TGF-β regulates Sca-1 expression and plasticity of pre-neoplastic mammary epithelial stem cells.
Animals
Ataxin-1
/ metabolism
Breast Neoplasms
/ genetics
Cell Line, Tumor
/ transplantation
Cell Plasticity
/ genetics
Epithelial Cells
/ pathology
Epithelial-Mesenchymal Transition
/ genetics
Female
Gene Expression Regulation, Neoplastic
Humans
Mammary Glands, Animal
/ pathology
Mammary Neoplasms, Experimental
/ genetics
Mice
Neoplastic Stem Cells
/ pathology
Receptor, ErbB-2
/ genetics
Recombinant Proteins
/ genetics
Signal Transduction
/ genetics
Transforming Growth Factor beta
/ genetics
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
09 07 2020
09 07 2020
Historique:
received:
18
10
2018
accepted:
15
06
2020
entrez:
11
7
2020
pubmed:
11
7
2020
medline:
22
12
2020
Statut:
epublish
Résumé
The epithelial-mesenchymal plasticity, in tight association with stemness, contributes to the mammary gland homeostasis, evolution of early neoplastic lesions and cancer dissemination. Focused on cell surfaceome, we used mouse models of pre-neoplastic mammary epithelial and cancer stem cells to reveal the connection between cell surface markers and distinct cell phenotypes. We mechanistically dissected the TGF-β family-driven regulation of Sca-1, one of the most commonly used adult stem cell markers. We further provided evidence that TGF-β disrupts the lineage commitment and promotes the accumulation of tumor-initiating cells in pre-neoplastic cells.
Identifiants
pubmed: 32647280
doi: 10.1038/s41598-020-67827-4
pii: 10.1038/s41598-020-67827-4
pmc: PMC7347574
doi:
Substances chimiques
Ataxin-1
0
Atxn1 protein, mouse
0
Recombinant Proteins
0
Transforming Growth Factor beta
0
Erbb2 protein, mouse
EC 2.7.10.1
Receptor, ErbB-2
EC 2.7.10.1
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
11396Références
Biteau, B., Hochmuth, C. E. & Jasper, H. Maintaining tissue homeostasis: Dynamic control of somatic stem cell activity. Cell Stem Cell 9, 402–411. https://doi.org/10.1016/j.stem.2011.10.004 (2011).
doi: 10.1016/j.stem.2011.10.004
pubmed: 22056138
pmcid: 3212030
Giraddi, R. R. et al. Single-cell transcriptomes distinguish stem cell state changes and lineage specification programs in early mammary gland development. Cell Rep 24, 1653–1666 e1657. https://doi.org/10.1016/j.celrep.2018.07.025 (2018).
Davis, F. M. et al. Single-cell lineage tracing in the mammary gland reveals stochastic clonal dispersion of stem/progenitor cell progeny. Nat. Commun. 7, 13053. https://doi.org/10.1038/ncomms13053 (2016).
doi: 10.1038/ncomms13053
pubmed: 27779190
pmcid: 5093309
Breindel, J. L. et al. Epigenetic reprogramming of lineage-committed human mammary epithelial cells requires DNMT3A and loss of DOT1L. Stem Cell Rep. 9, 943–955. https://doi.org/10.1016/j.stemcr.2017.06.019 (2017).
doi: 10.1016/j.stemcr.2017.06.019
Friedmann-Morvinski, D. & Verma, I. M. Dedifferentiation and reprogramming: origins of cancer stem cells. EMBO Rep. 15, 244–253. https://doi.org/10.1002/embr.201338254 (2014).
doi: 10.1002/embr.201338254
pubmed: 24531722
pmcid: 3989690
Challen, G. A., Boles, N., Lin, K. K. & Goodell, M. A. Mouse hematopoietic stem cell identification and analysis. Cytometry A 75, 14–24. https://doi.org/10.1002/cyto.a.20674 (2009).
doi: 10.1002/cyto.a.20674
pubmed: 19023891
pmcid: 2640229
Welm, B. E. et al. Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev. Biol. 245, 42–56. https://doi.org/10.1006/dbio.2002.0625 (2002).
doi: 10.1006/dbio.2002.0625
pubmed: 11969254
Mulholland, D. J. et al. Lin-Sca-1+CD49fhigh stem/progenitors are tumor-initiating cells in the Pten-null prostate cancer model. Cancer Res. 69, 8555–8562. https://doi.org/10.1158/0008-5472.CAN-08-4673 (2009).
doi: 10.1158/0008-5472.CAN-08-4673
pubmed: 19887604
pmcid: 2783355
Grange, C., Lanzardo, S., Cavallo, F., Camussi, G. & Bussolati, B. SCA-1 identifies the tumor-initiating cells in mammary tumors of BALB-neuT transgenic mice. Neoplasia 10, 1433–1443. https://doi.org/10.1593/neo.08902 (2008).
doi: 10.1593/neo.08902
pubmed: 19048122
pmcid: 2586694
Ma, X., Ling, K. W. & Dzierzak, E. Cloning of the Ly-6A (Sca-1) gene locus and identification of a 3’ distal fragment responsible for high-level gamma-interferon-induced expression in vitro. Br. J. Haematol. 114, 724–730 (2001).
doi: 10.1046/j.1365-2141.2001.02986.x
Camarata, T. D., Weaver, G. C., Vasilyev, A. & Arnaout, M. A. Negative regulation of TGFbeta signaling by stem cell antigen-1 protects against ischemic acute kidney injury. PLoS ONE 10, e0129561. https://doi.org/10.1371/journal.pone.0129561 (2015).
doi: 10.1371/journal.pone.0129561
pubmed: 26053644
pmcid: 4460127
Upadhyay, G. et al. Stem cell antigen-1 enhances tumorigenicity by disruption of growth differentiation factor-10 (GDF10)-dependent TGF-beta signaling. Proc. Natl. Acad. Sci. USA 108, 7820–7825. https://doi.org/10.1073/pnas.1103441108 (2011).
doi: 10.1073/pnas.1103441108
pubmed: 21518866
Knutson, K. L. et al. Immunoediting of cancers may lead to epithelial to mesenchymal transition. J. Immunol. 177, 1526–1533. https://doi.org/10.4049/jimmunol.177.3.1526 (2006).
doi: 10.4049/jimmunol.177.3.1526
pubmed: 16849459
Penvose, A. & Westerman, K. A. Sca-1 is involved in the adhesion of myosphere cells to alphaVbeta3 integrin. Biol. Open 1, 839–847. https://doi.org/10.1242/bio.20121222 (2012).
doi: 10.1242/bio.20121222
pubmed: 23213478
pmcid: 3507234
Brill, B., Boecher, N., Groner, B. & Shemanko, C. S. A sparing procedure to clear the mouse mammary fat pad of epithelial components for transplantation analysis. Lab. Anim. 42, 104–110. https://doi.org/10.1258/la.2007.06003e (2008).
doi: 10.1258/la.2007.06003e
pubmed: 18348772
Remsik, J. et al. Plasticity and intratumoural heterogeneity of cell surface antigen expression in breast cancer. Br. J. Cancer https://doi.org/10.1038/bjc.2017.497 (2018).
doi: 10.1038/bjc.2017.497
pubmed: 29462126
pmcid: 5886127
Thompson, T. C., Southgate, J., Kitchener, G. & Land, H. Multistage carcinogenesis induced by ras and myc oncogenes in a reconstituted organ. Cell 56, 917–930 (1989).
doi: 10.1016/0092-8674(89)90625-9
Shaw, A., Papadopoulos, J., Johnson, C. & Bushman, W. Isolation and characterization of an immortalized mouse urogenital sinus mesenchyme cell line. Prostate 66, 1347–1358. https://doi.org/10.1002/pros.20357 (2006).
doi: 10.1002/pros.20357
pubmed: 16752376
pmcid: 2802279
Liao, C. et al. Mouse prostate cancer cell lines established from primary and post-castration recurrent tumors. Horm Cancer 1, 44–54 (2010).
doi: 10.1007/s12672-009-0005-y
Slabakova, E. et al. Opposite regulation of MDM2 and MDMX expression in acquisition of mesenchymal phenotype in benign and cancer cells. Oncotarget 6, 36156–36171. https://doi.org/10.18632/oncotarget.5392 (2015).
doi: 10.18632/oncotarget.5392
pubmed: 26416355
pmcid: 4742168
Dereeper, A. et al. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res 36, W465–469. https://doi.org/10.1093/nar/gkn180 (2008).
Kmieciak, M., Knutson, K. L., Dumur, C. I. & Manjili, M. H. HER-2/neu antigen loss and relapse of mammary carcinoma are actively induced by T cell-mediated anti-tumor immune responses. Eur. J. Immunol. 37, 675–685. https://doi.org/10.1002/eji.200636639 (2007).
doi: 10.1002/eji.200636639
pubmed: 17304628
pmcid: 3732067
Deugnier, M. A. et al. Isolation of mouse mammary epithelial progenitor cells with basal characteristics from the Comma-Dbeta cell line. Dev. Biol. 293, 414–425. https://doi.org/10.1016/j.ydbio.2006.02.007 (2006).
doi: 10.1016/j.ydbio.2006.02.007
pubmed: 16545360
Campbell, S. M., Taha, M. M., Medina, D. & Rosen, J. M. A clonal derivative of mammary epithelial cell line COMMA-D retains stem cell characteristics of unique morphological and functional heterogeneity. Exp. Cell Res. 177, 109–121. https://doi.org/10.1016/0014-4827(88)90029-8 (1988).
doi: 10.1016/0014-4827(88)90029-8
pubmed: 2455648
Guo, W. et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell 148, 1015–1028. https://doi.org/10.1016/j.cell.2012.02.008 (2012).
doi: 10.1016/j.cell.2012.02.008
pubmed: 22385965
pmcid: 3305806
Kouros-Mehr, H., Slorach, E. M., Sternlicht, M. D. & Werb, Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 127, 1041–1055. https://doi.org/10.1016/j.cell.2006.09.048 (2006).
doi: 10.1016/j.cell.2006.09.048
pubmed: 2646406
pmcid: 2646406
Barcellos-Hoff, M. H. & Ravani, S. A. Irradiated mammary gland stroma promotes the expression of tumorigenic potential by unirradiated epithelial cells. Cancer Res. 60, 1254–1260 (2000).
pubmed: 10728684
Moses, H. & Barcellos-Hoff, M. H. TGF-beta biology in mammary development and breast cancer. Cold Spring Harb. Perspect. Biol. 3, a003277. https://doi.org/10.1101/cshperspect.a003277 (2011).
doi: 10.1101/cshperspect.a003277
pubmed: 20810549
pmcid: 3003461
Bierie, B., Gorska, A. E., Stover, D. G. & Moses, H. L. TGF-beta promotes cell death and suppresses lactation during the second stage of mammary involution. J. Cell Physiol. 219, 57–68. https://doi.org/10.1002/jcp.21646 (2009).
doi: 10.1002/jcp.21646
pubmed: 19086032
pmcid: 3038423
Jerry, D. J., Medina, D. & Butel, J. S. p53 mutations in COMMA-D cells. Vitro Cell Dev. Biol. Anim. 30A, 87–89. https://doi.org/10.1007/bf02631398 (1994).
doi: 10.1007/bf02631398
Dunphy, K. A. et al. Oncogenic transformation of mammary epithelial cells by transforming growth factor beta independent of mammary stem cell regulation. Cancer Cell Int. 13, 74. https://doi.org/10.1186/1475-2867-13-74 (2013).
doi: 10.1186/1475-2867-13-74
pubmed: 23883065
pmcid: 3733955
Long, K., Montano, M. & Pavlath, G. Sca-1 is negatively regulated by TGF-β1 in myogenic cells. FASEB J. 25, 1156–1165 (2011).
doi: 10.1096/fj.10-170308