Distinct stem cells contribute to mammary gland development and maintenance
Abstract
The mammary epithelium is composed of several cell lineages including luminal, alveolar and myoepithelial cells. Transplantation studies have suggested that the mammary epithelium is maintained by the presence of multipotent mammary stem cells. To define the cellular hierarchy of the mammary gland during physiological conditions, we performed genetic lineage-tracing experiments and clonal analysis of the mouse mammary gland during development, adulthood and pregnancy. We found that in postnatal unperturbed mammary gland, both luminal and myoepithelial lineages contain long-lived unipotent stem cells that display extensive renewing capacities, as demonstrated by their ability to clonally expand during morphogenesis and adult life as well as undergo massive expansion during several cycles of pregnancy. The demonstration that the mammary gland contains different types of long-lived stem cells has profound implications for our understanding of mammary gland physiology and will be instrumental in unravelling the cells at the origin of breast cancers.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Lineage tracing has identified long-lived stem cells in mammary epithelium and prostate.
“Lineage tracing experiments have also facilitated the identification of long-lived stem cells in the mammary epithelium36,37 and in glandular epithelia such as that found in the prostate38.”
From Molecular regulation of stem cell quiescence (2013) · cites this paper as [36]
Cites
A robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907 · see citing works
Identification of stem cells in small intestine and colon by marker gene Lgr5
Barker, N., van Es, J. H., Kuipers, J., Kujala, P., van den Born, M., Cozijnsen, M., Haegebarth, A., Korving, J., Begthel, H., Peters, P. J., et al. (2007) · Nature · doi:10.1038/nature06196 · Cited by 5,687 · see citing works
Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus
Srinivas, S., Watanabe, T., Lin, C.-S., William, C. M., Tanabe, Y., Jessell, T. M., & Costantini, F. (2001) · BMC Developmental Biology · doi:10.1186/1471-213x-1-4 · Cited by 3,121 · see citing works
In vitro propagation and transcriptional profiling of human mammary stem/progenitor cellsPreprint
Dontu, G., Abdallah, W. M., Foley, J. M., Jackson, K. W., Clarke, M. F., Kawamura, M., & Wicha, M. S. (2003) · Genes & Development · doi:10.1101/gad.1061803 · Cited by 2,413 · see citing works
Generation of a functional mammary gland from a single stem cell
Shackleton, M., Vaillant, F., Simpson, K. J., Stingl, J., Smyth, G. K., Asselin-Labat, M.-L., Wu, L., Lindeman, G. J., & Visvader, J. E. (2006) · Nature · doi:10.1038/nature04372 · Cited by 2,005 · see citing works
Purification and unique properties of mammary epithelial stem cells
Stingl, J., Eirew, P. D., Ricketson, I., Shackleton, M. J., Vaillant, F., Choi, D., Li, H. I., & Eaves, C. J. (2006) · Nature · doi:10.1038/nature04496 · Cited by 1,562 · see citing works
Epidermal homeostasis: a balancing act of stem cells in the skin
Blanpain, C., & Fuchs, E. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2636 · Cited by 1,270 · see citing works
Self-citationKeeping abreast of the mammary epithelial hierarchy and breast tumorigenesisPreprint
Visvader, J. E. (2009) · Genes & Development · doi:10.1101/gad.1849509 · Cited by 568 · see citing works
An entire functional mammary gland may comprise the progeny from a single cell
Kordon, E. C., & Smith, G. H. (1998) · Development · doi:10.1242/dev.125.10.1921 · Cited by 558 · see citing works
Early restriction of peripheral and proximal cell lineages during formation of the lung
Perl, A. T., Wert, S. E., Nagy, A., Lobe, C. G., & Whitsett, J. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.152238499 · Cited by 525 · see citing works
Sca-1pos Cells in the Mouse Mammary Gland Represent an Enriched Progenitor Cell Population
Welm, B. E., Tepera, S. B., Bowman, T. V., Graubert, T. A., Rosen, J. M., & Goodell, M. A. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0625 · Cited by 521 · see citing works
Liu, X., Holstege, H. H., van der Gulden, H. M. L., Treur-Mulder, M., Zevenhoven, J., Velds, A., Kerkhoven, R. M., van Vliet, M. H., Wessels, L. F. A., Peterse, J. L., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702969104 · Cited by 474 · see citing works
Lim, E., Wu, D., Pal, B., Bouras, T., Asselin-Labat, M.-L., Vaillant, F., Yagita, H., Lindeman, G. J., Smyth, G. K., & Visvader, J. E. (2010) · Breast Cancer Research · doi:10.1186/bcr2560 · Cited by 440 · see citing works
Hyperproliferation and Defects in Epithelial Polarity upon Conditional Ablation of α-Catenin in Skin
Vasioukhin, V., Bauer, C., Degenstein, L., Wise, B., & Fuchs, E. (2001) · Cell · doi:10.1016/s0092-8674(01)00246-x · Cited by 435 · see citing works
Mammary development in the embryo and adult: a journey of morphogenesis and commitment
Watson, C. J., & Khaled, W. T. (2008) · Development · doi:10.1242/dev.005439 · Cited by 414 · see citing works
Guðjónsson, Þ., Villadsen, R., Nielsen, H. L., Rønnov‐Jessen, L., Bissell, M. J., & PETERSEN, O. W. (2002) · Genes & Development · doi:10.1101/gad.952602 · Cited by 390 · see citing works
Stem cells and breast cancer: A field in transit
Smalley, M. J., & Ashworth, A. (2003) · Nature reviews. Cancer · doi:10.1038/nrc1212 · Cited by 380 · see citing works
Sleeman, K. E., Kendrick, H. D., Ashworth, A., Isacke, C. M., & Smalley, M. J. (2005) · Breast Cancer Research · doi:10.1186/bcr1371 · Cited by 321 · see citing works
Tcf3 Governs Stem Cell Features and Represses Cell Fate Determination in Skin
Nguyen, H., Rendl, M., & Fuchs, E. V. (2006) · Cell · doi:10.1016/j.cell.2006.07.036 · Cited by 287 · see citing works
Wagner, K., Boulanger, C. A., Henry, M. D., Sgagias, M. K., Hennighausen, L. G., & Smith, G. H. (2002) · Development · doi:10.1242/dev.129.6.1377 · Cited by 274 · see citing works
Epidermal progenitors give rise to Merkel cells during embryonic development and adult homeostasis
Keymeulen, A. V., Mascré, G., Youseff, K. K., Harel, I., Michaux, C., de Geest, N., Szpalski, C., Achouri, Y., Bloch, W., Hassan, B. A., et al. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200907080 · Cited by 274 · see citing works
Self-citationβ1 Integrin deletion from the basal compartment of the mammary epithelium affects stem cells
Hosseraye, I. T.-D. L., Deugnier, M., Faraldo, M. M., Petit, V., Bouvard, D., Medina, D., Fässler, R., Thiery, J. P., & Glukhova, M. A. (2008) · Nature Cell Biology · doi:10.1038/ncb1734 · Cited by 264 · see citing works
Srinivasan, K., Strickland, P. A., Valdes, A. M., Shin, G. C., & Hinck, L. (2003) · Developmental Cell · doi:10.1016/s1534-5807(03)00054-6 · Cited by 263 · see citing works
Stingl, J., Eaves, C. J., Kuusk, U., & Emerman, J. T. (1998) · Differentiation · doi:10.1111/j.1432-0436.1998.00201.x · Cited by 252 · see citing works
Smith, G. H. (1996) · Breast Cancer Research and Treatment · doi:10.1007/bf01806075 · Cited by 240 · see citing works
Human Mammary Luminal Epithelial Cells Contain Progenitors to Myoepithelial Cells
Péchoux, C., Guðjónsson, Þ., Rønnov‐Jessen, L., Bissell, M. J., & PETERSEN, O. W. (1999) · Developmental Biology · doi:10.1006/dbio.1998.9133 · Cited by 206 · see citing works
Chepko, G., & Smith, G. H. (1997) · Tissue and Cell · doi:10.1016/s0040-8166(97)80024-9 · Cited by 190 · see citing works
Welm, B. E., Dijkgraaf, G. J. P., Bledau, A. S., Welm, A. L., & Werb, Z. (2008) · Cell stem cell · doi:10.1016/j.stem.2007.10.002 · Cited by 190 · see citing works
Kendrick, H. D., Regan, J. L., Magnay, F., Grigoriadis, A. E., Mitsopoulos, C., Zvelebil, M., & Smalley, M. J. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-591 · Cited by 176 · see citing works
Detection and analysis of mammary gland stem cells
Stingl, J. (2009) · Journal of Pathology · doi:10.1002/path.2457 · Cited by 170 · see citing works
Tsai, Y. C., Lü, Y., Nichols, P. W., Zlotnikov, G., Jones, P. A., & Smith, H. S. (1996) · PubMed · Cited by 166 · see citing works
Badders, N. M., Goel, S., Clark, R. J., Klos, K. S., Kim, S. Y., Bafico, A., Lindvall, C. J., Williams, B. O., & Alexander, C. M. (2009) · PLoS ONE · doi:10.1371/journal.pone.0006594 · Cited by 127 · see citing works
Ca2+ Signaling During Mammalian Fertilization: Requirements, Players, and AdaptationsPreprint
Wakai, T., Vanderheyden, V., & Fissore, R. A. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a006767 · Cited by 92 · see citing works
Murine Mammary Epithelial Stem Cells: Discovery, Function, and Current StatusPreprint
Visvader, J. E., & Smith, G. (2010) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a004879 · Cited by 82 · see citing works
Alveolar progenitor cells develop in mouse mammary glands independent of pregnancy and lactation
Booth, B. W., Boulanger, C. A., & Smith, G. H. (2007) · Journal of Cellular Physiology · doi:10.1002/jcp.21071 · Cited by 67 · see citing works
Rudland, P. S., & Hughes, C. M. (1989) · Journal of Histochemistry & Cytochemistry · doi:10.1177/37.7.2471725 · Cited by 59 · see citing works
Retroviral expression of Wnt-1 and Wnt-7b produces different effects in mouse mammary epithelium
Naylor, S., Smalley, M. J., Robertson, D. M., Gusterson, B. A., Edwards, P. A., & Dale, T. C. (2000) · Journal of Cell Science · doi:10.1242/jcs.113.12.2129 · Cited by 39 · see citing works
Mapping mammary gland architecture using multi-scale in situ analysis
Fernández‐González, R., Illa-Bochaca, I., Welm, B. E., Fleisch, M. C., Werb, Z., Ortíz-de-Solórzano, C., & Barcellos‐Hoff, M. H. (2008) · Integrative Biology · doi:10.1039/b816933k · Cited by 22 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Batlle, E., & Clevers, H. (2017) · Nature Medicine · doi:10.1038/nm.4409 · Cited by 2,769 · see citing works
Evolution of the Cancer Stem Cell Model
Kreso, A., & Dick, J. E. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.02.006 · Cited by 2,212 · see citing works
Identification of the tumour transition states occurring during EMT
Pastushenko, I., Brisebarre, A., Sifrim, A., Fioramonti, M., Revenco, T., Boumahdi, S., Keymeulen, A. V., Brown, D. V., Moers, V., Lemaire, S., et al. (2018) · Nature · doi:10.1038/s41586-018-0040-3 · Cited by 1,488 · see citing works
Self-citationFeng, Y., Spezia, M., Huang, S., Yuan, C., Zeng, Z., Zhang, L., Ji, X., Liu, W., Huang, B., Luo, W., et al. (2018) · Genes & Diseases · doi:10.1016/j.gendis.2018.05.001 · Cited by 1,537 · see citing works
An integral program for tissue renewal and regeneration: Wnt signaling and stem cell control
Clevers, H. C., Loh, K. M., & Nusse, R. (2014) · Science · doi:10.1126/science.1248012 · Cited by 1,351 · see citing works
Molecular regulation of stem cell quiescence
Cheung, T. H., & Rando, T. A. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3591 · Cited by 1,148 · see citing works
Alveolar progenitor and stem cells in lung development, renewal and cancer
Desai, T., Brownfield, D., & Krasnow, M. A. (2014) · Nature · doi:10.1038/nature12930 · Cited by 1,066 · see citing works
Liu, S., Cong, Y., Wang, D., Sun, Y., Deng, L., Liu, Y., Martin-Trevino, R., Li, S., McDermott, S., Landis, M. D., et al. (2014) · Stem Cell Reports · doi:10.1016/j.stemcr.2013.11.009 · Cited by 1,056 · see citing works
Unravelling cancer stem cell potential
Beck, B., & Blanpain, C. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3597 · Cited by 895 · see citing works
Self-citationCancer Stem Cells: Basic Concepts and Therapeutic Implications
Nassar, D., & Blanpain, C. (2016) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathol-012615-044438 · Cited by 869 · see citing works
Self-citationThe great escape: tumour cell plasticity in resistance to targeted therapy
Boumahdi, S., & de Sauvage, F. J. (2019) · Nature Reviews Drug Discovery · doi:10.1038/s41573-019-0044-1 · Cited by 759 · see citing works
Kretzschmar, K., & Watt, F. M. (2012) · Cell · doi:10.1016/j.cell.2012.01.002 · Cited by 719 · see citing works
Lineage-negative progenitors mobilize to regenerate lung epithelium after major injury
Vaughan, A. E., Brumwell, A. N., Xi, Y., Gotts, J. E., Brownfield, D., Treutlein, B., Tan, K., Tan, V. M., Liu, F. C., Looney, M. R., et al. (2014) · Nature · doi:10.1038/nature14112 · Cited by 662 · see citing works
Self-citationDedifferentiation of committed epithelial cells into stem cells in vivo
Tata, P. R., Mou, H., Pardo–Saganta, A., Zhao, R., Prabhu, M., Law, B. M., Vinarsky, V., Cho, J. L., Breton, S., Sahay, A., et al. (2013) · Nature · doi:10.1038/nature12777 · Cited by 657 · see citing works
Yu, Z., Pestell, T. G., Lisanti, M. P., & Pestell, R. G. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.08.022 · Cited by 649 · see citing works
Phenotypic Plasticity: Driver of Cancer Initiation, Progression, and Therapy Resistance
Gupta, P. B., Pastushenko, I., Skibinski, A., Blanpain, C., & Kuperwasser, C. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.11.011 · Cited by 596 · see citing works
Self-citationChoi, J., Park, J.-E., Tsagkogeorga, G., Yanagita, M., Koo, B., Han, N., & Lee, J. (2020) · Cell stem cell · doi:10.1016/j.stem.2020.06.020 · Cited by 569 · see citing works
Plasticity of epithelial stem cells in tissue regeneration
Blanpain, C., & Fuchs, E. (2014) · Science · doi:10.1126/science.1242281 · Cited by 589 · see citing works
Self-citationTumor Heterogeneity in Breast Cancer
Turashvili, G., & Brogi, E. (2017) · Frontiers in Medicine · doi:10.3389/fmed.2017.00227 · Cited by 571 · see citing works
Mammary stem cells and the differentiation hierarchy: current status and perspectivesPreprint
Visvader, J. E., & Stingl, J. (2014) · Genes & Development · doi:10.1101/gad.242511.114 · Cited by 556 · see citing works
Linking EMT programmes to normal and neoplastic epithelial stem cells
Lambert, A. W., & Weinberg, R. A. (2021) · Nature reviews. Cancer · doi:10.1038/s41568-021-00332-6 · Cited by 530 · see citing works
In situ identification of bipotent stem cells in the mammary gland
Rios, A. C., Fu, N. Y., Lindeman, G. J., & Visvader, J. E. (2014) · Nature · doi:10.1038/nature12948 · Cited by 511 · see citing works
Mammary gland development: cell fate specification, stem cells and the microenvironment
Inman, J. L., Robertson, C., Mott, J. D., & Bissell, M. J. (2015) · Development · doi:10.1242/dev.087643 · Cited by 456 · see citing works
van Amerongen, R., Bowman, A. N., & Nusse, R. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.05.023 · Cited by 446 · see citing works
Eccles, S. A., Aboagye, E. O., Ali, S., Anderson, A. S., Armes, J., Berditchevski, F., Blaydes, J. P., Brennan, K. R., Brown, N. J., Bryant, H. E., et al. (2013) · Breast Cancer Research · doi:10.1186/bcr3493 · Cited by 416 · see citing works
Breast Cancer: Multiple Subtypes within a Tumor?
Yeo, S. K., & Guan, J. (2017) · Trends in cancer · doi:10.1016/j.trecan.2017.09.001 · Cited by 399 · see citing works
Dual SMAD Signaling Inhibition Enables Long-Term Expansion of Diverse Epithelial Basal Cells
Mou, H., Vinarsky, V., Tata, P. R., Brazauskas, K., Choi, S. H., Crooke, A. K., Zhang, B., Solomon, G. M., Turner, B., Bihler, H. J., et al. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.05.012 · Cited by 379 · see citing works
Profiling human breast epithelial cells using single cell RNA sequencing identifies cell diversity
Nguyen, Q., Pervolarakis, N., Blake, K., Ma, D., Davis, R. T., James, N., Phung, A. T., Willey, E., Kumar, R., Jabart, E., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04334-1 · Cited by 377 · see citing works
Self-citationTherapeutic Implications of Cellular Heterogeneity and Plasticity in Breast Cancer
Brooks, M., Burness, M. L., & Wicha, M. S. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.08.014 · Cited by 373 · see citing works
Differentiation dynamics of mammary epithelial cells revealed by single-cell RNA sequencing
Bach, K., Pensa, S., Grzelak, M., Hadfield, J., Adams, D. J., Marioni, J. C., & Khaled, W. T. (2017) · Nature Communications · doi:10.1038/s41467-017-02001-5 · Cited by 364 · see citing works
Single luminal epithelial progenitors can generate prostate organoids in culture
Chua, C. W., Shibata, M., Lei, M., Toivanen, R., Barlow, L. J., Bergren, S. K., Badani, K. K., McKiernan, J. M., Benson, M. C., Hibshoosh, H. H., et al. (2014) · Nature Cell Biology · doi:10.1038/ncb3047 · Cited by 352 · see citing works
Reactivation of multipotency by oncogenic PIK3CA induces breast tumour heterogeneity
Keymeulen, A. V., Lee, M. Y., Ousset, M., Brohée, S., Rorive, S., Giraddi, R. R., Wuidart, A., Bouvencourt, G., Dubois, C., Salmon, I. J., et al. (2015) · Nature · doi:10.1038/nature14665 · Cited by 353 · see citing works
Self-citationCancer cell plasticity during tumor progression, metastasis and response to therapy
Pérez-González, A., Bévant, K., & Blanpain, C. (2023) · Nature Cancer · doi:10.1038/s43018-023-00595-y · Cited by 353 · see citing works
Self-citationIdentification of multipotent mammary stem cells by protein C receptor expression
Wang, D., Cai, C., Dong, X., Yu, Q. C., Zhang, X.-O., Yang, L. C., & Zeng, Y. A. (2014) · Nature · doi:10.1038/nature13851 · Cited by 342 · see citing works
Choi, N., Zhang, B., Zhang, L., Ittmann, M., & Xin, L. (2012) · Cancer Cell · doi:10.1016/j.ccr.2012.01.005 · Cited by 336 · see citing works
Benz, C., Copley, M. R., Kent, D. G., Wöhrer, S., Cortés, A., Aghaeepour, N., Ma, E., Mader, H., Rowe, K. M., Day, C. W., et al. (2012) · Cell stem cell · doi:10.1016/j.stem.2012.02.007 · Cited by 322 · see citing works
PIK3CAH1047R induces multipotency and multi-lineage mammary tumours
Koren, S., Reavie, L. B., Couto, J. P., Silva, D. D., Stadler, M. B., Roloff, T. C., Britschgi, A., Eichlisberger, T., Kohler, H., Aina, O. H., et al. (2015) · Nature · doi:10.1038/nature14669 · Cited by 328 · see citing works
The Epidermis Comprises Autonomous Compartments Maintained by Distinct Stem Cell Populations
Page, M. E., Lombard, P., Ng, F., Göttgens, B., & Jensen, K. B. (2013) · Cell Stem Cell · doi:10.1016/j.stem.2013.07.010 · Cited by 320 · see citing works
Phenotypic and functional characterisation of the luminal cell hierarchy of the mammary gland
Shehata, M., Teschendorff, A., Sharp, G., Novcic, N., Russell, I. A., Avril, S., Prater, M., Eirew, P., Caldas, C., Watson, C. J., et al. (2012) · Breast Cancer Research · doi:10.1186/bcr3334 · Cited by 306 · see citing works
Wang, Z. A., Mitrofanova, A., Bergren, S. K., Abate-Shen, C. T., Cardiff, R. D., Califano, A., & Shen, M. M. (2013) · Nature Cell Biology · doi:10.1038/ncb2697 · Cited by 305 · see citing works
Lu, C. P., Polak, L., Rocha, A. S., Pasolli, H. A., Chen, S.-C., Sharma, N., Blanpain, C., & Fuchs, E. (2012) · Cell · doi:10.1016/j.cell.2012.04.045 · Cited by 301 · see citing works
“Moreover, in similar transplantation experiments performed with purified adult mammary myoepithelial cells, the frequency of lumenal differentiation declined when the engraftment mixture was spiked with increasing numbers of unmarked lumenal cells (Van Keymeulen et al., 2011).”
BackgroundResultInfluentialSelf-citationIL-6/STAT3 promotes regeneration of airway ciliated cells from basal stem cells
Tadokoro, T., Wang, Y., Barak, L. S., Bai, Y., Randell, S. H., & Hogan, B. L. M. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1409781111 · Cited by 288 · see citing works
Regenerative potential of prostate luminal cells revealed by single-cell analysis
Karthaus, W. R., Hofree, M., Choi, D., Linton, E. L., Turkekul, M., Bejnood, A., Carver, B., Gopalan, A., Abida, W. M., Laudone, V. P., et al. (2020) · Science · doi:10.1126/science.aay0267 · Cited by 286 · see citing works
Breast Tumor Heterogeneity: Source of Fitness, Hurdle for Therapy
Koren, S., & Bentires‐Alj, M. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.10.031 · Cited by 280 · see citing works
Unravelling stem cell dynamics by lineage tracing
Blanpain, C., & Simons, B. D. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3625 · Cited by 273 · see citing works
Self-citationTracing the cellular origin of cancer
Blanpain, C. (2013) · Nature Cell Biology · doi:10.1038/ncb2657 · Cited by 275 · see citing works
Self-citationLocal lung hypoxia determines epithelial fate decisions during alveolar regeneration
Xi, Y., Kim, T., Brumwell, A. N., Driver, I. H., Wei, Y., Tan, V. M., Jackson, J., Xu, J., Lee, D.-K., Gotts, J. E., et al. (2017) · Nature Cell Biology · doi:10.1038/ncb3580 · Cited by 268 · see citing works
Stem Cells and the Differentiation Hierarchy in Mammary Gland Development
Fu, N. Y., Nolan, E., Lindeman, G. J., & Visvader, J. E. (2019) · Physiological Reviews · doi:10.1152/physrev.00040.2018 · Cited by 262 · see citing works
Proliferation tracing reveals regional hepatocyte generation in liver homeostasis and repair
He, L., Pu, W., Liu, X., Zhang, Z., Han, M., Li, Y., Huang, X., Han, X., Li, Y., Liu, K., et al. (2021) · Science · doi:10.1126/science.abc4346 · Cited by 261 · see citing works
Panciera, T., Azzolin, L., Fujimura, A., Biagio, D. D., Frasson, C., Bresolin, S., Soligo, S., Basso, G., Bicciato, S., Rosato, A., et al. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.08.009 · Cited by 255 · see citing works
Anatomy of the human mammary gland: Current status of knowledge
Hassiotou, F., & Geddes, D. T. (2012) · Clinical Anatomy · doi:10.1002/ca.22165 · Cited by 260 · see citing works
Progesterone signalling in breast cancer: a neglected hormone coming into the limelight
Brisken, C. (2013) · Nature reviews. Cancer · doi:10.1038/nrc3518 · Cited by 255 · see citing works
Building and maintaining the epithelium of the lung
Rackley, C. R., & Stripp, B. R. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60519 · Cited by 250 · see citing works
Pericytes at the intersection between tissue regeneration and pathology: Figure 1
Birbrair, A., Zhang, T., Wang, Z., Messi, M. L., Mintz, A., & Delbono, O. (2014) · Clinical Science · doi:10.1042/cs20140278 · Cited by 243 · see citing works
L1CAM defines the regenerative origin of metastasis-initiating cells in colorectal cancer
Ganesh, K., Basnet, H., Kaygusuz, Y., Laughney, A. M., He, L., Sharma, R., O’Rourke, K. P., Reuter, V. P., Huang, Y.-H., Turkekul, M., et al. (2020) · Nature Cancer · doi:10.1038/s43018-019-0006-x · Cited by 245 · see citing works
Mammary stem cells have myoepithelial cell properties
Prater, M. D., Petit, V., Russell, I. A., Giraddi, R. R., Shehata, M., Menon, S., Schulte, R., Kalajzić, I., Rath, N., Olson, M. F., et al. (2014) · Nature Cell Biology · doi:10.1038/ncb3025 · Cited by 237 · see citing works
Spike, B. T., Engle, D. D., Lin, J., Cheung, S. K., La, J., & Wahl, G. M. (2012) · Cell stem cell · doi:10.1016/j.stem.2011.12.018 · Cited by 240 · see citing works
Defining Adult Stem Cells by Function, not by Phenotype
Clevers, H. C., & Watt, F. M. (2018) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-062917-012341 · Cited by 226 · see citing works
Multipotent and unipotent progenitors contribute to prostate postnatal development
Ousset, M., Van Keymeulen, A., Bouvencourt, G., Sharma, N., Achouri, Y., Simons, B. D., & Blanpain, C. (2012) · Nature Cell Biology · doi:10.1038/ncb2600 · Cited by 221 · see citing works
Self-citationSchwab, L. P., Peacock, D. L., Majumdar, D., Ingels, J. F., Jensen, L. C., Smith, K., Cushing, R. C., & Seagroves, T. N. (2012) · Breast Cancer Research · doi:10.1186/bcr3087 · Cited by 220 · see citing works
Epigenetic control of adult stem cell function
Avgustinova, A., & Benitah, S. A. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.76 · Cited by 216 · see citing works
Adipose tissue plasticity from WAT to BAT and in between
Lee, Y., Mottillo, E. P., & Granneman, J. G. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.05.011 · Cited by 215 · see citing works
Zhao, R., Fallon, T. R., Saladi, S. V., Pardo–Saganta, A., Villoria, J., Mou, H., Vinarský, V., Gonzalez-Celeiro, M., Nunna, N., Hariri, L. P., et al. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.06.004 · Cited by 219 · see citing works
Luo, M., Brooks, M. D., & Wicha, M. S. (2015) · Current Pharmaceutical Design · doi:10.2174/1381612821666141211120604 · Cited by 217 · see citing works
Development of the Human Breast
Lteif, A. N., & Javed, A. (2013) · Seminars in Plastic Surgery · doi:10.1055/s-0033-1343989 · Cited by 215 · see citing works
Breast Cancer: A Molecularly Heterogenous Disease Needing Subtype-Specific Treatments
Testa, U., Castelli, G., & Pelosi, E. (2020) · Medical Sciences · doi:10.3390/medsci8010018 · Cited by 226 · see citing works
Progesterone/RANKL Is a Major Regulatory Axis in the Human Breast
Tanos, T., Sflomos, G., Echeverría, P. C., Ayyanan, A., Gutierrez, M., Delaloye, J.-F., Raffoul, W., Fiche, M., Dougall, W. C., Schneider, P., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005654 · Cited by 208 · see citing works
A matter of life and death: self‐renewal in stem cells
Fuchs, E. V., & Chen, T. (2012) · EMBO Reports · doi:10.1038/embor.2012.197 · Cited by 210 · see citing works
Genetic Lineage Tracing of Nonmyocyte Population by Dual Recombinases
Li, Y., He, L., Huang, X., Bhaloo, S. I., Zhao, H., Zhang, S., Pu, W., Tian, X., Liu, Q., Liu, Q., et al. (2018) · Circulation · doi:10.1161/circulationaha.118.034250 · Cited by 205 · see citing works
Lgr5-Expressing Cells Are Sufficient and Necessary for Postnatal Mammary Gland Organogenesis
Plaks, V., Brenot, A., Lawson, D. A., Linnemann, J. R., van Kappel, E. C., Wong, K., de Sauvage, F. J., Klein, O. D., & Werb, Z. (2013) · Cell Reports · doi:10.1016/j.celrep.2012.12.017 · Cited by 201 · see citing works
Regulators of genetic risk of breast cancer identified by integrative network analysis
Castro, M. A. A., de Santiago, I., Campbell, T. M., Vaughn, C. M., Hickey, T. E., Ross, E. M., Tilley, W. D., Markowetz, F. M., Ponder, B. A. J., & Meyer, K. B. (2015) · Nature Genetics · doi:10.1038/ng.3458 · Cited by 195 · see citing works
CD157 Marks Tissue-Resident Endothelial Stem Cells with Homeostatic and Regenerative Properties
Wakabayashi, T., Naito, H., Suehiro, J., Lin, Y., Kawaji, H., Iba, T., Kouno, T., Ishikawa-Kato, S., Furuno, M., Takara, K., et al. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.01.010 · Cited by 200 · see citing works
Clonal Dynamics Reveal Two Distinct Populations of Basal Cells in Slow-Turnover Airway Epithelium
Watson, J. K., Rulands, S., Wilkinson, A. C., Wuidart, A., Ousset, M., Keymeulen, A. V., Göttgens, B., Blanpain, C., Simons, B. D., & Rawlins, E. L. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.06.011 · Cited by 194 · see citing works
Self-citationIdentity and dynamics of mammary stem cells during branching morphogenesis
Scheele, C. L. G. J., Hannezo, É., Muraro, M. J., Zomer, A., Langedijk, N. S. M., van Oudenaarden, A., Simons, B. D., & van Rheenen, J. (2017) · Nature · doi:10.1038/nature21046 · Cited by 197 · see citing works
Notch 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
Parent stem cells can serve as niches for their daughter cells
Pardo–Saganta, A., Tata, P. R., Law, B. M., Sáez, B., Chow, R. D.-W., Prabhu, M., Gridley, T., & Rajagopal, J. (2015) · Nature · doi:10.1038/nature14553 · Cited by 194 · see citing works
Targeting Breast Cancer Stem Cells
Zhang, L., Chen, W.-M., Liu, S.-L., & Chen, C.-S. (2023) · International Journal on Biological Sciences · doi:10.7150/ijbs.76187 · Cited by 128 · see citing works
Watanabe, K., VILLARREAL-PONCE, A. P., Sun, P., Salmans, M., Fallahi, M., D, B. A. M., & Dai, X. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.03.006 · Cited by 182 · see citing works
Cellular Origin and Developmental Program of Coronary Angiogenesis
Tian, X., Pu, W. T., & Zhou, B. (2015) · Circulation Research · doi:10.1161/circresaha.116.305097 · Cited by 184 · see citing works
The Terminal End Bud: the Little Engine that Could
Paine, I. S., & Lewis, M. T. (2017) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-017-9372-0 · Cited by 184 · see citing works
Lv, C., Li, F., Li, X., Tian, Y., Zhang, Y., Sheng, X., Song, Y., Meng, Q., Yuan, S., Luan, L., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01059-5 · Cited by 182 · see citing works
Type-1 pericytes participate in fibrous tissue deposition in aged skeletal muscle
Birbrair, A., Zhang, T., Wang, Z.-M., Messi, M. L., Mintz, A., & Delbono, O. (2013) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00171.2013 · Cited by 177 · see citing works
The Deubiquitinase USP28 Stabilizes LSD1 and Confers Stem-Cell-like Traits to Breast Cancer Cells
Wu, Y., Wang, Y., Yang, X. H., Kang, T., Zhao, Y., Wang, C., Evers, B. M., & Zhou, B. P. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.08.030 · Cited by 171 · see citing works
Somatic stem cell heterogeneity: diversity in the blood, skin and intestinal stem cell compartments
Goodell, M., Nguyen, H., & Shroyer, N. (2015) · Nature reviews. Molecular cell biology · doi:10.1038/nrm3980 · Cited by 166 · see citing works
Stretching the limits: from homeostasis to stem cell plasticity in wound healing and cancer
Ge, Y., & Fuchs, E. (2018) · Nature reviews genetics · doi:10.1038/nrg.2018.9 · Cited by 160 · see citing works
Stem Cell Heterogeneity and Plasticity in Epithelia
Donati, G., & Watt, F. M. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.04.014 · Cited by 169 · see citing works
The origin of breast tumor heterogeneity
Skibinski, A., & Kuperwasser, C. (2015) · Oncogene · doi:10.1038/onc.2014.475 · Cited by 166 · see citing works
Giraddi, R. R., Chung, C., Heinz, R. E., Balcioglu, O., Novotny, M. A., Trejo, C. L., Dravis, C., Hagos, B. M., Mehrabad, E. M., Rodewald, L. W., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.07.025 · Cited by 166 · see citing works
A census of the lung: CellCards from LungMAP
Sun, X., Perl, A. T., Li, R., Bell, S. M., Sajti, E., Kalinichenko, V. V., Kalin, T. V., Misra, R. S., Deshmukh, H. S., Clair, G., et al. (2021) · Developmental Cell · doi:10.1016/j.devcel.2021.11.007 · Cited by 157 · see citing works
Yang, L., Tang, H., Kong, Y., Xie, X., Chen, J., Song, Y., 刘晓平, Ye, F., Li, N., Wang, N., et al. (2015) · Stem Cells · doi:10.1002/stem.2083 · Cited by 164 · see citing works
Quantitative lineage tracing strategies to resolve multipotency in tissue-specific stem cellsPreprint
Wuidart, A., Ousset, M., Rulands, S., Simons, B. D., Keymeulen, A. V., & Blanpain, C. (2016) · Genes & Development · doi:10.1101/gad.280057.116 · Cited by 161 · see citing works
Self-citationEarly lineage segregation of multipotent embryonic mammary gland progenitors
Wuidart, A., Sifrim, A., Fioramonti, M., Matsumura, S., Brisebarre, A., Brown, D. V., Centonze, A., Dannau, A., Dubois, C., Keymeulen, A. V., et al. (2018) · Nature Cell Biology · doi:10.1038/s41556-018-0095-2 · Cited by 160 · see citing works
Self-citationSkibinski, A., Breindel, J. L., Prat, A., Galván, P., Smith, E., Rolfs, A., Gupta, P. B., LaBaer, J., & Kuperwasser, C. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.02.038 · Cited by 159 · see citing works
Sweat Gland Progenitors in Development, Homeostasis, and Wound RepairPreprint
Lu, C. P.-J., & Fuchs, E. V. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a015222 · Cited by 156 · see citing works
de Visser, K. E., Ciampricotti, M., Michalak, E. M., Tan, D. W., Speksnijder, E. N., Hau, C., Clevers, H. C., Barker, N., & Jonkers, J. (2012) · The Journal of Pathology · doi:10.1002/path.4096 · Cited by 157 · see citing works
BCL11A is a triple-negative breast cancer gene with critical functions in stem and progenitor cells
Khaled, W. T., Lee, S. C., Stingl, J., Chen, X., Ali, H. R., Rueda, O. M., Hadi, F., Wang, J., Yu, Y., Chin, S., et al. (2015) · Nature Communications · doi:10.1038/ncomms6987 · Cited by 154 · see citing works
Tata, A., Kobayashi, Y., Chow, R. D.-W., Tran, J., Desai, A. P., Massri, A. J., McCord, T. J., Gunn, M. D., & Tata, P. R. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.03.018 · Cited by 152 · see citing works
Arterial Sca1+ Vascular Stem Cells Generate De Novo Smooth Muscle for Artery Repair and Regeneration
Tang, J., Wang, H., Huang, X., Li, F., Zhu, H., Li, Y., He, L., Zhang, H., Pu, W., Liu, K., et al. (2019) · Cell stem cell · doi:10.1016/j.stem.2019.11.010 · Cited by 151 · see citing works
Tissue-specific designs of stem cell hierarchies
Visvader, J. E., & Clevers, H. (2016) · Nature Cell Biology · doi:10.1038/ncb3332 · Cited by 150 · see citing works
Luminal Cells Are Favored as the Cell of Origin for Prostate Cancer
Wang, Z. A., Toivanen, R., Bergren, S. K., Chambon, P., & Shen, M. M. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.08.002 · Cited by 148 · see citing works
- Authors
- Van Keymeulen, A., Rocha, A. S., Ousset, M., Beck, B., Bouvencourt, G., Rock, J., Sharma, N., Dekoninck, S., & Blanpain, C.
- Affiliations
- Université Libre de Bruxelles (BE)
- Duke Medical Center (US)
- Corresponding author
- Blanpain, Cédric
- Venue
- Nature
- Published
- 2011-10-09
- Volume
- 479
- Issue
- 7372
- Pages
- 189-193
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W2082161467
- Cited by
- 854
- References
- 38
- Citations by year
- 2026: 24 · 2025: 38 · 2024: 41 · 2023: 44 · 2022: 30 · 2021: 55 · 2020: 62 · 2019: 51 · 2018: 73 · 2017: 55 · 2016: 54 · 2015: 91 · 2014: 83 · 2013: 81 · 2012: 68
- FWCI
- 36.95
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Dépôt institutionnel de l'Université libre de Bruxelles (Université Libre de Bruxelles) (submittedVersion)
- HAL (submittedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Topics
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
- Keywords
- mammary stem cells, mammary gland development, mammary epithelium, cellular hierarchy, lineage tracing, clonal expansion, multipotent stem cells, luminal cells, myoepithelial cells, alveolar cells, mammary gland morphogenesis, pregnancy, lactation
- MeSH terms
- Aging, Animals, Cell Differentiation, Epithelium, Female, Homeostasis, Lactation, Mammary Glands, Animal, Pregnancy, Stem Cells, Cell Transplantation, Cell Lineage, Multipotent Stem Cells, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
