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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Background
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Background
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BackgroundMethodInfluential
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BackgroundInfluential
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“Moreover, when mice are ovariectomized or treated with letrozole (to inhibit endogenous estrogen biosynthesis and provide a normal stromal and hormonal environment for all other hormones), a decrease in the absolute number of repopulating cells and in ductal growth and expansion was reported in the fat pads following…”
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Reprogramming of the estrogen responsive transcriptome contributes to tamoxifen-dependent protection against tumorigenesis in the p53 null mammary epithelial cells
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Alterations in Progesterone Receptor Isoform Balance in Normal and Neoplastic Breast Cells Modulates the Stem Cell Population
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Background
Premenopausal Plasma Osteoprotegerin and Breast Cancer Risk: A Case–Control Analysis Nested within the Nurses' Health Study II
Kotsopoulos, J., McGee, E. E., Lozano‐Esparza, S., Garber, J. E., Ligibel, J. A., Collins, L. C., Polyák, K., Brown, M. A., Narod, S. A., Tamimi, R. M., et al. (2020) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-19-1154 · Cited by 10
“Activation of the RANK/RANKL pathway promotes proliferation, differentiation, andmigration of mammary epithelial cell (1, 3) as well as expansion and survival of mammary stem cells (4).”
Background
Dietary suppression of the mammary CD29hiCD24+ epithelial subpopulation and its cytokine/chemokine transcriptional signatures modifies mammary tumor risk in MMTV-Wnt1 transgenic mice
Rahal, O. M., Machado, H. L., Montales, M. T. E., Pabona, J. M. P., Heard, M. E., Nagarajan, S., & Simmen, R. C. M. (2013) · Stem Cell Research · doi:10.1016/j.scr.2013.08.006 · Cited by 10
“…systemic levels of progesterone and estradiol While both human and mouse MaSCs lack estrogen receptor and progesterone receptor expression, MaSC activity is under hormonal regulation via paracrine signaling from the luminal compartment (Asselin-Labat et al., 2006, 2010; Joshi et al., 2010).”
Background
Lineage Tracing of Mammary Stem and Progenitor Cells
van de Moosdijk, A. A. A., Fu, N. Y., Rios, A. C., Visvader, J. E., & van Amerongen, R. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-6475-8_15 · Cited by 10
Macrophages stimulate mammary stem cells
Kannan, N., & Eaves, C. J. (2018) · Science · doi:10.1126/science.aau1394 · Cited by 10
Aberrant Activation of the RANK Signaling Receptor Induces Murine Salivary Gland Tumors
Szwarc, M. M., Kommagani, R., Jacob, A. P., Dougall, W. C., Ittmann, M., & Lydon, J. P. (2015) · PLoS ONE · doi:10.1371/journal.pone.0128467 · Cited by 9
A Potential Role of Progestin-Induced Laminin-5/α6-Integrin Signaling in the Formation of Side Branches in the Mammary Gland
Meyer, G., Leipprandt, J. R., Xie, J., Aupperlee, M. D., & Haslam, S. Z. (2012) · Endocrinology · doi:10.1210/en.2012-1518 · Cited by 9
Three-dimensional genome architecture coordinates key regulators of lineage specification in mammary epithelial cells
Milevskiy, M., Coughlan, H., Kane, S. R., Johanson, T. M., Kordafshari, S., Chan, W.-F., Tsai, M., Surgenor, E. E., Wilcox, S., Allan, R., et al. (2023) · Cell Genomics · doi:10.1016/j.xgen.2023.100424 · Cited by 10
“17,18,21,60 Furthermore, we identiﬁed lineage-speciﬁc SEs that overlapped crucial mammary regulatory genes, including Trp63 , Foxp1 , Foxa1 , Gata3 , Esr1 , and Notch1 .”
Dual role of pregnancy in breast cancer risk
Fu, S., Hao, K., Yuan, H., Xu, H., Chen, W., & Zhao, L. (2024) · General and Comparative Endocrinology · doi:10.1016/j.ygcen.2024.114501 · Cited by 9
Metastasis initiating cells in primary prostate cancer tissues from transurethral resection of the prostate (TURP) predicts castration-resistant progression and survival of prostate cancer patients
Li, Q., Li, Q., Nuccio, J., Liu, C., Duan, P., Wang, R., Jones, L. W., Chung, L. W. K., & Zhau, H. E. (2015) · The Prostate · doi:10.1002/pros.23011 · Cited by 9
“Increased RANK–RANKL signaling in PC cells could enhance normal bone turnover [14–17], stem cell renewal, and differentiation [16,18,19] and these factors together contribute to prostate and breast cancer bone and soft tissue metastases [5,10,20–23].”
Background
Protein tyrosine phosphatase 1B restrains mammary alveologenesis and secretory differentiation
Milani, E. S., Brinkhaus, H., Dueggeli, R., Klebba, I., Mueller, U., Stadler, M. B., Kohler, H., Smalley, M. J., & Bentires‐Alj, M. (2012) · Development · doi:10.1242/dev.082941 · Cited by 9
Deregulated ephrin-B2 signaling in mammary epithelial cells alters the stem cell compartment and interferes with the epithelial differentiation pathway
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Intrinsic cues and hormones control mouse mammary epithelial tree size
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“Conversely, it might help explain the increase in breast cancer incidence that accompanies pregnancy (21) or the decrease in breast cancer risk associated with ovariectomy.”
Background
The prognostic role of RANK SNP rs34945627 in breast cancer patients with bone metastases
Ferreira, A. R., Alho, I., Vendrell, I., Melo, M., Lopes-Brás, R., Costa, A. L., Sousa, A. R., Mansinho, A., Abreu, C., Pulido, C., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.9356 · Cited by 9
“Besides its role in bone, RANK-RANKL signaling pathway has also a key role in mammary gland development [23, 24].”
Background
Engineering Mammary Gland in Vitro Models for Cancer Diagnostics and Therapy
Campbell, J. J., Hume, R. D., & Watson, C. J. (2014) · Molecular Pharmaceutics · doi:10.1021/mp500121c · Cited by 9
LPA receptor activity is basal specific and coincident with early pregnancy and involution during mammary gland postnatal development
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“Together with luminal cells, the basal epithelial population undergoes significant changes at the gene expression level when exposed to the ovarian hormones 17 β -estradiol and progesterone 7,38 .”
Lack of Breastfeeding History in Parous Women with Inflammatory Breast Cancer Predicts Poor Disease-Free Survival
Stecklein, S. R., Reddy, J. P., Wolfe, A. R., Lopez, M. S., Fouad, T. M., Debeb, B. G., Ueno, N. T., Brewster, A. M., & Woodward, W. A. (2017) · Journal of Cancer · doi:10.7150/jca.20095 · Cited by 9
Serum osteoprotegerin levels and mammographic density among high-risk women
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cIAP2 Is an Independent Signaling and Survival Factor during Mammary Lactational Involution and Tumorigenesis
Carr, D., Lau, R., Hnatykiw, A. D., Ward, G. C. D., Daneshmand, M., Cabrita, M. A., & Pratt, M. A. C. (2018) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-018-9398-y · Cited by 9
Calorie restriction and rapamycin administration induce stem cell self-renewal and consequent development and production in the mammary gland
Kfir, S. H., & Barash, I. (2019) · Experimental Cell Research · doi:10.1016/j.yexcr.2019.06.022 · Cited by 9
Inducible knockout of ∆Np63 alters cell polarity and metabolism during pubertal mammary gland development
Kumar, S., Nandi, A., Mahesh, A., Sinha, S., Flores, E. R., & Chakrabarti, R. (2019) · FEBS Letters · doi:10.1002/1873-3468.13703 · Cited by 9
RANKL and OPG and their influence on breast volume changes during pregnancy in healthy women
Wunderle, M., Ruebner, M., Häberle, L., Schwenke, E., Hack, C. C., Bayer, C. M., Koch, M., Schwitulla, J., Schulz-Wendtland, R., Kozieradzki, I., et al. (2020) · Scientific Reports · doi:10.1038/s41598-020-62070-3 · Cited by 9
Single-cell and spatial analyses reveal a tradeoff between murine mammary proliferation and lineage programs associated with endocrine cues
Gray, G. K., Girnius, N., Kuiken, H. J., Henstridge, A. Z., & Brugge, J. S. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113293 · Cited by 10
Therapeutic Implications of Cytokines and Chemokines Network in Cancer
Mir, M. A., Jan, N., & Noor, I. (2023) · Springer eBooks · doi:10.1007/978-981-99-4657-0_14 · Cited by 12
Transcriptomic Analysis of Pubertal and Adult Virgin Mouse Mammary Epithelial and Stromal Cell Populations
Heijmans, N., Wiese, K. E., Jonkers, J., & van Amerongen, R. (2024) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-024-09565-1 · Cited by 8
“Studies investigating the link between steroid hormones and Wnt genes or MaSC activity are often performed using ovariectomized mice receiving treatment with progesterone and/or estrogen pellets or injections [9, 10, 16, 19, 30].”
Background
RANK/RANKL Signaling Pathway in Breast Development and Cancer
Pérez-Chacón, G., Santamarı́a, P. G., Redondo-Pedraza, J., & González‐Suárez, E. (2025) · Advances in experimental medicine and biology · doi:10.1007/978-3-031-70875-6_16 · Cited by 9
Antiprogestins for breast cancer treatment: We are almost ready
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Activity of ABCG2 Is Regulated by Its Expression and Localization in DHT and Cyclopamine‐Treated Breast Cancer Cells
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“An interesting finding from these studies was that similar to ER and PR expression [Asselin-Labat et al., 2010], AR expression was undetectable in the Hoechst 33342/CD44/CD24”
Result
Reproductive and Lifestyle Factors and Circulating sRANKL and OPG Concentrations in Women: Results from the EPIC Cohort
Sarink, D., Yang, J., Johnson, T., Chang-Claude, J. C., Overvad, K., Olsen, A., Tjønneland, A. M., Fournier, A., Mancini, F. R., Kvaskoff, M., et al. (2019) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-19-0241 · Cited by 8
“In addition to progesterone, prolactin and parathyroid hormone-related peptide, but not 257 estradiol, have been shown to induce RANKL expression in mouse mammary tissue [24-28].”
Background
Hormone-Responsive BMP Signaling Expands Myoepithelial Cell Lineages and Prevents Alveolar Precocity in Mammary Gland
Shao, C., Lou, P., Liu, R., Bi, X., Li, G., Xu, Y., Sheng, X., Xu, J., Lv, C., & Yu, Z. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.691050 · Cited by 8
Lysine stimulates the development of the murine mammary gland at puberty via PI3K/AKT/mTOR signalling axis.
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“Recent studies have demonstrated the role of RANK– RANKL signaling in murine mammary stem cell (MaSC) maintenance.[61,62] RANK–RANKL axis has been shown to be a major player in maintaining the MaSC pool in the mammary glands of mice.”
Early-Onset Breast Cancer: What do We Know about the Risk Factors?
Narod, S. A. (2011) · Current Oncology · doi:10.3747/co.v18i5.938 · Cited by 8
Hormone replacement therapy dependent changes in breast cancer‐related gene expression in breast tissue of healthy postmenopausal women
Sieuwerts, A. M., Napoli, G. D., van Galen, A., Kloosterboer, H. J., de Weerd, V., Zhang, H., Martens, J. W. M., Foekens, J. A., & Geyter, C. D. (2011) · Molecular Oncology · doi:10.1016/j.molonc.2011.09.003 · Cited by 7
Breast
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Vyatkin, A. D., Otnyukov, D. V., Leonov, S. V., & Belikov, A. V. (2022) · PLoS Genetics · doi:10.1371/journal.pgen.1009996 · Cited by 7
“, 2017), and combine it with the knowledge that sex hormones increase the rate of stem cell division (Asselin-Labat et al., 2010; Joshi et al., 2010; Nakada et al., 2014), the link becomes clear.”
Background
Multiple roles for Bcl-3 in mammary gland branching, stromal collagen invasion, involution and tumor pathology
Carr, D., Zein, A. A., Coulombe, J., Jiang, T., Cabrita, M. A., Ward, G. C. D., Daneshmand, M., SAU, A. C., & Pratt, M. A. C. (2022) · Breast Cancer Research · doi:10.1186/s13058-022-01536-w · Cited by 7
Activation function 1 of progesterone receptor is required for mammary development and regulation of RANKL during pregnancy
Lee, S. H., Yap, Y. H. Y., Lim, C. L., Woo, A. R. E., & Lin, V. C. L. (2022) · Scientific Reports · doi:10.1038/s41598-022-16289-x · Cited by 7
Macrophage-Secreted CSF1 Transmits a Calorie Restriction-Induced Self-Renewal Signal to Mammary Epithelial Stem Cells
Kosenko, A., Salame, T. M., Friedlander, G., & Barash, I. (2022) · Cells · doi:10.3390/cells11182923 · Cited by 6
“For example, steroid hormones were found to induce an 11-fold increase in MaSC number during pregnancy through paracrine signaling by the RANK ligand secreted by mature luminal cells [15].”
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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