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Dissociation between Steroid Receptor Expression and Cell Proliferation in the Human Breast¹

Tumor Biochemistry Laboratory, Clinical Research Department [R. B. C., E. A.], Department of Epithelial Biology, Paterson Institute for Cancer Research [C. S. P.], and Cancer Research Campaign Department of Medical Oncology [A. H.], (University of Manchester) Christie Hospital (National Health Service) Trust, Manchester M20 4BX, United Kingdom

We have shown previously that estradiol stimulates cell proliferation and progesterone receptor (PgR) synthesis in luminal epithelial cells of the normal human breast. Approximately 10–15% of luminal epithelial cells within the normal breast express immunodetectable estrogen receptor (ER), but little is known about their distribution within lobules and their organization in relation to the smaller population of proliferating cells. Using normal human breast tissue, we show that ER-positive cells are distributed evenly throughout the mammary epithelium. Using double antibody immunofluorescence, we show that 96% of steroid receptor-positive cells synthesize both ER and PgR (n = 25). Double labeling with antibodies to either ER or PgR coupled with either [³H]thymidine histoautoradiography or with antibodies to the Ki67 proliferation antigen indicates that dividing cells are separate from those expressing the receptors (although they are often in close proximity). However, in contrast to the normal human breast, two-thirds of ER-positive human mammary tumors examined (n = 19) have a high proportion of dividing cells that are ER positive. These data are consistent with the hypothesis that cells in normal human breast epithelium are hierarchical in organization and support a model in which proliferation of ER-negative cells is controlled by paracrine factors released from ER-positive cells under the influence of estradiol. This organization may be disrupted in some tumors.

¹ R. B. C. and E. A. are supported by the Christie Hospital (National Health Service) Trust Research Endowment Fund. A. H. and C. S. P. are supported by the Cancer Research Campaign.

² To whom requests for reprints should be addressed, at Tumor Biochemistry Laboratory, Clinical Research Department, Christie Hospital-Paterson Institute, Wilmslow Road, Withington, Manchester M20 4BX, United Kingdom. Phone: 0161-446-3210; Fax: 0161-446-3218; E-mail: clrrbc@picr.cr.man.ac.uk.

Received 8/18/97. Accepted 10/ 3/97.

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				J. G. Liehr Is Estradiol a Genotoxic Mutagenic Carcinogen? Endocr. Rev., February 1, 2000; 21(1): 40 - 54. [Abstract] [Full Text]

				A. Brinkman, S. van der Flier, E. M. Kok, and L. C. J. Dorssers BCAR1, a Human Homologue of the Adapter Protein p130Cas, and Antiestrogen Resistance in Breast Cancer Cells J Natl Cancer Inst, January 19, 2000; 92(2): 112 - 120. [Abstract] [Full Text] [PDF]

				S. Saji, E. V. Jensen, S. Nilsson, T. Rylander, M. Warner, and J.-A. Gustafsson Estrogen receptors alpha and beta in the rodent mammary gland PNAS, January 4, 2000; 97(1): 337 - 342. [Abstract] [Full Text] [PDF]

				B. S. Shoker, C. Jarvis, R. B. Clarke, E. Anderson, J. Hewlett, M. P. A. Davies, D. R. Sibson, and J. P. Sloane Estrogen Receptor-Positive Proliferating Cells in the Normal and Precancerous Breast Am. J. Pathol., December 1, 1999; 155(6): 1811 - 1815. [Abstract] [Full Text] [PDF]

				A. Balsari, P. Casalini, E. Tagliabue, M. Greco, S. Pilotti, R. Agresti, R. Giovanazzi, L. Alasio, C. Rumio, N. Cascinelli, et al. Fluctuation of HER2 Expression in Breast Carcinomas during the Menstrual Cycle Am. J. Pathol., November 1, 1999; 155(5): 1543 - 1547. [Abstract] [Full Text] [PDF]

				M. D. Planas-Silva, J. L. Donaher, and R. A. Weinberg Functional Activity of Ectopically Expressed Estrogen Receptor Is Not Sufficient for Estrogen-mediated Cyclin D1 Expression Cancer Res., October 1, 1999; 59(19): 4788 - 4792. [Abstract] [Full Text] [PDF]

				A. M. Raafat, L. J. Hofseth, S. Li, J. M. Bennett, and S. Z. Haslam A Mouse Model to Study the Effects of Hormone Replacement Therapy on Normal Mammary Gland during Menopause: Enhanced Proliferative Response to Estrogen in Late Postmenopausal Mice Endocrinology, June 1, 1999; 140(6): 2570 - 2580. [Abstract] [Full Text]

				W.-S. Shim, J. DiRenzo, J. A. DeCaprio, R. J. Santen, M. Brown, and M.-H. Jeng Segregation of steroid receptor coactivator-1 from steroid receptors in mammary epithelium PNAS, January 5, 1999; 96(1): 208 - 213. [Abstract] [Full Text] [PDF]

				H.-L. C. Liu, E. Golder-Novoselsky, M. H. Seto, L. Webster, J. McClary, and D. A. Zajchowski The Novel Estrogen-Responsive B Box Protein (EBBP) Gene Is Tamoxifen Regulated in Cells Expressing an Estrogen Receptor DNA-Binding Domain Mutant Mol. Endocrinol., November 1, 1998; 12(11): 1733 - 1748. [Abstract] [Full Text]

				E. V. Jensen, G. Cheng, C. Palmieri, S. Saji, S. Makela, S. Van Noorden, T. Wahlstrom, M. Warner, R. C. Coombes, and J.-A. Gustafsson Estrogen receptors and proliferation markers in primary and recurrent breast cancer PNAS, December 18, 2001; 98(26): 15197 - 15202. [Abstract] [Full Text] [PDF]