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Role Of Estrogens And Their Receptors In Adhesion And Invasiveness Of Breast Cancer Cells

Our data demonstrated that estradiol and ERa expression inhibit cancer cell invasiveness in breast cancer cells through different mechanisms. Inhibition by estrogens is dependent to transcriptional activation of specific sasaran genes that are probably involved in an increase of cell-cell adhesion. The unliganded inhibits ERa invasion via protein-protein interactions within the first zinc finger region of the receptor. These data could explain the protective role of ERa against tumor invasion and metastasis previously found in these cell lines. ERa expression has been associated with a low invasiveness and low motility in culture tests (24, 25). Moreover, when ERa-positive cells were implanted in nude mice, tumors appeared only in the presence of estrogens and are poorly metastatic as compared to those developed from ERa-negative breast cancer cell lines (20).
Clinical data supporting that estrogens prevent invasion. There is a great deal of evidence to support the hypothesis that estrogens are important because they are potent mitogens for normal breast epithelial cells, and it is believed that the duration of breast epithelium exposure to estrogens is a significant risk factor for breast cancer development. However, in mammary carcinogenesis, even though the mitogenic effect of estrogens is well demonstrated, the presence of ERa is associated with more differentiated and less invasive tumors and a more favorable prognosis. Moreover, there is some clinical evidences indicating that estrogens and their receptors protect against invasion. Epidemiological studies have evaluated the breast cancer risk in women using hormone replacement therapy (HRT) where 80% were taking preparations containing estrogen alone (26, 27). Among the women using HRT, the risk of breast cancer slightly increased, but the tumors under estradiol treatment were confined to localized disease with more favorable prognosis. Tumors in HRT-users were less invasive to axillary lymph nodes and to more distant sites. Other studies of tamoxifen therapy of primary breast cancer suggest that tamoxifen increased the spreading of ERa-positive primary tumor cells to contralateral sites. Tamoxifen use decreased (0.8 fold) the risk of ERa-positive tumors, but it appeared to increase (4.9-fold) the risk of ERa-negative contralateral tumors (28). All together, these clinical data are in agreement with an anti-invasive effect of estrogens.
Role of estrogen receptor variants in cancer progression? Numerous studies have identified ERa and ERa variants from differential splicing of their mRNAs in both neoplastic breast tissue and cell lines (29, 30). These mRNA variants lack one or several exons and are usually coexpressed with the wild-type ER message. However, their pathophysiological significance is unclear. Several studies using transient transfection have shown that individual ERa variant proteins can have positive or negative effects on the wild-type ERa activity (29, 30). The presence of one or more variant proteins in variable levels in normal breast epithelium and neoplastic tissue could infuence the wild-type receptor  (31). The variants ERa D3 (lacking the second zinc finger) and ERa D4 (deleted in the hormone-binding domain) are overexpressed in normal cells rather than in breast cancer cells. These variants, which contain the first zinc finger domain, could have an invasion-suppression activity independent of the hormone action. This was verified by expression of the ERa D3 variant (31). A more detailed clinical evaluation of the ER variants is required to determine their influence in mammary carcinogenesis and the response to therapy.
Missense mutants of the ERα gene with point mutation have been found in only 1 % of primary breast tumors (32). Even the functionality of only few mutations has been studied; initial data indicate that these mutations could affect normal ERa function and alter the evolution of individual tumors.  This suggests that these somatic mutations, although infrequent, may significantly alter the evolution of individual tumors.
In conclusion, we present evidences that estrogens inhibit invasiveness of breast cancer cells via a classical activation of ERE-regulated genes leading to an increase in cell-cell adhesion. In the absence of ligand, the receptor could also prevent invasion through interaction with an unknown protein. Non-classical mechanisms of action, in which the receptor may bind to other transcription factors instead of DNA or to the proteins involved in pathways such as motility and invasion, requires further investigation. The identification of the factors that inhibit the invasiveness of ERa positive cells would be a useful step in the development of new therapeutic targets to cure the most aggressive ERa -negative tumors.

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