BPTF Maintains Chromatin Accessibility and the Self-Renewal Capacity of Mammary Gland Stem Cells

Stem Cell Reports

Volumn 9, Issue 1, 2017, Pages 23-31

  Frey, Wesley D ^a   Chaudhry, Anisha ^a   Slepicka, Priscila F ^a   Ouellette, Adam M ^a   Kirberger, Steven E ^b   Pomerantz, William C K ^b   Hannon, Gregory J ^c   dos Santos, Camila O ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

BPTF; chromatin remodeling; enhancer landscape; gene regulation; mammary gland development; mammary stem cells

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; BRD4 PROTEIN; BSX PROTEIN; CHD1 PROTEIN; CHD4 PROTEIN; CYTOKERATIN 18; CYTOKERATIN 5; CYTOKERATIN 8; DNA; JHDM1D PROTEIN; JMJD1C PROTEIN; KCNQ1OT1 PROTEIN; MESSENGER RNA; MLL1 PROTEIN; MLL3 PROTEIN; MLL5 PROTEIN; PEPTIDES AND PROTEINS; PHF2 PROTEIN; PRKCD PROTEIN; PRMD2 PROTEIN; PROTEIN; SATB1 PROTEIN; SETD2 PROTEIN; SETD7 PROTEIN; SMARCA5 PROTEIN; SOMATOMEDIN C; TAF1 PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BPTF; UNCLASSIFIED DRUG; CELL NUCLEUS ANTIGEN; FETAL ALZHEIMER ANTIGEN; NERVE PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BREAST CELL; BREAST DEVELOPMENT; BREAST EPITHELIUM; BREAST EPITHELIUM CELL; CELL CYCLE ARREST; CELL DIFFERENTIATION; CELL FATE; CELL SURVIVAL; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DOWN REGULATION; ENHANCER REGION; EPIGENETICS; FEMALE; GENE EXPRESSION REGULATION; GENE REPRESSION; GENOME-WIDE ASSOCIATION STUDY; MAMMARY GLAND STEM CELL; MOUSE; MYOEPITHELIUM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; STEM CELL; STEM CELL SELF-RENEWAL; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; EPITHELIUM CELL; GENETIC EPIGENESIS; GENETICS; METABOLISM; UDDER;

ANIMALS; ANTIGENS, NUCLEAR; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; EPIGENESIS, GENETIC; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MAMMARY GLANDS, ANIMAL; NERVE TISSUE PROTEINS; STEM CELLS; TRANSCRIPTION FACTORS;

EID: 85020104077     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2017.04.031     Document Type: Article

References (28)

1. Asselin-Labat, M.L., Sutherland, K.D., Barker, H., Thomas, R., Shackleton, M., Forrest, N.C., Hartley, L., Robb, L., Grosveld, F.G., van der Wees, J., et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat. Cell Biol. 9 (2007), 201–209.
2. Chakrabarti, R., Wei, Y., Romano, R.A., DeCoste, C., Kang, Y., Sinha, S., Elf5 regulates mammary gland stem/progenitor cell fate by influencing notch signaling. Stem Cells 30 (2012), 1496–1508.
3. Chen, Y., Olopade, O.I., MYC in breast tumor progression. Expert Rev. Anticancer Ther. 8 (2008), 1689–1698.
4. dos Santos, C.O., Rebbeck, C., Rozhkova, E., Valentine, A., Samuels, A., Kadiri, L.R., Osten, P., Harris, E.Y., Uren, P.J., Smith, A.D., et al. Molecular hierarchy of mammary differentiation yields refined markers of mammary stem cells. Proc. Natl. Acad. Sci. USA 110 (2013), 7123–7130.
5. Dravis, C., Spike, B.T., Harrell, J.C., Johns, C., Trejo, C.L., Southard-Smith, E.M., Perou, C.M., Wahl, G.M., Sox10 regulates stem/progenitor and mesenchymal cell states in mammary epithelial cells. Cell Rep. 12 (2015), 2035–2048.
6. Goller, T., Vauti, F., Ramasamy, S., Arnold, H.H., Transcriptional regulator BPTF/FAC1 is essential for trophoblast differentiation during early mouse development. Mol. Cell. Biol. 28 (2008), 6819–6827.
7. Hesling, C., Fattet, L., Teyre, G., Jury, D., Gonzalo, P., Lopez, J., Vanbelle, C., Morel, A.P., Gillet, G., Mikaelian, I., et al. Antagonistic regulation of EMT by TIF1gamma and Smad4 in mammary epithelial cells. EMBO Rep. 12 (2011), 665–672.
8. Hynes, N.E., Stoelzle, T., Key signalling nodes in mammary gland development and cancer: Myc. Breast Cancer Res., 11, 2009, 210.
9. Indra, A.K., Warot, X., Brocard, J., Bornert, J.M., Xiao, J.H., Chambon, P., Metzger, D., Temporally-controlled site-specific mutagenesis in the basal layer of the epidermis: comparison of the recombinase activity of the tamoxifen-inducible Cre-ER(T) and Cre-ER(T2) recombinases. Nucleic Acids Res. 27 (1999), 4324–4327.
10. Koludrovic, D., Laurette, P., Strub, T., Keime, C., Le Coz, M., Coassolo, S., Mengus, G., Larue, L., Davidson, I., Chromatin-remodelling complex NURF is essential for differentiation of adult melanocyte stem cells. PLoS Genet., 11, 2015, e1005555.
11. Landry, J., Sharov, A.A., Piao, Y., Sharova, L.V., Xiao, H., Southon, E., Matta, J., Tessarollo, L., Zhang, Y.E., Ko, M.S., et al. Essential role of chromatin remodeling protein Bptf in early mouse embryos and embryonic stem cells. PLoS Genet., 4, 2008, e1000241.
12. Landry, J.W., Banerjee, S., Taylor, B., Aplan, P.D., Singer, A., Wu, C., Chromatin remodeling complex NURF regulates thymocyte maturation. Genes Dev. 25 (2011), 275–286.
13. Li, H., Ilin, S., Wang, W., Duncan, E.M., Wysocka, J., Allis, C.D., Patel, D.J., Molecular basis for site-specific read-out of histone H3K4me3 by the BPTF PHD finger of NURF. Nature 442 (2006), 91–95.
14. Li, X., Gonzalez, M.E., Toy, K., Filzen, T., Merajver, S.D., Kleer, C.G., Targeted overexpression of EZH2 in the mammary gland disrupts ductal morphogenesis and causes epithelial hyperplasia. Am. J. Pathol. 175 (2009), 1246–1254.
15. Pal, B., Bouras, T., Shi, W., Vaillant, F., Sheridan, J.M., Fu, N., Breslin, K., Jiang, K., Ritchie, M.E., Young, M., et al. Global changes in the mammary epigenome are induced by hormonal cues and coordinated by Ezh2. Cell Rep 3 (2013), 411–426.
16. Pinkas, J., Leder, P., MEK1 signaling mediates transformation and metastasis of EpH4 mammary epithelial cells independent of an epithelial to mesenchymal transition. Cancer Res. 62 (2002), 4781–4790.
17. Richart, L., Carrillo-de Santa Pau, E., Rio-Machin, A., de Andres, M.P., Cigudosa, J.C., Lobo, V.J., Real, F.X., BPTF is required for c-MYC transcriptional activity and in vivo tumorigenesis. Nat. Commun., 7, 2016, 10153.
18. Rios, A.C., Fu, N.Y., Lindeman, G.J., Visvader, J.E., In situ identification of bipotent stem cells in the mammary gland. Nature 506 (2014), 322–327.
19. Rodilla, V., Dasti, A., Huyghe, M., Lafkas, D., Laurent, C., Reyal, F., Fre, S., Luminal progenitors restrict their lineage potential during mammary gland development. PLoS Biol., 13, 2015, e1002069.
20. Ruthenburg, A.J., Li, H., Milne, T.A., Dewell, S., McGinty, R.K., Yuen, M., Ueberheide, B., Dou, Y., Muir, T.W., Patel, D.J., et al. Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions. Cell 145 (2011), 692–706.
21. Schedin, P., Keely, P.J., Mammary gland ECM remodeling, stiffness, and mechanosignaling in normal development and tumor progression. Cold Spring Harb. Perspect. Biol., 3, 2011, a003228.
22. Shi, P., Feng, J., Chen, C., Hippo pathway in mammary gland development and breast cancer. Acta Biochim. Biophys. Sin. 47 (2015), 53–59.
23. Urick, A.K., Hawk, L.M., Cassel, M.K., Mishra, N.K., Liu, S., Adhikari, N., Zhang, W., Dos Santos, C.O., Hall, J.L., Pomerantz, W.C., Dual screening of BPTF and Brd4 using protein-observed fluorine NMR uncovers new bromodomain probe molecules. ACS Chem. Biol. 10 (2015), 2246–2256.
24. van Bragt, M.P., Hu, X., Xie, Y., Li, Z., RUNX1, a transcription factor mutated in breast cancer, controls the fate of ER-positive mammary luminal cells. eLife, 3, 2014, e03881.
25. Van Keymeulen, A., Rocha, A.S., Ousset, M., Beck, B., Bouvencourt, G., Rock, J., Sharma, N., Dekoninck, S., Blanpain, C., Distinct stem cells contribute to mammary gland development and maintenance. Nature 479 (2011), 189–193.
26. Yamaji, D., Na, R., Feuermann, Y., Pechhold, S., Chen, W., Robinson, G.W., Hennighausen, L., Development of mammary luminal progenitor cells is controlled by the transcription factor STAT5A. Genes Dev. 23 (2009), 2382–2387.
27. Zhao, M., Shirley, C.R., Hayashi, S., Marcon, L., Mohapatra, B., Suganuma, R., Behringer, R.R., Boissonneault, G., Yanagimachi, R., Meistrich, M.L., Transition nuclear proteins are required for normal chromatin condensation and functional sperm development. Genesis 38 (2004), 200–213.
28. Zou, M.R., Cao, J., Liu, Z., Huh, S.J., Polyak, K., Yan, Q., Histone demethylase jumonji AT-rich interactive domain 1B (JARID1B) controls mammary gland development by regulating key developmental and lineage specification genes. J. Biol. Chem. 289 (2014), 17620–17633.