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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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“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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Effects of estrogen on the proportion of stem cells in the breast
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“Previous studies have shown that hormonal treatment expandsMaSCs in vivo and that elevatedWnt4 and Rankl levels are correlated with hormonal treatment (Asselin-Labat et al. 2010; Joshi et al. 2010).”
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“In gravid rodents, hormones, particularly progesterone, are implicated in proliferation of breast epithelium and massive expansion of stem cells during pregnancy (33).”
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“Mammary stem cells have also been shown to be responsive to sex steroid hormones despite not having a clear expression of an ER or PR.(39) In the EPIC cohort, prediagnostic levels of estrogens were found to be associated with both HR-positive and HRnegative postmenopausal breast cancer.”
BackgroundRANKL and RANK: From Mammalian Physiology to Cancer Treatment
Rao, S., Cronin, S. J. F., Sigl, V., & Penninger, J. M. (2017) · Trends in Cell Biology · doi:10.1016/j.tcb.2017.11.001 · Cited by 95
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“BCSC are considered ERα negative, but can still be stimulated by estradiol via paracrine mechanisms [121].”
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“…hormones released during the estrus cycle and pregnancy (Asselin-Labat et al., 2007; Asselin-Labat et al., 2010; Joshi et al., 2010) and these pregnancy-induced MaSCs possess distinct properties compared to MaSCs in the virgin gland such as more limited self-renewal (Asselin-Labat et al., 2010).”
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“…pregnancy or estrus), induces amplification of the basal myoepithelial cell population and expansion of the mammary stem cell population via paracrine mechanisms involving the Wnt and RANK pathways (Brisken and O’Malley 2010; Incassati et al., 2010; Asselin-Labat et al., 2010; Joshi et al., 2010).”
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“Although stem cells in other tissues, such as breast, are reported to lack expression of sex steroid receptors [41,42,55], estrogen and progesterone may impact the function of stem/progenitor cells indirectly by mediating the supply of regulatory factors from neighboring cells (such as Wnt or receptor activator of NF-…”
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BackgroundStem Cells in Toxicology: Fundamental Biology and Practical Considerations
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“Elegant fluorescence-activated cell sorting experiments revealed that the size of the stem-cellenriched population depends on the hor monal status of the animal, increasing during diestrous and pregnancy and decreasing with ovariectomy and antiestrogen treatments [95,96].”
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“Indeed, recent studies suggest that RANKL may be a critical link between PR luminal cells and mammary stem/progenitor cells (32, 33).”
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“By late pregnancy, the number of stem cells returns to near basal levels observed in prepregnant mice (Tiede et al. 2009; Asselin-Labat et al. 2010).”
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BackgroundRANK Signaling Amplifies WNT-Responsive Mammary Progenitors through R-SPONDIN1
Joshi, P. A., Waterhouse, P. D., Kannan, N., Narala, S., Fang, H., Grappa, M. A. D., Jackson, H. W., Penninger, J. M., Eaves, C. J., & Khokha, R. (2015) · Stem Cell Reports · doi:10.1016/j.stemcr.2015.05.012 · Cited by 80
“RANKL is a known, and sufficient, mediator of mammary lobuloalveologenesis downstream of progesterone (Beleut et al., 2010; Fata et al., 2000), but little is known of its effect on different adult mammary epithelial subsets and progenitors.”
BackgroundEstrogen Receptor β as a Therapeutic Target in Breast Cancer Stem Cells
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“Although considered ERa-negative, BSC and MSC numbers can be expanded by incubation with estradiol (12,13), previously explained by paracrine stimulation (14,15).”
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“Stem cells as defined by the first approach are located in the basal layer and express high levels of integrin 1 and 6 (48, 49) and have been shown to expand in response to hormone stimulation (50, 51).”
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“In addition to mediating the mitogenic effect of progesterone, RANKL also controls the responsiveness of mammary stem cell and luminal progenitors(12) to progesterone.(13,14) These observations provided the initial rationale that RANKL might also directly stimulate tumor formation and metastatic progression through ac…”
BackgroundIdentification of Quiescent, Stem-Like Cells in the Distal Female Reproductive Tract
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Borcherding, N. C., Kusner, D. M., Kolb, R. H., Xie, Q. M., Li, W., Yuan, F., Velez, G., Askeland, R. W., Weigel, R. J., & Zhang, W. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-2761 · Cited by 72
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Identification of NOG as a Specific Breast Cancer Bone Metastasis-supporting Gene
Tarragona, M., Pavlović, M., Estape, A. A., Urosevic, J., Morales, M. L. G., Guiu, M., Planet, E., González‐Suárez, E., & Gomis, R. R. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.355834 · Cited by 75
“Moreover, the induction of ID2 correlatedwith a higher expression level ofRANK, which has been described to be key tomaintain the pool of mammary stem epithelial cells (24) and is in agreement with previous findings (25).”
BackgroundResultChen, C.-C., & Chuong, C. (2012) · Journal of Dermatological Science · doi:10.1016/j.jdermsci.2012.02.007 · Cited by 69
Jonas, W., & Woodside, B. C. (2015) · Hormones and Behavior · doi:10.1016/j.yhbeh.2015.07.018 · Cited by 78
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“Breast SCs are sensitive to steroid hormone signaling, even in the absence of ER and PR (Asselin-Labat et al. 2010).”
BackgroundRANKL and RANK in sex hormone-induced breast cancer and breast cancer metastasis
Schramek, D., Sigl, V., & Penninger, J. M. (2011) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2011.02.007 · Cited by 73
Ogba, N., Manning, N. G., Bliesner, B., Ambler, S. K., Haughian, J. M., Pinto, M. P., Jedlicka, P., Joensuu, K. M., Heikkilä, P., & Horwitz, K. B. (2014) · Breast Cancer Research · doi:10.1186/s13058-014-0489-4 · Cited by 68
“P appears to have no effect on long-term tumor growth in vivo [11] but expands normal adult mammary stem cells and cancer stem cells [12-14].”
Inflammatory breast cancer: unique biological and therapeutic considerations
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Moving Breast Cancer Therapy up a Notch
Mollen, E., Ient, J., Tjan‐Heijnen, V. C. G., Boersma, L. J., Miele, L., Smidt, M. L., & Vooijs, M. (2018) · Frontiers in Oncology · doi:10.3389/fonc.2018.00518 · Cited by 67
“This mainly targets the tumor bulk, however, important implications have been made for hormone receptor-positive stem cells (244, 245).”
BackgroundBrisken, C., & Scabia, V. (2020) · Journal of Molecular Endocrinology · doi:10.1530/jme-20-0091 · Cited by 68
Progestin regulated miRNAs that mediate progesterone receptor action in breast cancer
Cochrane, D. R., Jacobsen, B. M., Connaghan, K. D., Howe, E. N., Bain, D. L., & Richer, J. K. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.12.020 · Cited by 68
“Recently, several groups have demonstrated in both normal and malignant breast cells, that P4 mediates the expansion of a stem cell population (Asselin-Labat et al., 2010; Graham et al., 2009; Horwitz and Sartorius, 2008; Joshi et al., 2010).”
BackgroundPardo, I., Lillemoe, H. A., Blosser, R. J., Choi, M.-R., Sauder, C. A. M., Doxey, D. K., Mathieson, T., Hancock, B. A., Baptiste, D. F., Atale, R. V., et al. (2014) · Breast Cancer Research · doi:10.1186/bcr3627 · Cited by 61
“Asselin-Labat and colleagues utilized fluorescentactivated cell sorting to divide mouse mammary cells into luminal (CD29CD24) and mammary stem cellenriched (CD29CD24) subfractions [18].”
BackgroundMethodInfluentialStem cells in prostate cancer: treating the root of the problem
Taylor, R. A., Toivanen, R., & Risbridger, G. P. (2010) · Endocrine Related Cancer · doi:10.1677/erc-10-0145 · Cited by 71
Mammary Gland Reprogramming: Metalloproteinases Couple Form with FunctionPreprint
Khokha, R., & Werb, Z. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a004333 · Cited by 73
“2010), and 11-fold during gestation (Asselin-Labat et al. 2010).”
BackgroundEstrogen receptors in breast and bone: from virtue of remodeling to vileness of metastasis
Bado, I., Gugala, Z., Fuqua, S. A. W., & Zhang, X. (2017) · Oncogene · doi:10.1038/onc.2017.94 · Cited by 65
A Longitudinal Study of Growth, Sex Steroids, and IGF-1 in Boys With Physiological Gynecomastia
Mieritz, M. G., Rakêt, L. L., Hagen, C. P., Nielsen, J. E., Talman, M., Petersen, J. H., Sommer, S., Main, K. M., Jørgensen, N., & Juul, A. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-2836 · Cited by 65
“ceptors (IGF-1R), andprogesterone receptors (16,17), but”
Wnt Signaling in Mammary Glands: Plastic Cell Fates and Combinatorial SignalingPreprint
Alexander, C. M., Goel, S., Fakhraldeen, S. A., & Kim, S. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008037 · Cited by 62
SH3RF3 promotes breast cancer stem-like properties via JNK activation and PTX3 upregulation
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Basree, M. M., Shinde, N., Koivisto, C. S., Cuitiño, M. C., Kladney, R. D., Zhang, J., Stephens, J. A., Palettas, M. S., Zhang, A., Kim, H. K., et al. (2019) · Breast Cancer Research · doi:10.1186/s13058-019-1163-7 · Cited by 67
RANKL/RANK: from bone loss to the prevention of breast cancer
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Breast Cancer Stem Cells and Their Role in Resistance to Endocrine Therapy
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“01% cells expressing ER [40, 41].”
BackgroundRANKL, a necessary chance for clinical application to osteoporosis and cancer-related bone diseases
Yasuda, H. (2013) · World Journal of Orthopedics · doi:10.5312/wjo.v4.i4.207 · Cited by 62
The mammary cellular hierarchy and breast cancer
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“Three weeks of treatment with the aromatase inhibitor Letrozole, which inhibits the synthesis of estrogen, is sufficient to significantly decrease the numbers and activity of mammary stem cells [6].”
InfluentialRole of the RANK/RANKL pathway in breast cancer
Kiesel, L., & Kohl, A. (2016) · Maturitas · doi:10.1016/j.maturitas.2016.01.001 · Cited by 64
Fu, N. Y., Pal, B., Chen, Y., Jackling, F. C., Milevskiy, M. J. G., Vaillant, F., Capaldo, B. D., Guo, F., Liu, K. H., Rios, A. C., et al. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.10.001 · Cited by 60
The Mammary Stem Cell Hierarchy
Fu, N. Y., Lindeman, G. J., & Visvader, J. E. (2014) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/b978-0-12-416022-4.00005-6 · Cited by 66
Salmen, J., Neugebauer, J. K., Fasching, P. A., Haeberle, L., Huober, J., Wöckel, A., Rauh, C., Schütz, F., Weissenbacher, T. M., Kost, B., et al. (2014) · Breast Cancer Research and Treatment · doi:10.1007/s10549-014-3130-4 · Cited by 59
RANK as a therapeutic target in cancer
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Ritter, H. D., Antonova, L., & Mueller, C. R. (2012) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-11-0423-t · Cited by 59
“Elevated progesterone levels have been suggested to lead to an increase in the breast stem cell population (41, 42); altered BRCA1 levels as a consequence of altered GR levels may produce the same effect through decreased BRCA1 blocking differentiation.”
BackgroundMakarem, M., Kannan, N., Nguyen, L. V., Knapp, D. J. H. F., Balani, S., Prater, M. D., Stingl, J., Raouf, A., Nemirovsky, O., Eirew, P. D., et al. (2013) · PLoS Biology · doi:10.1371/journal.pbio.1001630 · Cited by 59
“mammary cells or other cell types (16 ng/ml bFGF [21], 16 ng/”
Huntingtin Regulates Mammary Stem Cell Division and Differentiation
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“These populations are negative for steroid hormone receptors and consist of cells that express basal cell markers (Asselin-Labat et al., 2010).”
BackgroundProgesterone Receptor and Stat5 Signaling Cross Talk Through RANKL in Mammary Epithelial Cells
Obr, A. E., Grimm, S. L., Bishop, K. A., Pike, J. W., Lydon, J. P., & Edwards, D. P. (2013) · Molecular Endocrinology · doi:10.1210/me.2013-1077 · Cited by 58
“In addition to proliferation of mature luminal epithelial cells, RANKL mediates P4-induced expansion and activation of ER/PR-negative mouse mammary stem cell populations by a paracrine pathway (23, 24), and it is a paracrine mediator of P4 induction of Elf5 in PR-negative luminal progenitor cell populations required f…”
RANK expression on breast cancer cells promotes skeletal metastasis
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Metadata
- 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 › 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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