in some areas, and the outer zone with a few mitochondria, rough endoplasmic reticulum, and secretory granules. The inner and mid zones corresponded to the perinuclear halo observed in Giemsa stained cells and to the area of actomyosin localization disclosed by the indirect immunofluorescence method. No cellular attachments were evident, since no cell clumps were observed. However, an increased number of microvilli were found where cells faced close to each other (Photo 5). The peritoneal surface of the initially transplanted mouse showed diffuse proliferation of moderately anaplastic cells with small inconspicuous nest formation (Photo 4a, b). A few crescent cells positively stained with PTAH stain suggestive of myoepithelial cells were found at the border of such nests. A few cells possessed intracytoplasmic mucin positively stained with Alcian Blue and PAS. The histological features were compatible with those of poorly differentiated ductal carcinoma of the human breast. Bilateral lung metastases were found in 2 of 5 mice at the 2nd passage. The presence of epithelial mucin, secretory granules, and intracytoplasmic lumina equipped with microvilli indicates differentiation of tumor cells toward acinar or duct lining cells, and the presence of actomyosin, PTAHpositive materials, and bundles of fibrils in cytoplasm indicates differentiation toward myoepithelial cells. The chromosomal analysis of ascites tumor cells of the 2nd passage disclosed an aneuploid human karyotype, with a mode of 80 A variety of human neoplasms serially transplantable in the subcutaneous tissue of nude mice have been established,6,10) but slow growth of human solid tumors and prolonged survival of tumor-bearing mice in 67(3) 1976 general impeded effective performance of screeing antitumor agents and of experimental studies for cancer chemotherapy. In this sense, the ascites-form human breast cancer established here may become a useful system for such purposes. Although the fact that the tumor was transplantable in both male and female mice indicates hormone independency of this tumor, at least in an ascites form, there remains a possibility that treatment with cyclic nucleotides or other chemicals may change it hormone dependent, as suggested by recent in vitro investigation.11) Establishment of hormone-dependent, ascites-form human breast cancer transplantable in nude mice is desired from basic and clinical standpoints. A variety of human cancers proliferating free in the peritoneal cavity of mice may become good models for experimental chemotherapy and for studies on tumor cell differentiation and growth. The authors are greatly indebted to Drs. K. Minato and M. Shimoyama for providing them the cultured cells of Hattori line. Their thanks are extended to Dr. I. Nagashima for karyotype analysis and also to Prof. K. Kageyama for his kind discussions and encouragement. (Received December 27, 1975) REFERENCES 4) Kameya, T., Kuramoto, H., Suzuki, K., Kenjo, T., Oshikiri, T., Hayashi, H., Ita- 6) Kuga, N., Yoshida, K., Seido, T., Oboshi, S., Koide, T., Shimosato, Y., Nomura, T., 7) Minato, K., Shimoyama, M., Kaneda, H., Kimura, K., Oboshi, S., Kamata, N., Proc. Jpn. Cancer Assoc., 33rd Annu. Meet., 15 (1974). 8) Nomura, T., Ito, T., Proc. First Int. Workshop

4 S. HIROHASHI, ET AL. 10) Shimosato, Y., Kameya, T., Nagai, K., Hirohashi, S., Koide, T., Hayashi, H., Nomura, T., J. Natl. Cancer Inst., 56 (1976), in press. 11) Tsuji, K., Hayata, Y., Shimosato, Y., Koide, T., Fukushima, Y., Igaku-no-Ayumi (1976), in press. EXPLANATION OF PLATES Photo 1. Marked distention of abdomen of a female mouse due to accumulation of ascites 80 equipped with microvilli. x 11,500. Photo 2. Giemsa stain of a smear prepared from ascites, showing tumor cells with perinuclear Photo 4. (a) Diffusely infiltrating anaplastic carcinoma in the superficial layer of the parietal peritoneum of the mouse shown in Photo 1. H- (b) Higher magnification of infiltrating tumor Photo 3. Positive immunofluorescence for actomyosin in cytoplasm of tumor cells correspond- Photo 5. Electron-micrograph of ascites tumor cells with microvilli on the surface, and bundles of fibrils in the mid zone of cytoplasm. Microvilli are better developed in areas where two Photo 6. Electron-micrograph of an ascites tumor cell possessing an intracytoplasmic lumen Photo 8. Karyotype of an ascites tumor cell revealing 78 human chromosomes. 434 Gann

5 TRANSPLANTABLE HUMAN BREAST CANCER 67(3)

6 S. HIROHASHI, ET AL. 436 Gann

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