Summary
In an accompanying report (Moreno-Cuevas, J. E.; Sirbasku, D. A., In Vitro Cell. Dev. Biol.; 2000), we demonstrated 80-fold estrogen mitogenic effects with MTW9/PL2 rat mammary tumor cells in cultures supplemented with charcoaldextran-treated serum. All sera tested contained an estrogen reversible inhibitor(s). The purpose of this report is to extend those observations to additional sex steroid-responsive human and rodent cell lines. Every line tested showed a biphasic response to hormone-depleted serum. Concentrations of ≤10% (v/v) promoted substantive growth. At higher concentrations, serum was progressively inhibitory. With estrogen receptor-positive (ER+) human breast cancer cells, rat pituitary tumor cells, and Syrian hamster kidney tumor cells, 50% (v/v) serum caused significant inhibition, which was reversed by very low physiologic concentrations of estrogens. This same pattern was observed with the steroid hormone-responsive LNCaP human prostatic carcinoma cells. Because steroid hormone mitogenic effects are now easily demonstrable using our new methods, the identification of positive results has nullified our original endocrine estromedin hypothesis. We also evaluated autocrine/paracrine growth factor models of estrogen-responsive growth. We asked if insulin-like growth factors I and II, insulin, transforming growth factor alpha, or epidermal growth factor substituted for the positive effects of estrogens. Growth factors did not reverse the serum-caused inhibition. We asked also if transforming growth factor beta (TGFβ) substituted for the serum-borne inhibitor. TGFβ did not substitute. Altogether, our results are most consistent with the concept of a unique serum-borne inhibitor as has been proposed in the estrocolyone model. However, the aspect of the estrocolyone model related to steroid hormone mechanism of action requires more evaluation. The effects of sex steroids at picomolar concentrations may reflect mediation via inhibitor “activated” intracellular signaling pathways.
Similar content being viewed by others
References
Allegra, J. C.; Lippman, M. E. Growth of a human breast cancer cell line in serum-free hormone supplemented medium. Cancer Res. 38:3823–3829; 1978.
Amara, J. F.; Dannies, P. S. 17β-Estradiol has a biphasic effect on GH cell growth. Endocrinology 112:1141–1143; 1983.
Anderson, J. N.; Clark, J. H.; Peck, E. J., Jr. The relationship between nuclear receptor estrogen binding and uterotrophic responses. Biochem. Biophys. Res. Commun. 48:1460–1468; 1972.
Anderson, J. N.; Peck, E. J., Jr.; Clark, J. H. Nuclear receptor estradiol complex: a requirement for uterotropic responses. Endocrinology 95: 174–178; 1974.
Anderson, J. N.; Peck, E. J., Jr.; Clark, J. H. Estrogen-induced uterine responses and growth: relationship to receptor binding by uterine nuclei. Endocrinology 96:160–167; 1975.
Aronica, S. M.; Kraus, W. L.; Katzenellenbogen, B. S. Estrogen action via the cAMP signaling pathway: stimulation of adenylate cyclase and cAMP-regulated gene transcription. Proc. Natl. Acad. Sci. USA 91: 8517–8521; 1994.
Arrick, B. A.; Korc, M.; Derynck, R. Differential regulation of expression of three transforming growth factor beta species in human breast cancer cell lines by estradiol. Cancer Res. 50:299–303; 1990.
Arteaga, C. L.; Coffey, R. J.; Dugger, T. C., et al. Growth stimulation of human breast cancer cells with anti-transforming growth factor β antibodies: evidence for a negative autocrine regulation by transforming growth factor β. Cell Growth Differ. 1:367–374; 1990.
Arteaga, C. L.; Kitten, L. J.; Coronado, E. B., et al. Blockade of the type 1 somatomedin receptor inhibits growth of human breast cancer cells in athymic mice. J. Clin. Invest. 84:1418–1423; 1989.
Arteaga, C. L.; Tandon, A. K.; von Hoff, D. D., et al. Transforming growth factor β; potential autocrine growth inhibitor of estrogen receptor negative human breast cancer. Cancer Res. 48:3898–3904; 1988.
Bansal, G. S.; Cox, H. C.; Marsh, S., et al. Expression of keratinocyte growth factor and its receptor in human breast cancer. Br. J. Cancer 75: 1567–1574; 1997.
Barnes, D.; Sato, G. Growth of a human mammary tumor cell line in serum-free medium. Nature (Lond) 281:388–389; 1980.
Beato, M. Gene regulation by steroid hormones. Cell 56:335–344; 1989.
Bélanger, C.; Veilleux, R.; Labrie, F. Stimulatory effects of androgens, estrogens, progestins, and dexamethasone on growth of the LNCaP human prostate cancer cells. Ann. N.Y. Acad. Sci. 595:399–402; 1990.
Berthois, Y.; Katzenellenbogen, J. A.; Katzenellenbogen, B. S. Phenol red in tissue culture media is a weak estrogen: implications concerning the study of estrogen-responsive cells in tissue culture. Proc. Natl. Acad. Sci. USA 83:2496–2500; 1986.
Blum, W. F.; Jenne, E. W.; Reppin, F., et al. Insulin-like growth factor I (IGF-I)-binding protein complex is a better mitogen than free IGF-I. Endocrinology 125:766–772; 1989.
Briand, P.; Lykkesfeldt, A. E. Long-term cultivation of a human breast cancer cell line, MCF-7, in a chemically defined medium. Effect of estradiol. Anticancer Res. 6:85–90; 1986.
Bronzert, D. A.; Bates, S. E.; Sheridan, J. A., et al. TGFβ induces PDGF mRNA and PDGF secretion while inhibiting growth in normal human mammary epithelial cells. Mol. Endocrinol. 4:981–989; 1990.
Butler, W. B.; Kelsey, W. H.; Goran, N., et al. Effects of serum and insulin on the sensitivity of the human breast cancer cell line MCF-7 to estrogen and antiestrogens. Cancer Res. 41:82–88; 1981.
Butler, W. B.; Kirkland, W. L.; Gargala, T. L., et al. Steroid stimulation of plasminogen activator production in a human breast cancer cell line (MCF-7). Cancer Res. 43:1637–1641; 1983.
Carruba, G.; Leake, R. E.; Rinaldi, F., et al. Steroid-growth factor interaction in human prostate cancer. 1. Short-term effects of transforming growth factors on growth of human prostate cancer cells. Steroids 59:412–420; 1994.
Carson-Jurica, M. A.; Schrader, W.; O'Malley, B. Steroid receptor family: structure and functions. Endocr. Rev. 11:201–220; 1990.
Castagnetta, L. A.; Carruba, G. Human prostate cancer: a direct role for oestrogens. Ciba Found. Symp. 191:269–286; 1995.
Chalbos, D.; Vignon, F.; Keydar, I., et al. Estrogens stimulate cell proliferation in a human breast cancer cell line (T47D). J. Clin. Endocrinol. Metab. 55:276–283; 1982.
Clark, D. A.; Coker, R. Transforming growth factor-beta (TGF-beta). Int. J. Biochem. Cell Biol. 30:293–298; 1998.
Clark, J. H.; Markaverich, B. M. The agonistic and antagonistic effects of short acting estrogens: a review. Pharm. Ther. 21:429–453; 1983.
Cullen, K. J.; Yee, D.; Sly, W. S., et al. Insulin-like growth factor receptor expression and function in human breast cancer. Cancer Res. 50:48–53; 1990.
Cunha, G. R.; Alarid, E. T.; Turner, T., et al. Normal and abnormal development of the male urogenital tract. Role of androgens, mesenchymal-epithelial interactions, and growth factors. J. Androl. 13:465–475; 1992.
Danielpour, D.; Riss, T. L.; Ogasawara, M., et al. Growth of MTW9/PL2 estrogen-responsive rat mammary tumor cells in hormonally defined serum-free media. In Vitro Cell. Dev. Biol. 24:42–52; 1988.
Danielpour, D.; Sirbasku, D. A. New perspectives in hormone dependent, responsive and autonomous mammary tumor growth: role of autostimulatory growth factors. In Vitro 20:975–980; 1984.
Darbre, P. D.; Curtis, S.; King, R. J. B. Effects of estradiol and tamoxifen on human breast cancer cells in serum-free culture. Cancer Res. 44: 2790–2793; 1984.
Darbre, P.; Yates, J.; Curtis, S., et al. Effect of estradiol on human breast cancer cells in culture. Cancer Res. 43:349–355; 1983.
de Jong, J. S.; van Diest, P. J.; van der Valk, P., et al. Expression of growth factors, growth-inhibiting factors, and their receptors in invasive breast cancer. I. An inventory in search of autocrine and paracrine loops. J. Pathol. 184:44–52; 1998a.
de Jong, J. S.; van Diest, P. J.; van der Valk, P., et al. Expression of growth factors, growth-inhibiting factors, and their receptors in invasive breast cancer. II. Correlations with proliferation and angiogenesis. J. Pathol. 184:53–57; 1998b.
de Launoit, Y.; Veilleux, R.; Dufour, M., et al. Characteristics of the biphasic action of androgens and the potent anti-proliferative effects of the new pure antiestrogen EM-139 on cell cycle kinetic parameters in LNCaP human prostatic cancer cells. Cancer Res. 51:5165–5170; 1991.
De Mellow, J. S. M.; Baxter, R. C. Growth hormone-dependent insulin-like growth factor (IGF) binding protein both inhibits and potentiates IGF-I-stimulated DNA synthesis in human skin fibroblasts. Biochem. Biophys. Res. Commun. 156:199–204; 1988.
Derynck, R. Transforming growth factor-α. Cell 54:593–595; 1988.
DiAugustine, R. P.; Petruez, P.; Bell, G. I., et al. Influences of estrogens on mouse uterine epidermal growth factor precursor protein messenger ribonucleic acid. Endocrinology 122:2355–2363; 1988.
Dickson, R. B.; Bates, S. E.; McManaway, M. E., et al. Characterization of estrogen responsive transforming activity in human breast cancer cell lines. Cancer Res. 46:1707–1713; 1986a.
Dickson, R. B.; Huff, K. K.; Spencer, E. M., et al. Induction of epidermal growth factor-related polypeptides by 17β-estradiol in MCF-7 human breast cancer cells. Endocrinology 118:138–142; 1985.
Dickson, R. B.; Lippman, M. E. Estrogenic regulation of growth and polypeptide growth factor secretion in human breast carcinoma. Endocr. Rev. 8:29–43; 1987.
Dickson, R. B.; McManaway, M. E.; Lippman, M. E. Estrogen-induced factors of breast cancer cells partially replace estrogen to promote tumor growth. Science (Wash DC) 232:1542–1543; 1986b.
Eby, J. E.; Sato, H.; Sirbasku, D. A. Preparation of iron-deficient tissue culture medium by deferoxamine-sepharose treatment and application to the differential actions of apotransferrin and diferric transferrin. Anal. Biochem. 203:317–325; 1992.
Eby, J. E.; Sato, H.; Sirbasku, D. A. Apotransferrin stimulation of thyroid hormone dependent rat pituitary tumor cell growth in serum-free chemically defined medium: role of Fe(III) chelation. J. Cell. Physiol. 156:588–600; 1993.
Edwards, D. P.; Adams, D. J.; Savage, N., et al. Estrogen induced synthesis of specific proteins in human breast cancer cells. Biochem. Biophys. Res. Commun. 93:804–812; 1980.
Elgin, R. G.; Busby, W. H., Jr.; Clemmons, D. R. An insulin-like growth factor (IGF) binding protein enhances the biologic response to IGF-I. Proc. Natl. Acad. Sci. USA 84:3254–3258; 1987.
Engle, L. W.; Young, N. A.; Tralka, T. S., et al. Establishment and characterization of three new continuous cell lines derived from human breast carcinomas. Cancer Res. 38:3352–3364; 1978.
Ethier, S. P. Growth factor synthesis and human breast cancer progression. J. Natl. Cancer Inst. 87:964–973; 1995.
Evans, R. M. The steroid and thyroid hormone receptor superfamily. Science (Wash DC) 240:889–895; 1988.
Furlanetto, R. W.; DiCarlo, J. N. Somatomedin-C receptors and growth effects in human breast cancer cells maintained in long-term tissue culture. Cancer Res. 44:2122–2128; 1984.
Gorski, J.; Hansen, J. C. The “one and only” step model of estrogen action. Steroids 49:461–475; 1987.
Gorski, J.; Toft, D. O.; Shymala, G., et al. Studies on the interaction of estrogen with the uterus. Recent Prog. Horm. Res. 24:45–80; 1968.
Gorski, J.; Welshons, W.; Sakai, D. Review: remodeling the estrogen receptor model. Mol. Cell. Endocrinol. 36:11–15; 1984.
Gospodarowicz, D.; Moran, J. S. Growth factors in mammalian cell culture. Annu. Rev. Biochem. 45:531–558; 1976.
Goustin, A. S.; Leof, E. B.; Shipley, G. D., et al. Growth factors and cancer. Cancer Res. 46:1015–1029; 1986.
Harris, J.; Gorski, J. Evidence for a discontinuous requirement for estrogen in stimulation of deoxyribonucleic acid synthesis in the immature rat uterus. Endocrinology 103:240–245; 1978.
Horoszewicz, J. S.; Leong, S. S.; Kawinski, E., et al. LNCaP model of human prostatic carcinoma. Cancer Res. 43:1809–1818; 1983.
Horwitz, K. B.; McGuire, W. L. Nuclear mechanisms of estrogen action. Effects of estradiol and antiestrogens on estrogen receptors and nuclear receptor processing. J. Biol. Chem. 253:8185–8191; 1978.
Huet-Hudson, Y. M.; Chakraborty, C.; De, S. K., et al. Estrogen regulates synthesis of epidermal growth factor in mouse uterine epithelial cells. Mol. Endocrinol. 4:510–523; 1990.
Huff, K. K.; Kaufman, D.; Gabbay, K. J., et al. Human breast cancer cells secrete an insulin-like growth factor-I related polypeptide. Cancer Res. 46:4613–4619; 1986.
Huff, K. K.; Knabbe, C.; Lindsey, R., et al. Multihormonal regulation of insulin-like growth factor-I-related protein in MCF-7 human breast cancer cells. Mol. Endocrinol. 2:200–208; 1988.
Huseby, R. A.; Maloney, T. M.; McGrath, C. M. Evidence for a direct growth-stimulating effect of estradiol on human MCF-7 cells in vivo. Cancer Res. 44:2654–2659; 1984.
Ikeda, T.; Liu, Q.-F.; Danielpour, D., et al. Identification of estrogen-inducible growth factors (estromedins) for rat and human mammary tumor cells in culture. In Vitro 18:961–979; 1982.
Iscove, N. N. Culture of lymphocytes and hematopoietic cells in serum-free medium. Methods for serum-free culture of neuronal and lymphoid cells. In: Barnes, D. W.; Sirbasku, D. A.; Sato, G. H., ed. Cell culture methods for molecular and cell biology. Vol. 4. New York: Liss/Wiley; 1984:169–185.
Jensen, E. V.; DeSombre, E. R. Estrogen-receptor interaction. Estrogenic hormones effect transformation of specific receptor proteins to a biochemically functional form. Science (Wash DC) 182:126–134; 1973.
Jensen, E. V.; Jacobson, H. I. Basic guides to the mechanism of estrogen action. Recent Prog. Horm. Res. 18:387–414; 1962.
Jensen, E. V.; Suzuki, T.; Kawashima, T., et al. A two-step mechanism for the interaction of estradiol with rat uterus. Proc. Natl. Acad. Sci. USA 59:632–638; 1968.
Jozan, S.; Moure, C.; Gillois, M., et al. Effects of estrone on cell proliferation of human breast cancer (MCF-7) in long term tissue culture. J. Steroid Biochem. 10:341–342; 1979.
Kano-Sueoka, T. Growth of rat mammary tumor cells in serum-free hormone-supplemented medium. Methods for serum-free culture of cells of the endocrine system. In: Barnes, D. W.; Sirbasku, D. A.; Sato, G.H., ed. Cell culture methods for molecular and cell biology. Vol. 2. New York: Liss/John Wiley; 1984:89–104.
Karey, K. P.; Sirbasku, D. A. Differential responsiveness of the human breast cancer cell lines MCF-7 and T47-D to growth factors and 17β-estradiol. Cancer Res. 48:4083–4092; 1988.
Katzenellenbogen, B. S. Dynamics of steroid hormone receptor action. Annu. Rev. Physiol. 42:17–35; 1980.
Katzenellenbogen, B. S. Biology and receptor interactions of estriol and estriol derivatives in vitro and in vivo. J. Steroid Biochem. 20:1033–1037; 1984.
Katzenellenbogen, B. S. Estrogen receptors: bioactivities and interactions with cell signaling pathways. Biol. Reprod. 54:287–293; 1996.
Katzenellenbogen, B. S.; Kendra, K. L.; Norman, M. J., et al. Proliferation, hormonal responsiveness, and estrogen receptor content of MCF-7 human breast cancer cells grown in the short-term and long-term absence of estrogens. Cancer Res. 47:4355–4360; 1987.
Kenney, N. J.; Saeki, T.; Gottardis, M., et al. Expression of transforming growth factor α antisense mRNA inhibits the estrogen-induced production of TGFα and estrogen-induced proliferation of estrogen-responsive human breast cancer cells. J. Cell. Physiol. 156:497–514; 1993.
Keydar, I.; Chen, L.; Karby, S., et al. Establishment and characterization of a cell line of human breast carcinoma origin. Eur. J. Cancer 15:659–670; 1979.
Kim, I. Y.; Kim, J.-H.; Zelner, D. J., et al. Transforming growth factor-β1 is a mediator of androgen-regulated growth arrest in an androgen-responsive prostatic cancer cell line, LNCaP. Endocrinology 137:991–999; 1996.
Kirkland, W. L.; Sorrentino, J. M.; Sirbasku, D. A. Control of cell growth. III. Demonstration of the direct mitogenic effect of thyroid hormones on an estrogen-dependent rat pituitary tumor cell line. J. Natl. Cancer Inst. 56:1159–1164; 1976.
Knabbe, C.; Lippman, M. E.; Wakefield, L. M., et al. Evidence that transforming growth factor-β is a hormonally regulated negative growth factor in human breast cancer cells. Cell 48:417–428; 1987.
Laursen, I.; Briand, P.; Lykkesfeldt, A. E. Serum albumin as a modulator on growth of the human breast cancer cell line, MCF-7. Anticancer Res. 10:343–352; 1990.
Lee, C.; Sutkowski, D. M.; Sensibar, J. A., et al. Regulation of proliferation and production of prostate specific antigen in androgen-sensitive prostatic cancer cells, LNCaP, by dihydrotestosterone. Endocrinology 136:796–803; 1995.
Leland, F. E.; Danielpour, D.; Sirbasku, D. A. Studies of the endocrine, paracrine, and autocrine control of mammary tumor cell growth. In: Sato, G. H.; Pardee, A. B.; Sirbasku, D. A., ed. Cold Spring Harbor Conferences on Cell Proliferation. Vol. 9. Growth of cells in hormonally defined media. New York: Cold Spring Harbor Press; 1982:741–750.
Leland, F. E.; Iio, M.; Sirbasku, D. A. Hormone-dependent cell lines. In: Sato, G. H., ed. Functional differentiated cell lines. New York: Liss/Wiley; 1981:1–46.
Lippman, M. E.; Bolan, G.; Huff, K. The effects of estrogens and antiestrogens on hormone-responsive human breast cancer in long-term tissue culture. Cancer Res. 36:4595–4601; 1976.
Lippman, M. E.; Dickson, R. B.; Kasid, A., et al. Autocrine and paracrine growth regulation of human breast cancer. J. Steroid Biochem. 24: 147–154; 1986.
Lippman, M. E.; Manaco, M. E.; Bolan, G. Effects of estrone, estradiol, and estriol on hormone responsive human breast cancer in long term tissue culture. Cancer Res. 37:1901–1907; 1977.
Liu, S. C.; Sanfilippo, B.; Perroteau, I., et al. Expression of transforming growth factor α (TGFα) in differentiated rat mammary tumors: estrogen induction of TGFα production. Mol. Endocrinol. 1:683–692; 1987.
Lykkesfeldt, A. E.; Briand, P. Indirect mechanism of oestradiol stimulation of cell proliferation of human breast cancer cell lines. Br. J. Cancer 53:29–35; 1986.
MacIndoe, J. H.; Woods, G. R.; Etre, L. A. The specific binding of estradiol and estrone and the subsequent distribution of estrogen-receptor complexes within MCF-7 human breast cancer cells. Steroids 39:245–258; 1982.
Markaverich, B. M.; Clark, J. H. Two binding sites for estradiol in rat uterine nuclei: relationship to uterotropic response. Endocrinology 105:1458–1462; 1979.
Massagué, J. TGF-beta signal transduction. Annu. Rev. Biochem. 67:753–791; 1998.
Minuto, E.; Del Monte, P.; Barreca, A., et al. Partial characterization of somatomedin C-like immunoreactivity secreted by breast cancer cells in vitro. Mol. Cell. Endocrinol. 54:179–184; 1987.
Moreno-Cuevas, J. E.; Sirbasku, D. A. Estrogen mitogenic action. I. Demosonstration of estrogen-dependent MTW9/PL2 carcinogen-induced rat mammary tumor cell growth in serum supplemented culture and technical implications. In Vitro Cell. Dev. Biol. 36(7):410–427; 2000a.
Moreno-Cuevas, J. E.; Sirbasku, D. A. Estrogen mitogenic action. III. Is phenol red a “red herring”? In Vitro Cell. Dev. Biol. 36(7):447–464; 2000b.
Morisset, M.; Capony, F.; Rochefort, H. The 52-kDa estrogen-induced protein secreted by MCF-7 cells is a lysosomal acidic protease. Biochem. Biophys. Res. Commun. 138:102–109; 1986.
Murphy, L. J.; Ghahary, A. Uterine insulin-like growth factor-1: Regulation of expression and its role in estrogen-induced uterine proliferation. Endocr. Rev. 11:443–453; 1990.
Murphy, L. J.; Murphy, L. C.; Friesen, H. G. A role for the insulin-like growth factors as estromedins in the rat uterus. Trans. Assoc. Am. Phys. 100: 204–214; 1987.
Myal, Y.; Shiu, R. P. C.; Bhaumick, B., et al. Receptor bindingd and growth-promoting activity of insulin-like growth factors in human breast cancer cells (T-47D) in culture. Cancer Res. 44:5486–5490; 1984.
Natoli, C.; Sica, G.; Natoli, V., et al. Two new estrogen-suppressitive variants of the MCF-7 human breast cancer cell line. Breast Cancer Res. Treat. 3:23–32; 1983.
Normanno, N.; Ciardiello, F.; Brandt, R., et al. Epidermal growth factor-related peptides in the pathogenesis of human breast cancer. Breast Cancer Res. Treat. 29:11–27; 1994.
Ogasawara, M.; Sirbasku, D. A. A new serum-free method of measuring growth factor activities for human breast cancer cells in culture. In Vitro Cell. Dev. Biol. 24:911–920; 1988.
O'Malley, B. W. The steroid receptor superfamily: more excitement predicted for the future. Mol. Endocrinol. 4:363–369; 1990.
O'Malley, B. W.; Means, A. R. Female steroid hormones and target cell nuclei. Science (Wash DC) 183:610–620; 1974.
Osborne, C. K.; Coronado, E. B.; Kitten, L. J., et al. Insulin-like growth factor-II (IGF-II): a potential autocrine/paracrine growth factor for human breast cancer acting via the IGF-I receptor. Mol. Endocrinol. 3:1701–1709; 1989.
Page, M. J.; Field, K. J.; Everett, N. P., et al. Serum regulation of the estrogen responsiveness of the human breast cancer cell line MCF-7. Cancer Res. 43:1244–1250; 1983.
Peehl, D. M.; Rubin, J. S. Keratinocyte growth factor: an androgen-regulated mediator of stromal-epithelial interactions in the prostate. World J. Urol. 13:312–317; 1995.
Peehl, D. M.; Wong, S. T.; Rubin, J. S. KGF and EGF differentially regulate the phenotype of prostatic epithelial cells. Growth Regul. 6:22–31; 1996.
Ramsdell, J. S. Transforming growth factor-alpha and-beta are potent and effective inhibitors of GH4 pituitary tumor cell proliferation. Endocrinology 128:1981–1990; 1991.
Rechler, M.; Zapf, J.; Nissley, S. P., et al. Interactions of insulin-like growth factors I and II and multiplication-stimulating activity with receptors and serum carrier proteins. Endocrinology 107:1451–1459; 1980.
Reddy, K. B.; Yee, D.; Hilsenbeck, S. G., et al. Inhibition of estrogen-induced breast cancer cell proliferation by reduction in autocrine transforming growth factor alpha expression. Cell Growth Differ. 5:1275–1282; 1994.
Reese, C. C.; Warshaw, M. L.; Murai, J. T., et al. Alternative models for estrogen and androgen regulation of human breast cancer cell (T47D) growth. Ann. N.Y. Acad. Sci. 538:112–121; 1988.
Renoir, J.-M.; Mercier-Bodard, C.; Baulieu, E.-E. Hormonal and immunological aspects of the phylogeny of sex steroid binding plasma protein. Proc. Natl. Acad. Sci. USA 77:4578–4582; 1980.
Reny, J.-C.; Soto, A. M. Human serum does not contain a high affinity estrogen-binding glycoprotein different from sex hormone-binding globulin. J. Clin. Endocrinol. Metab. 68:938–945; 1989.
Riss, T. L.; Sirbasku, D. A. Rat pituitary tumor cells in serum-free culture. II. Serum factor and thyroid hormone requirements for estrogen-responsive growth. In Vitro Cell. Dev. Biol. 25:136–142; 1989.
Rochefort, H.; Capony, F.; Garcia, M., et al. Estrogen-induced lysosomal proteases secreted by breast cancer cells: a role in carcinogenesis? J. Cell Biochem. 35:17–29; 1987.
Ruedl, C.; Cappelletti, V.; Coradini, D., et al. Influence of culture conditions on the estrogenic cell growth stimulation of human breast cancer cells. J. Steroid Biochem. Mol. Biol. 37:195–200; 1990.
Salomon, D. S.; Zwiebel, J. A.; Bano, M., et al. Presence of transforming growth factors in human breast cancer cells. Cancer Res. 44:4069–4077; 1984.
Sato, H.; Eby, J. E.; Sirbasku, D. A. Iron is deleterious to hormone-responsive pituitary cell growth in serum-free defined medium. In Vitro Cell. Dev. Biol. 27A:599–602; 1991.
Schatz, R. W.; Soto, A. M.; Sonnenschein, C. Effects of interaction, between estradiol-17β and progesterone on proliferation of cloned breast tumor cells (MCF-7 and T47D). J. Cell. Physiol. 124:386–390; 1985.
Schubert, J. The chemical basis of chelation. In: Gross, F., ed. Iron metabolism. Berlin: Springer; 1964:466–498.
Schuurmans, A. L. G.; Bolt, J.; Mulder, E. Androgens stimulate both the growth rate and epidermal growth factor receptor activity of the human prostate tumor cell line LNCaP. The Prostate 12:55–64; 1988.
Seibert, K.; Shafie, S. M.; Triche, T. J., et al. Clonal variation of MCF-7 breast cancer cells in vitro and in athymic nude mice. Cancer Res. 43:2223–2239; 1983.
Shafie, S. M. Estrogen and growth of breast cancer. New evidence suggests indirect action. Science (Wash DC) 209:701–702; 1980.
Silberstein, G. B.; Daniel, C. W. Reversible inhibition of mammary gland growth by transforming growth factor-β. Science (Wash DC) 237:291–293; 1987.
Silberstein, G. B.; Flanders, K. C.; Roberts, A. B., et al. Regulation of mammary morphogenesis: evidence for extracellular matrix-mediated inhibition of ductal budding by transforming growth factor-β1. Dev. Biol. 152:354–362; 1992.
Sirbasku, D. A. Estrogen-induction of growth factors specific for hormone-responsive mammary, pituitary, and kidney tumor cells. Proc. Natl Acad. Sci. USA 75:3786–3790; 1978.
Sirbasku, D. A. New concepts in control of estrogen-responsive tumor growth. Banbury Rep. 8:425–443; 1981.
Sirbasku, D. A.; Benson, R. H. Estrogen-inducible growth factors that may act as mediators (estromedins) of estrogen promoted tumor cell growth. In: Sato, G. H., Ross, R., ed. Hormones and cell culture. Cold Spring Harbor Conferences on Cell Proliferation. Vol. 6. New York: Cold Spring Harbor Laboratory; 1979:477–497.
Sirbasku, D. A.; Kirkland, W. L. Control of cell growth. IV. Growth properties of a new cell line established from an estrogen-dependent tumor of the Syrian hamster. Endocrinology 98:1260–1272; 1976.
Sirbasku, D. A.; Leland, F. E. Proposal of new mechanisms of estrogen-promoted tumor cell growth. In: Litwack, G., ed. Biochemical actions of hormones. Vol. 9. New York: Academic Press; 1982:115–140.
Sirbasku, D. A.; Moreno-Cuevas, J. E.; Walterscheid, J. P. Serum factor regulation of estrogen responsive mammary tumor cell growth [abstract]. Proceedings of the 1997 Meeting of the “Department of Defense Breast Cancer Research Program: An Era of Hope”, pp. 739–740. Washington, D. C., 31 October through 4 November 1997.
Sonnenschein, C.; Olea, N.; Pasanen, M. E., et al. Negative controls of cell proliferation: human prostate cancer cells and androgens. Cancer Res. 49:3474–3481; 1989.
Sonnenschein, C.; Soto, A. M. But … are estrogens per se growth promoting hormones? J. Natl. Cancer Inst. 64:211–215; 1980.
Sonnenschein, C.; Soto, A. M.; Michaelson, C. L. Human serum albumin shares the properties of estrocolyone-I, the inhibitor of the proliferation of estrogen-target cells. J. Steroid Biochem. Mol. Biol. 59:147–154; 1996.
Sorrentino, J. M.; Kirkland, W. L.; Sirbasku, D. A. Control of cell growth. I. Estrogen-dependent growth in vivo of a rat pituitary tumor cell line. J. Natl. Cancer Inst. 56:1149–1154; 1976.
Soto, A. M.; Bass, J. C.; Sonnenschein, C. Proliferative behavior of the cloned Syrian hamster tumor cells H301. Cancer Res. 48:3676–3680; 1988.
Soto, A. M.; Murai, J. T.; Siiteri, P. K., et al. Control of cell proliferation: evidence for negative control on estrogen-sensitive T47D human breast cancer cells. Cancer Res. 46:2271–2275; 1986.
Soto, A. M.; Silvia, R. M.; Sonnenschein, C. A plasma-borne inhibitor of the proliferation of human estrogen-sensitive breast tumor cells (estrocolyone-1). J. Steroid Biochem. Mol. Biol. 43:703–712; 1992.
Soto, A. M.; Sonnenschein, C. Mechanism of estrogen action on cellular proliferation: evidence for indirect and negative control on cloned breast tumor cells. Biochem. Biophys. Res. Commun. 122:1097–1103; 1984.
Soto, A. M.; Sonnenschein, C. The role of estrogens on proliferation of human breast tumor cells (MCF-7). J. Steroid Biochem. 23:87–94; 1985.
Soto, A. M.; Sonnenschein, C. Cell proliferation of estrogen-sensitive cells: the case for negative regulation. Endocr. Rev. 8:44–52; 1987.
Soule, H. D.; Vazquez, J.; Long, A., et al. A human cell line from a pleural effusion from a breast carcinoma. J. Natl. Cancer Inst. 51:1409–1416; 1973.
Spiro, T. G.; Allerton, S. E.; Renner, J., et al. The hydrolytic polymerization of iron (III). J. Am. Chem. Soc. 88:2721–2726; 1966.
Sporn, M. B.; Todaro, G. J. Autocrine secretion and malignant transformation of cells. N. Engl. J. Med. 303:878–880; 1980.
Stack, G.; Gorski, J. Direct mitogenic effect of estrogen on the prepuberal rat uterus: studies on isolated nuclei. Endocrinology 115:1141–1150; 1984.
Stewart, A. J.; Johnson, M. D.; May, F. E., et al. Role of insulin-like growth factors and the type I insulin-like growth factor receptor in the estrogen-stimulated proliferation of human breast cancer cells. J. Biol. Chem. 265:21,172–21,178; 1990.
Tashjian, A. H. Jr. Clonal strains of hormone-producing pituitary cells. Methods Enzymol. 58:527–535; 1979.
Tashjian, A. H., Jr.; Bancroft, F. C.; Levine, L. Production of both prolactin and growth hormone by clonal strains of rat pituitary tumor cells: differential effects of hydrocortisome and tissue extracts. J. Cell. Biol. 47:61–70; 1970.
Tashjian, A. H., Jr.; Yasumura, Y.; Levine, L., et al., Establishment of clonal strains of rat pituitary tumor cells that secrete growth hormone. Endocrinology 82:342–352; 1968.
Truss, M.; Beato, M. Steroid hormone receptors: interaction with deoxyribonucleic acid and transcription factors. Endocr. Rev. 14:459–479; 1993.
Tsai, M. J.; O'Malley, B. W. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 63:451–486; 1994.
van der Burg, B.; Rutteman, G. R.; Blankenstein, M. A., et al. Mitogenic stimulation of human breast cancer cells in a growth factor-defined medium: synergistic action of insulin and estrogen. J. Cell. Physiol. 134:101–108; 1988.
Veldscholte, J.; Ris-Stalpers, C.; Kuiper, G. G. A mutation in the ligand binding domain of the androgen receptor of human LNCaP cells affects steroid binding characteristics and responses to anti-androgens. Biochem. Biophys. Res. Commun. 173:534–540; 1990a.
Veldscholte, J.; Voorhorst-Ogink, M. M.; Bolt-de Vries, J., et al. Unusual specificity of the androgen receptor in the human prostate tumor cell line LNCaP: high affinity for progrestagenic and estrogenic steroids. Biochim. Biophys. Acta 1052:187–194; 1990b.
Vignon, F.; Capony, F.; Chambon, M., et al. Autocrine growth stimulation of the MCF-7 breast cancer cells by the estrogen-regulated 52K protein. Endocrinology 118:1537–1545; 1986.
Wiese, T. E.; Kral, L. G.; Dennis, K. E., et al. Optimization of estrogen growth response in MCF-7 cells. In Vitro Cell. Dev. Biol. 28A:595–602; 1992.
Wilding, G.; Zugmeier, G.; Knabbe, C., et al. Differential effects of transforming growth factor beta on human prostate cancer cells in vitro. Mol. Cell. Endocrinol. 62:79–87; 1989.
Yamamoto, K. R. Steroid receptor-regulated transcription of specific genes and gene networks. Annu. Rev. Genet. 19:209–252; 1985.
Yasumura, Y.; Tashjian, A. H., Jr.; Sato, G. Establishment of four functional clonal strains of animal cells in culture. Science (Wash DC) 154: 1186–1189; 1966.
Yee, D.; Cullen, K. J.; Paik, S., et al. Insulin-like growth factor II mRNA expression in human breast cancer. Cancer Res. 48:6691–6696; 1988.
Yee, D.; Favoni, R. E.; Lippman, M. E., et al. Identification of insulin-like growth factor binding proteins in breast cancer cells. Breast Cancer Res. Treat. 18:3–10; 1991.
Zapf, J.; Schoenle, E.; Jagars, G., et al. Inhibition of the action of nonsupressible insulin-like activity on isolated rat fat cells by binding to its carrier protein. J. Clin. Invest. 63:1077–1084; 1978.
Zava, D. T.; McGuire, W. L. Human breast cancer: androgen action mediated by estrogen receptor. Science (Wash DC) 199:787–788; 1978.
Zugmaier, G.; Ennis, B. W.; Deschauer, B., et al. Transforming growth factors type β1 and β2 are equipotent growth inhibitors of human breast cancer cell lines. J. Cell Physiol. 141:353–361; 1989.
Zugmaier, G.; Knabbe, C.; Fritsch, C., et al. Tissue culture conditions determine the effects of estrogen and growth factors on the anchorage independent growth of human breast cancer cell lines. J. Steroid Biochem. Mol. Biol. 39:681–685; 1991.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sirbasku, D.A., Moreno-Cuevas, J.E. Estrogen mitogenic action. II. Negative regulation of the steroid hormone-responsive growth of cell lines derived from human and rodent target tissue tumors and conceptual implications. In Vitro Cell.Dev.Biol.-Animal 36, 428–446 (2000). https://doi.org/10.1290/1071-2690(2000)036<0428:EMAINR>2.0.CO;2
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1290/1071-2690(2000)036<0428:EMAINR>2.0.CO;2