Cited by 693Estrogen and related hormone effectsCancer Cells and MetastasisBreast Cancer Treatment Studies

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Control of mammary stem cell function by steroid hormone signalling

Asselin-Labat, Marie-Liesse, Vaillant, François, Sheridan, Julie M., Pal, Bhupinder, Wu, Di, Simpson, Evan R., Yasuda, Hisataka, Smyth, Gordon K., Martin, T. John, Lindeman, Geoffrey J., Visvader, Jane E.·2010·Nature

DOI 10.1038/nature09027

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Abstract

The ovarian hormones oestrogen and progesterone profoundly influence breast cancer risk, underpinning the benefit of endocrine therapies in the treatment of breast cancer. Modulation of their effects through ovarian ablation or chemoprevention strategies also significantly decreases breast cancer incidence. Conversely, there is an increased risk of breast cancer associated with pregnancy in the short term. The cellular mechanisms underlying these observations, however, are poorly defined. Here we demonstrate that mouse mammary stem cells (MaSCs) are highly responsive to steroid hormone signalling, despite lacking the oestrogen and progesterone receptors. Ovariectomy markedly diminished MaSC number and outgrowth potential in vivo, whereas MaSC activity increased in mice treated with oestrogen plus progesterone. Notably, even three weeks of treatment with the aromatase inhibitor letrozole was sufficient to reduce the MaSC pool. In contrast, pregnancy led to a transient 11-fold increase in MaSC numbers, probably mediated through paracrine signalling from RANK ligand. The augmented MaSC pool indicates a cellular basis for the short-term increase in breast cancer incidence that accompanies pregnancy. These findings further indicate that breast cancer chemoprevention may be achieved, in part, through suppression of MaSC function.

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Items 301–400 of 691

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Background
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Background
Impact of body mass index on breast cancer in accordance with the life-stage of women
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Background
Progesterone from ovulatory menstrual cycles is an important cause of breast cancer
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Background
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Background
Cell sex affects extracellular matrix protein expression and proliferation of smooth muscle progenitor cells derived from human pluripotent stem cells
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“Stem cell differentiation in sexually dimorphic mammalian organs (such as sexual glands) is regulated by sex hormone [38, 46].”
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“Similar evidence indicates a role for steroids such as E2 and progesterone in the control of normalmammary stem cell function (16, 17) and implicates stem cells as key targets during hormonal carcinogenesis.”
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MTSS1 suppresses mammary tumor-initiating cells by enhancing RBCK1-mediated p65 ubiquitination
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The network of pluripotency, epithelial–mesenchymal transition, and prognosis of breast cancer
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“Activation of RANKL signalling induced by progesterone results in the expansion of mammary progenitor cells and increases the survival of tumour cells growing in suspension [ 32 , 34, 43].”
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Paracrine signaling by progesterone
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“Likewise, treatment of virgin or pregnant mice with anti-RANKL monoclonal antibody and subsequent in vitro assays showed impairment in clonogenicity of MaSCs enriched CD29 cells compared to their untreated counterpart (Asselin-Labat et al., 2010) (Fig.”
BackgroundInfluential
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Background
Cell Fate Decisions During Breast Cancer Development
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Background
Alteration of Mammary Gland Development and Gene Expression by In Utero Exposure to Cadmium
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Background
Oxytocin receptor induces mammary tumorigenesis through prolactin/p-STAT5 pathway
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“The extensive and complex mechanisms of estrogen signaling are known to have a multitude of effects on breast cell growth and function [57-60].”
Background
A TGFβ–miR-182–BRCA1 axis controls the mammary differentiation hierarchy
Martinez‐Ruiz, H., Illa-Bochaca, I., Omene, C. O., Hanniford, D., Liu, Q., Hernando, E., & Barcellos‐Hoff, M. H. (2016) · Science Signaling · doi:10.1126/scisignal.aaf5402 · Cited by 28
“epithelial cells restrict the expansion of MaSC (45) may also be reinforced by TGFβ because TGFβ activation in estrogen receptor-positive luminal epithelial cells at estrus inhibits their proliferation and thus, the proportion of estrogen-receptor cells (3, 4).”
Background
Hormones induce the formation of luminal-derived basal cells in the mammary gland
Song, W., Wang, R., Jiang, W., Yin, Q., Peng, G., Yang, R., Yu, Q. C., Chen, J., Li, J., Cheung, T. H., et al. (2019) · Cell Research · doi:10.1038/s41422-018-0137-0 · Cited by 28
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“As reported previously (Asselin-Labat et al., 2010; Joshi et al., 2010), mammary epithelial structures in WT females were strongly responsive to these hormones (Figures 2Bi–iv and S1).”
BackgroundInfluential
The Role of the RANKL/RANK Axis in the Prevention and Treatment of Breast Cancer with Immune Checkpoint Inhibitors and Anti-RANKL
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Hormone Replacement Therapy and Breast Cancer
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c-Jun N-terminal Kinase 2 Regulates Multiple Receptor Tyrosine Kinase Pathways in Mouse Mammary Tumor Growth and Metastasis
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“Two groups recently reported that progesterone and estrogen induce hormonesensitive luminal cells to secrete RANKL, which activates RANK, expressed on MaSCs, to increase proliferation of MaSC populations during puberty, diestrus, and pregnancy.(47,48) Thus, it is not unexpected that tumor cells may usurp these signali…”
Background
SCA-1 Labels a Subset of Estrogen-Responsive Bipotential Repopulating Cells within the CD24 + CD49f hi Mammary Stem Cell-Enriched Compartment
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“It is now accepted that MaSC hormone sensitivity is mediated indirectly by the RANK/ RANKL axis (Asselin-Labat et al., 2010; Joshi et al., 2010; Tanos et al., 2013).”
Influential
Repressor of Estrogen Receptor Activity (REA) Is Essential for Mammary Gland Morphogenesis and Functional Activities: Studies in Conditional Knockout Mice
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Minireview: Prolactin Regulation of Adult Stem Cells
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“Pregnancy modulates mammary stem cell number and function, but the long-term implications of these changes are unclear (33).”
Background
Somatic loss of estrogen receptor beta and p53 synergize to induce breast tumorigenesis
Bado, I. L., Nikolos, F., Rajapaksa, G. K., Wu, W., Castañeda, J., Krishnamurthy, S., Webb, P., Gustafsson, J.-Α., & Thomas, C. G. (2017) · Breast Cancer Research · doi:10.1186/s13058-017-0872-z · Cited by 25
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Background
Translational opportunities for broad‐spectrum natural phytochemicals and targeted agent combinations in breast cancer
Nagaprashantha, L. D., Adhikari, R., Singhal, J., Chikara, S., Awasthi, S., Horne, D. A., & Singhal, S. S. (2017) · International Journal of Cancer · doi:10.1002/ijc.31085 · Cited by 26
“E2 treatment enhances the proportion of mammary stem cells and aromatase knockout mice have significantly decreased number of mammary stem cells.(30) The genetic defects in BRCA1 and loss of tumor suppressors PTEN also facilitate an unhindered estrogen induced proliferative signaling by PI3K/AKT pathway due to dysfunc…”
Background
Thyroid Hormone Receptor β Inhibits Self-Renewal Capacity of Breast Cancer Stem Cells
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“Although ERa levels are low in CSCs (10,11), estrogen induces paracrine fibroblast growth factor 9 (FGF9)/ fibroblast growth factor receptor (FGFR) signaling in the non-CSC compartment that ultimately increases the CSC population (10,12).”
Expression of receptor activator of NFkB (RANK) drives stemness and resistance to therapy in ER+HER2- breast cancer
Gomes, I., de Almeida, B. P., Dâmaso, S., Mansinho, A., Correia, I. A., Henriques, S. C., Cruz-Duarte, R., Vilhais, G., Félix, P., Alves, P., et al. (2020) · Oncotarget · doi:10.18632/oncotarget.27576 · Cited by 25
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Modifications to glucocorticoid and progesterone receptors alter cell fate in breast cancer
Leehy, K. A., Anderson, T. M. R., Daniel, A. R., Lange, C. A., & Ostrander, J. H. (2016) · Journal of Molecular Endocrinology · doi:10.1530/jme-15-0322 · Cited by 25
Recurrence and metastasis of breast cancer is influenced by ovarian hormone’s effect on breast cancer stem cells
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Background

Authors: Asselin-Labat, M.-L., Vaillant, F., Sheridan, J. M., Pal, B., Wu, D., Simpson, E. R., Yasuda, H., Smyth, G. K., Martin, T. J., Lindeman, G. J., & Visvader, J. E.
Affiliations: Walter and Eliza Hall Institute of Medical Research (AU)
The University of Melbourne (AU)
Monash Medical Centre (AU)
Oriental Yeast Co., Ltd. (Japan) (JP)
St Vincents Institute of Medical Research (AU)
The Royal Melbourne Hospital (AU)
Corresponding author: Lindeman, Geoffrey J.
Visvader, Jane E.
ORCID: Asselin-Labat, Marie-Liesse
Vaillant, François
Sheridan, Julie M.
Pal, Bhupinder
Wu, Di
Simpson, Evan R.
Yasuda, Hisataka
Smyth, Gordon K.
Lindeman, Geoffrey J.
Visvader, Jane E.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2010-04-11
Volume: 465
Issue: 7299
Pages: 798-802
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature09027
OpenAlex: W2117963341
Cited by: 693
References: 38
Citations by year: 2026: 8 · 2025: 16 · 2024: 29 · 2023: 22 · 2022: 29 · 2021: 30 · 2020: 30 · 2019: 32 · 2018: 40 · 2017: 44 · 2016: 45 · 2015: 63 · 2014: 53 · 2013: 64 · 2012: 76
FWCI: 45.37
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
Keywords: mammary stem cells, steroid hormone signaling, estrogen, progesterone, RANKL, breast cancer risk, pregnancy, ovariectomy, letrozole, aromatase inhibition, chemoprevention, paracrine signaling, mammary gland development
MeSH terms: Letrozole, Animals, Aromatase, Cell Count, Estrogens, Female, Humans, Mammary Glands, Animal, Nitriles, Ovariectomy, Pregnancy, Pregnancy, Animal, Progesterone, Receptors, Estrogen, Receptors, Progesterone, Stem Cells, Triazoles, Signal Transduction, Integrin beta1, Paracrine Communication, Integrin beta3, Aromatase Inhibitors, Mice, CD24 Antigen, RANK Ligand, ErbB Receptors

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Control of mammary stem cell function by steroid hormone signalling

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