Control of mammary stem cell function by steroid hormone signalling
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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Roast is especially useful for finding similarities in gene expression patterns between different expression studies.
“It is therefore especially useful for finding similarities in gene expression patterns between different expression studies (57,59–61) (Figure 4C).”
From limma powers differential expression analyses for RNA-sequencing and microarray studies (2015) · cites this paper as [61]
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“Current understanding is that the profile CD49f/CD29/CD24 characterizes bipotent MaSCs in the resting (from non-pregnant, non-lactating females) human breast and that subsequent progenitors gradually lose expression of the stem cell marker CD49f.(13,15,16) MaSCs are also thought to express cytokeratin 5 (CK5), which s…”
BackgroundChakrabarti, R., Wei, Y., Hwang, J., Hang, X., Blanco, M. A., Choudhury, A., Tiede, B., Romano, R. A., DeCoste, C. J., Mercatali, L., et al. (2014) · Nature Cell Biology · doi:10.1038/ncb3040 · Cited by 207 · see citing works
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“Conversely, the recent findings of positive effects of ovarian steroid hormones on stem cell proliferation in mammals (46, 47) suggest that BR promotion of boundary cell growth may reflect an ancient function of steroid hormones in promoting stem cell proliferation.”
BackgroundPalafox, M., Ferrer, I., Pellegrini, P., Vila, S., Hernández-Ortega, S., Urruticoechea, A., Climent, F., Soler, M. T., Muñoz, P., Viñals, F., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-0044 · Cited by 199 · see citing works
“The RANK/RANKL signaling pathway, although dispensable for the initial development of the mammary gland in mice (2), controls the expansion of the stem cell compartment in adults (5, 6).”
BackgroundDougall, W. C. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-2507 · Cited by 200 · see citing works
Pal, B., Chen, Y., Vaillant, F., Jamieson, P. R., Gordon, L., Rios, A. C., Wilcox, S., Fu, N. Y., Liu, K. H., Jackling, F. C., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01560-x · Cited by 189 · see citing works
PTP1B: A simple enzyme for a complex world
Feldhammer, M., Uetani, N., Miranda‐Saavedra, D., & Tremblay, M. L. (2013) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2013.819830 · Cited by 195 · see citing works
“part through the reduced expression of the estrogenresponsive genes progesterone and Rankl, which are critical in the formation of mammary alveoli and expansion of mammary stem cells (Asselin-Labat et al., 2010; Joshi et al., 2010).”
BackgroundNotch ligand Dll1 mediates cross-talk between mammary stem cells and the macrophageal niche
Chakrabarti, R., Celià-Terrassa, T., Kumar, S., Hang, X., Wei, Y., Choudhury, A., Hwang, J., Peng, J., Nixon, B. G., Grady, J. J., et al. (2018) · Science · doi:10.1126/science.aan4153 · Cited by 196 · see citing works
“Gene set enrichment analysis (GSEA) confirmed that P4-Dll1 cells were enriched for MaSC signatures (26, 30), whereas P4-Dll1 cells were enriched for luminal signatures (Fig.”
BackgroundMethodInfluentialThe biology of progesterone receptor in the normal mammary gland and in breast cancer
Obr, A. E., & Edwards, D. P. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.10.030 · Cited by 189 · see citing works
“…P4 can regulate MaSCs, administration of P4 in intact adult mice increased the population of MaSCs and ovariectomy reduced the total number of repopulating cells in the mammary gland and diminished ductal outgrowths in transplantation experiments (Asselin-Labat et al., 2010; Joshi et al., 2010).”
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Dynamic visualization of RANKL and Th17-mediated osteoclast function
Kikuta, J., Wada, Y., Kowada, T., Wang, Z., Sun‐Wada, G., Nishiyama, I., Mizukami, S., Maiya, N., Yasuda, H., Kumanogoh, A., et al. (2013) · Journal of Clinical Investigation · doi:10.1172/jci65054 · Cited by 189 · see citing works
“Pretreatment of Th17 with anti-RANKL neutralizing antibody (27, 28) or osteoprotegerin (OPG), a decoy receptor for RANKL (29), reduced association of these T cells with the osteoclasts (Figure 5, E and F, Supplemental Figure 6, and Supplemental Video 8), whereas we observed no effect of anti-RANKL on the mobility of T…”
The role of NF-κB in breast cancer initiation, growth, metastasis, and resistance to chemotherapy
Pavitra, E., Kancharla, J., Gupta, V. K., Prasad, K., Sung, J. Y., Kim, J., Tej, M. B., Choi, R., Lee, J., Han, Y., et al. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114822 · Cited by 194 · see citing works
Paracrine activation of WNT/β-catenin pathway in uterine leiomyoma stem cells promotes tumor growth
Ono, M., Yin, P., Navarro, A., Moravek, M. B., Coon, J. S., Druschitz, S. A., Serna, V. A., Qiang, W., Brooks, D. C., Malpani, S. S., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1313650110 · Cited by 186 · see citing works
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Advances in the biology of bone metastasis: How the skeleton affects tumor behavior
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“(Adapted from [120] and [109].”
BackgroundEstrogen receptor alpha-36 (ER-α36): A new player in human breast cancer
Wang, Z., & Yin, L. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.04.017 · Cited by 185 · see citing works
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RANK-ligand (RANKL) expression in young breast cancer patients and during pregnancy
Azim, H. A., Peccatori, F. A., Brohée, S., Branstetter, D. G., Loi, S., Viale, G., Piccart, M. J., Dougall, W. C., Pruneri, G., & Sotiriou, C. P. (2015) · Breast Cancer Research · doi:10.1186/s13058-015-0538-7 · Cited by 181 · see citing works
“We also found that RANK and RANKL expression differ according to the pregnancy trimester (Additional file 2), which was also observed in preclinical experiments [4].”
BackgroundResultInfluentialHormone replacement therapy and the risk of breast cancer
Narod, S. A. (2011) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2011.110 · Cited by 179 · see citing works
The Transcription Factor FOXM1 (Forkhead box M1)
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RANKL/RANK control Brca1 mutation-driven mammary tumors
Sigl, V., Owusu-Boaitey, K. E., Joshi, P. A., Kavirayani, A. M., Wirnsberger, G., Novatchkova, M., Kozieradzki, I., Schramek, D., Edokobi, N., Hersl, J., et al. (2016) · Cell Research · doi:10.1038/cr.2016.69 · Cited by 173 · see citing works
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“Cel Steroid hormone levels vary with gender and physiology and affect proliferation, survival, and cell fate in multiple adult tissues supported by stem cells, such as the brain, mammary epithelium, and hematopoietic system (Asselin-Labat et al., 2010; Pawluski et al., 2009; Ray et al., 2008).”
RANKL/RANK/OPG system beyond bone remodeling: involvement in breast cancer and clinical perspectives
Infante, M., Fabi, A., Cognetti, F., Gorini, S., Caprio, M., & Fabbri, A. (2019) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-018-1001-2 · Cited by 180 · see citing works
“supported by the fact that MaSCs pool increases during the luteal diestrus phase and throughout pregnancy [56, 57].”
BackgroundInfluentialOvarian steroids, stem cells and uterine leiomyoma: therapeutic implications
Moravek, M. B., Yin, P., Ono, M., Coon, J. S., Dyson, M. T., Navarro, A., Marsh, E. E., Chakravarti, D., Kim, J. J., Wei, J., et al. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu048 · Cited by 157 · see citing works
“Scientific direction may be taken from the breast cancer literature, which is a better-studied model of stem-progenitor cells that are deficient in ERs and PRs, but are hormone responsive via paracrine interaction with surrounding differentiated cells (Asselin-Labat et al., 2010; Fillmore et al., 2010; Roarty and Rose…”
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“For ovariectomization and stimulation studies procedures were performed as previously described.(32)”
Tissue-specific designs of stem cell hierarchies
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“The adult mammary gland seems to harbour multiple stem cell populations, including slow-cycling 43 or putative quiescent MaSCs 44,45 , as well as a molecularly distinct MaSC subset that transiently expands during pregnancy 46 .”
Self-citationPhillips, K.-A., Milne, R. L., Rookus, M. A., Daly, M. B., Antoniou, A. C., Peock, S., Frost, D., Easton, D. F., Ellis, S., Friedlander, M. L., et al. (2013) · Journal of Clinical Oncology · doi:10.1200/jco.2012.47.8313 · Cited by 171 · see citing works
Leeuwen, I. J. D. V.-V., Pereira, D. D. C., Flach, K. D., Piersma, S. R., Haase, C., Bier, D., Yalçin, Z., Michalides, R. J. A. M., Feenstra, K. A., Jiménez, C. R., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1220809110 · Cited by 148 · see citing works
“Current therapeutic strategies to treat these tumors rely on selective ER modulators (SERMs), like tamoxifen (TAM) (1) or aromatase inhibitors (AIs) that block estradiol synthesis (2).”
BackgroundHilton, H. N., Clarke, C. L., & Graham, J. D. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.08.011 · Cited by 146 · see citing works
Impact of risk factors on early cancer evolution
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Role of stem cells in human uterine leiomyoma growth
Ono, M., Qiang, W., Serna, V. A., Yin, P., Coon, J. S., Navarro, A., Monsivais, D., Kakinuma, T., Dyson, M., Druschitz, S., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036935 · Cited by 141 · see citing works
“In mammary structures of humans and mice, mammary stem cells, despite being void of ESR1 and PGR themselves, are subject to regulation in both number and repopulating ability by steroid hormones, particularly progesterone [40,41,42,43].”
BackgroundWnt/β-catenin Signaling in Normal and Cancer Stem Cells
Valkenburg, K. C., Graveel, C. R., Diegel, C. R., Zhong, Z. A., & Williams, B. O. (2011) · Cancers · doi:10.3390/cancers3022050 · Cited by 141 · see citing works
“In mice MaSCs are highly enriched in the CD49f hi CD29 hi CD24 + Sca1 - subpopulation [103-105], whereas human cells with features of MaSCs have been identified in the CD49f hi EpCAM - subpopulation [106,107].”
BackgroundInfluentialGenomic aberrations in young and elderly breast cancer patients
Azim, H. A., Nguyen, B., Brohée, S., Zoppoli, G. M., & Sotiriou, C. P. (2015) · BMC Medicine · doi:10.1186/s12916-015-0504-3 · Cited by 140 · see citing works
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“In addition, it has been reported that endogenous progesterone affects the numbers of Lin-CD24+CD49f mammary epithelial stem cells during pregnancy [69] and during the 650 J Mol Med (2011) 89:647–656”
BackgroundIdentification of quiescent and spatially restricted mammary stem cells that are hormone responsive
Fu, N. Y., Rios, A. C., Pal, B., Law, C. W., Jamieson, P. R., Liu, R., Vaillant, F., Jackling, F. C., Liu, K. H., Smyth, G. K., et al. (2017) · Nature Cell Biology · doi:10.1038/ncb3471 · Cited by 134 · see citing works
Breastfeeding and the risk of breast cancer in BRCA1 and BRCA2 mutation carriers
Kotsopoulos, J., Lubiński, J., Salmena, L., Lynch, H. T., Kim‐Sing, C., Foulkes, W. D., Ghadirian, P., Neuhausen, S. L., Demsky, R., Tung, N., et al. (2012) · Breast Cancer Research · doi:10.1186/bcr3138 · Cited by 135 · see citing works
“Recent studies have identified an important role for progesterone in regulating the number of stem cells in normal human and mouse mammary glands [25,26].”
BackgroundGlobal Changes in the Mammary Epigenome Are Induced by Hormonal Cues and Coordinated by Ezh2
Pal, B., Bouras, T., Shi, W., Vaillant, F., Sheridan, J. M., Fu, N. Y., Breslin, K. A., Jiang, K., Ritchie, M. E., Young, M. D., et al. (2013) · Cell Reports · doi:10.1016/j.celrep.2012.12.020 · Cited by 132 · see citing works
“However, the changes apparent in cell cycle regulators may suffice to drive MaSCs into a more quiescent state, as indicated by molecular profiling and cellular analyses (Asselin-Labat et al., 2010).”
BackgroundInfluentialForm and Function: how Estrogen and Progesterone Regulate the Mammary Epithelial Hierarchy
Arendt, L. M., & Kuperwasser, C. (2015) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-015-9337-0 · Cited by 135 · see citing works
“Treatment of mice with the aromatase inhibitor letrozole significantly diminishes repopulating cell numbers [125].”
BackgroundRitte, R., Lukanova, A., Berrino, F., Dossus, L., Tjønneland, A. M., Olsen, A., Overvad, T. F., Overvad, K., Clavel‐Chapelon, F., Fournier, A., et al. (2012) · Breast Cancer Research · doi:10.1186/bcr3186 · Cited by 127 · see citing works
The anti-tumor effect of RANKL inhibition in malignant solid tumors – A systematic review
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Progestin suppression of miR-29 potentiates dedifferentiation of breast cancer cells via KLF4
Cittelly, D. M., Finlay-Schultz, J., Howe, E. N., Spoelstra, N. S., Axlund, S. D., Hendricks, P., Jacobsen, B. M., Sartorius, C. A., & Richer, J. K. (2012) · Oncogene · doi:10.1038/onc.2012.275 · Cited by 126 · see citing works
Derailed estrogen signaling and breast cancer: an authentic couple.
Manavathi, B., Dey, O., Gajulapalli, V. N. R., Bhatia, R., Bugide, S., & Kumar, R. (2013) · Endocrine reviews · doi:10.1210/er.2011-1057 · Cited by 123 · see citing works
“creased in mice treated with E2 plus progesterone (291).”
BackgroundReproductive history and breast cancer risk
Kobayashi, S., Sugiura, H., Ando, Y., Shiraki, N., Yanagi, T., Yamashita, H., & Toyama, T. (2012) · Breast Cancer · doi:10.1007/s12282-012-0384-8 · Cited by 123 · see citing works
“were clarified by 2 different groups [36, 37] (Fig.”
BackgroundAyyanan, A., Laribi, O., Schuepbach‐Mallepell, S., Schrick, C., Gutierrez, M. J., Tanos, T., Lefebvre, G. C., Rougemont, J., Yalcin-Ozuysal, Ö., & Brisken, C. (2011) · Molecular Endocrinology · doi:10.1210/me.2011-1129 · Cited by 123 · see citing works
From milk to malignancy: the role of mammary stem cells in development, pregnancy and breast cancer
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Common Breast Cancer Susceptibility Loci Are Associated with Triple-Negative Breast Cancer
Purrington, K. S., Vachon, C. M., Lee, A. M., Slager, S., Lesnick, T. G., Olswold, C., Fasching, P. A., Miron, P. L., Eccles, D., Carpenter, J., et al. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-1266 · Cited by 119 · see citing works
“However, recent studies in mice have shown that the mammary stem cell compartment can be regulated by 17 く-estradiol and progesterone through a paracrine-signalling mechanism from steroid receptor-positive luminal cells to steroid receptor-negative stem cells (29, 30).”
The RANK–RANKL–OPG System: A Multifaceted Regulator of Homeostasis, Immunity, and Cancer
León-Oliva, D. D., Barrena-Blázquez, S., Jiménez-Álvarez, L., Fraile‐Μartinez, O., Montero, C. G., López-González, L., Torres‐Carranza, D., García-Puente, L. M., Carranza, S. T., Álvarez-Mon, M. Á., et al. (2023) · Medicina · doi:10.3390/medicina59101752 · Cited by 136 · see citing works
“RANKL then engages with RANK in both an autocrine and paracrine fashion, thereby stimulating cellular proliferation, including the pool of mammary stem cells, and the formation of milk-secreting acini throughout pregnancy (Figure 2) [44,45].”
BackgroundGarbe, J. C., Pepin, F., Pelissier, F. A., Sputova, K., Fridriksdottir, A. J., Guo, D. E., Villadsen, R., Park, M., Petersen, O. W., Borowsky, A. D., et al. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-0157 · Cited by 121 · see citing works
“Estrogen and progesterone can directly impact the epithelium by causing fluctuations in the stem cell pool (8, 9) and are required for gland morphogenesis (10–12).”
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“Other pathways associated with mammary stem/progenitor cells and mammary gland development [39–41], such as Wnt/b-catenin and RANK signaling pathways were also implicated in the gene expression patterns.”
HER2 and Breast Cancer Stem Cells: More than Meets the Eye
Körkaya, H., & Wicha, M. S. (2013) · Cancer Research · doi:10.1158/0008-5472.can-13-0260 · Cited by 117 · see citing works
“It has previously been shown that normal breast stem cells are regulated by RANK ligand, which is produced in response to progesterone elevation during pregnancy (21, 22).”
BackgroundMammary Development and Breast Cancer: A Wnt Perspective
Yu, Q. C., Verheyen, E. M., & Zeng, Y. A. (2016) · Cancers · doi:10.3390/cancers8070065 · Cited by 116 · see citing works
“RANKL (receptor activator of NF-kB ligand) is another downstream target of progesterone that has been proposed to be a hormone-mediated local factor for MaSCs [139].”
BackgroundWnt and Neuregulin1/ErbB signalling extends 3D culture of hormone responsive mammary organoids
Jardé, T., Lloyd‐Lewis, B., Thomas, M., Kendrick, H. D., Melchor, L., Bougaret, L., Watson, P., Ewan, K., Smalley, M. J., & Dale, T. C. (2016) · Nature Communications · doi:10.1038/ncomms13207 · Cited by 114 · see citing works
Estrogen and Progesterone in Normal Mammary Gland Development and in Cancer
Stingl, J. (2010) · Hormones and Cancer · doi:10.1007/s12672-010-0055-1 · Cited by 115 · see citing works
“The effects of reduced exposure to estrogen on MRUs are thought to be mediated by inducing these cells into a quiescent state [ 32 ].”
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“Recent evidence indicates a special role of steroid hormones in the control of normal mammary stem cell function (24, 25) that implicates stem cells as the potential target during hormonal carcinogenesis.”
BackgroundMammary Stem Cells: Premise, Properties, and Perspectives
Lloyd‐Lewis, B., Harris, O. B., Watson, C. J., & Davis, F. M. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.04.001 · Cited by 112 · see citing works
- 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
- Venue
- Nature
- Published
- 2010-04-11
- Volume
- 465
- Issue
- 7299
- Pages
- 798-802
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- 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 › Genetics › 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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