Visvader JE, Stingl J. Mammary stem cells and the differentiation hierarchy: current status and perspectives. Genes Dev. 2014;28:1143–58.
Article
PubMed
PubMed Central
CAS
Google Scholar
Macias H, Hinck L. Mammary gland development. Wiley Interdiscip Rev Dev Biol. 2012;1:533–57.
Article
PubMed
PubMed Central
CAS
Google Scholar
Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, Li HI, Eaves CJ. Purification and unique properties of mammary epithelial stem cells. Nature. 2006;439:993–7.
Article
PubMed
CAS
Google Scholar
Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. Generation of a functional mammary gland from a single stem cell. Nature. 2006;439:84–8.
Article
PubMed
CAS
Google Scholar
Wang D, Cai C, Dong X, Yu QC, Zhang XO, Yang L, Zeng YA. Identification of multipotent mammary stem cells by protein C receptor expression. Nature. 2015;517:81–4.
Article
PubMed
CAS
Google Scholar
Rios AC, Fu NY, Lindeman GJ, Visvader JE. In situ identification of bipotent stem cells in the mammary gland. Nature. 2014;506:322–7.
Article
PubMed
CAS
Google Scholar
Van Keymeulen A, Rocha AS, 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. 2011;479:189–93.
Article
PubMed
CAS
Google Scholar
van Amerongen R, Bowman AN, Nusse R. Developmental stage and time dictate the fate of Wnt/beta-catenin-responsive stem cells in the mammary gland. Cell Stem Cell. 2012;11:387–400.
Article
PubMed
CAS
Google Scholar
Prater MD, Petit V, Alasdair Russell I, Giraddi RR, Shehata M, Menon S, Schulte R, Kalajzic I, Rath N, Olson MF, et al. Mammary stem cells have myoepithelial cell properties. Nat Cell Biol. 2014;16:942–50. 941-947
Article
PubMed
PubMed Central
CAS
Google Scholar
Wuidart A, Ousset M, Rulands S, Simons BD, Van Keymeulen A, Blanpain C. Quantitative lineage tracing strategies to resolve multipotency in tissue-specific stem cells. Genes Dev. 2016;30:1261–77.
Article
PubMed
PubMed Central
CAS
Google Scholar
Galliot B, Ghila L. Cell plasticity in homeostasis and regeneration. Mol Reprod Dev. 2010;77:837–55.
Article
PubMed
CAS
Google Scholar
Chaffer CL, Marjanovic ND, Lee T, Bell G, Kleer CG, Reinhardt F, D'Alessio AC, Young RA, Weinberg RA. Poised chromatin at the ZEB1 promoter enables breast cancer cell plasticity and enhances tumorigenicity. Cell. 2013;154:61–74.
Article
PubMed
PubMed Central
CAS
Google Scholar
Holliday R, Pugh JE. DNA modification mechanisms and gene activity during development. Science. 1975;187:226–32.
Article
PubMed
CAS
Google Scholar
Smith ZD, Meissner A. DNA methylation: roles in mammalian development. Nat Rev Genet. 2013;14:204–20.
Article
PubMed
CAS
Google Scholar
Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997;389:251–60.
Article
PubMed
CAS
Google Scholar
Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21:381–95.
Article
PubMed
PubMed Central
CAS
Google Scholar
Skulte KA, Phan L, Clark SJ, Taberlay PC. Chromatin remodeler mutations in human cancers: epigenetic implications. Epigenomics. 2014;6:397–414.
Article
PubMed
CAS
Google Scholar
Liang G, Zhang Y. Embryonic stem cell and induced pluripotent stem cell: an epigenetic perspective. Cell Res. 2013;23:49–69.
Article
PubMed
CAS
Google Scholar
Sharma S, Gurudutta G. Epigenetic regulation of hematopoietic stem cells. Int J Stem Cells. 2016;9:36–43.
Article
PubMed
PubMed Central
CAS
Google Scholar
Sharma S, Kelly TK, Jones PA. Epigenetics in cancer. Carcinogenesis. 2010;31:27–36.
Article
PubMed
CAS
Google Scholar
Bestor TH. The DNA methyltransferases of mammals. Hum Mol Genet. 2000;9:2395–402.
Article
PubMed
CAS
Google Scholar
Laurent L, Wong E, Li G, Huynh T, Tsirigos A, Ong CT, Low HM, Kin Sung KW, Rigoutsos I, Loring J, et al. Dynamic changes in the human methylome during differentiation. Genome Res. 2010;20:320–31.
Article
PubMed
PubMed Central
CAS
Google Scholar
Huang K, Fan G. DNA methylation in cell differentiation and reprogramming: an emerging systematic view. Regen Med. 2010;5:531–44.
Article
PubMed
CAS
Google Scholar
Bogdanovic O. Tet proteins: master regulators of vertebrate body plan formation? Epigenomics. 2017;9:93–6.
Article
PubMed
CAS
Google Scholar
Huh SJ, Clement K, Jee D, Merlini A, Choudhury S, Maruyama R, Yoo R, Chytil A, Boyle P, Ran FA, et al. Age- and pregnancy-associated DNA methylation changes in mammary epithelial cells. Stem Cell Rep. 2015;4:297–311.
Article
CAS
Google Scholar
Dos Santos CO, Dolzhenko E, Hodges E, Smith AD, Hannon GJ. An epigenetic memory of pregnancy in the mouse mammary gland. Cell Rep. 2015;11:1102–9.
Article
PubMed
PubMed Central
CAS
Google Scholar
Bloushtain-Qimron N, Yao J, Snyder EL, Shipitsin M, Campbell LL, Mani SA, Hu M, Chen H, Ustyansky V, Antosiewicz JE, et al. Cell type-specific DNA methylation patterns in the human breast. Proc Natl Acad Sci U S A. 2008;105:14076–81.
Article
PubMed
PubMed Central
Google Scholar
Maruyama R, Choudhury S, Kowalczyk A, Bessarabova M, Beresford-Smith B, Conway T, Kaspi A, Wu Z, Nikolskaya T, Merino VF, et al. Epigenetic regulation of cell type-specific expression patterns in the human mammary epithelium. PLoS Genet. 2011;7:e1001369.
Article
PubMed
PubMed Central
CAS
Google Scholar
Gascard P, Bilenky M, Sigaroudinia M, Zhao J, Li L, Carles A, Delaney A, Tam A, Kamoh B, Cho S, et al. Epigenetic and transcriptional determinants of the human breast. Nat Commun. 2015;6:6351.
Article
PubMed
PubMed Central
CAS
Google Scholar
Lee HJ, Hinshelwood RA, Bouras T, Gallego-Ortega D, Valdes-Mora F, Blazek K, Visvader JE, Clark SJ, Ormandy CJ. Lineage specific methylation of the Elf5 promoter in mammary epithelial cells. Stem Cells. 2011;29:1611–9.
Article
PubMed
CAS
Google Scholar
Berdasco M, Esteller M. DNA methylation in stem cell renewal and multipotency. Stem Cell Res Ther. 2011;2:42.
Article
PubMed
PubMed Central
CAS
Google Scholar
Britt K, Ashworth A, Smalley M. Pregnancy and the risk of breast cancer. Endocr Relat Cancer. 2007;14:907–33.
Article
PubMed
CAS
Google Scholar
Pathania R, Ramachandran S, Elangovan S, Padia R, Yang P, Cinghu S, Veeranan-Karmegam R, Arjunan P, Gnana-Prakasam JP, Sadanand F, et al. DNMT1 is essential for mammary and cancer stem cell maintenance and tumorigenesis. Nat Commun. 2015;6:6910.
Article
PubMed
PubMed Central
CAS
Google Scholar
Hebbes TR, Thorne AW, Crane-Robinson C. A direct link between core histone acetylation and transcriptionally active chromatin. EMBO J. 1988;7:1395–402.
Article
PubMed
PubMed Central
CAS
Google Scholar
Liang G, Lin JC, Wei V, Yoo C, Cheng JC, Nguyen CT, Weisenberger DJ, Egger G, Takai D, Gonzales FA, et al. Distinct localization of histone H3 acetylation and H3-K4 methylation to the transcription start sites in the human genome. Proc Natl Acad Sci U S A. 2004;101:7357–62.
Article
PubMed
PubMed Central
CAS
Google Scholar
Black JC, Van Rechem C, Whetstine JR. Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol Cell. 2012;48:491–507.
Article
PubMed
CAS
Google Scholar
Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125:315–26.
Article
PubMed
CAS
Google Scholar
Calo E, Wysocka J. Modification of enhancer chromatin: what, how, and why? Mol Cell. 2013;49:825–37.
Article
PubMed
CAS
Google Scholar
Pal B, Bouras T, Shi W, Vaillant F, Sheridan JM, Fu N, Breslin K, Jiang K, Ritchie ME, Young M, et al. Global changes in the mammary epigenome are induced by hormonal cues and coordinated by Ezh2. Cell Rep. 2013;3:411–26.
Article
PubMed
CAS
Google Scholar
Pellacani D, Bilenky M, Kannan N, Heravi-Moussavi A, Knapp DJ, Gakkhar S, Moksa M, Carles A, Moore R, Mungall AJ, et al. Analysis of normal human mammary epigenomes reveals cell-specific active enhancer states and associated transcription factor networks. Cell Rep. 2016;17:2060–74.
Article
PubMed
CAS
Google Scholar
Locke WJ, Zotenko E, Stirzaker C, Robinson MD, Hinshelwood RA, Stone A, Reddel RR, Huschtscha LI, Clark SJ. Coordinated epigenetic remodelling of transcriptional networks occurs during early breast carcinogenesis. Clin Epigenetics. 2015;7:52.
Article
PubMed
PubMed Central
CAS
Google Scholar
Lim E, Wu D, Pal B, Bouras T, Asselin-Labat ML, Vaillant F, Yagita H, Lindeman GJ, Smyth GK, Visvader JE. Transcriptome analyses of mouse and human mammary cell subpopulations reveal multiple conserved genes and pathways. Breast Cancer Res. 2010;12:R21.
Article
PubMed
PubMed Central
CAS
Google Scholar
Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, Asselin-Labat ML, Gyorki DE, Ward T, Partanen A, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med. 2009;15:907–13.
Article
PubMed
CAS
Google Scholar
Fu NY, Rios AC, Pal B, Law CW, Jamieson P, Liu R, Vaillant F, Jackling F, Liu KH, Smyth GK, et al. Identification of quiescent and spatially restricted mammary stem cells that are hormone responsive. Nat Cell Biol. 2017;19:164–76.
Article
PubMed
CAS
Google Scholar
Sauvageau M, Sauvageau G. Polycomb group proteins: multi-faceted regulators of somatic stem cells and cancer. Cell Stem Cell. 2010;7:299–313.
Article
PubMed
PubMed Central
CAS
Google Scholar
van Kruijsbergen I, Hontelez S, Veenstra GJ. Recruiting polycomb to chromatin. Int J Biochem Cell Biol. 2015;67:177–87.
Article
PubMed
PubMed Central
CAS
Google Scholar
Schwartz YB, Pirrotta V. A new world of Polycombs: unexpected partnerships and emerging functions. Nat Rev Genet. 2013;14:853–64.
Article
PubMed
CAS
Google Scholar
Zhou W, Zhu P, Wang J, Pascual G, Ohgi KA, Lozach J, Glass CK, Rosenfeld MG. Histone H2A monoubiquitination represses transcription by inhibiting RNA polymerase II transcriptional elongation. Mol Cell. 2008;29:69–80.
Article
PubMed
PubMed Central
CAS
Google Scholar
Li X, Gonzalez ME, Toy K, Filzen T, Merajver SD, Kleer CG. Targeted overexpression of EZH2 in the mammary gland disrupts ductal morphogenesis and causes epithelial hyperplasia. Am J Pathol. 2009;175:1246–54.
Article
PubMed
PubMed Central
CAS
Google Scholar
Michalak EM, Nacerddine K, Pietersen A, Beuger V, Pawlitzky I, Cornelissen-Steijger P, Wientjens E, Tanger E, Seibler J, van Lohuizen M, et al. Polycomb group gene Ezh2 regulates mammary gland morphogenesis and maintains the luminal progenitor pool. Stem Cells. 2013;31:1910–20.
Article
PubMed
CAS
Google Scholar
Yoo KH, Oh S, Kang K, Hensel T, Robinson GW, Hennighausen L. Loss of EZH2 results in precocious mammary gland development and activation of STAT5-dependent genes. Nucleic Acids Res. 2015;43:8774–89.
Article
PubMed
PubMed Central
CAS
Google Scholar
Pietersen AM, Evers B, Prasad AA, Tanger E, Cornelissen-Steijger P, Jonkers J, van Lohuizen M. Bmi1 regulates stem cells and proliferation and differentiation of committed cells in mammary epithelium. Curr Biol. 2008;18:1094–9.
Article
PubMed
CAS
Google Scholar
Liu S, Dontu G, Mantle ID, Patel S, Ahn NS, Jackson KW, Suri P, Wicha MS. Hedgehog signaling and Bmi-1 regulate self-renewal of normal and malignant human mammary stem cells. Cancer Res. 2006;66:6063–71.
Article
PubMed
PubMed Central
CAS
Google Scholar
Nottke A, Colaiacovo MP, Shi Y. Developmental roles of the histone lysine demethylases. Development. 2009;136:879–89.
Article
PubMed
PubMed Central
CAS
Google Scholar
Yamane K, Tateishi K, Klose RJ, Fang J, Fabrizio LA, Erdjument-Bromage H, Taylor-Papadimitriou J, Tempst P, Zhang Y. PLU-1 is an H3K4 demethylase involved in transcriptional repression and breast cancer cell proliferation. Mol Cell. 2007;25:801–12.
Article
PubMed
CAS
Google Scholar
Scibetta AG, Santangelo S, Coleman J, Hall D, Chaplin T, Copier J, Catchpole S, Burchell J, Taylor-Papadimitriou J. Functional analysis of the transcription repressor PLU-1/JARID1B. Mol Cell Biol. 2007;27:7220–35.
Article
PubMed
PubMed Central
CAS
Google Scholar
Catchpole S, Spencer-Dene B, Hall D, Santangelo S, Rosewell I, Guenatri M, Beatson R, Scibetta AG, Burchell JM, Taylor-Papadimitriou J. PLU-1/JARID1B/KDM5B is required for embryonic survival and contributes to cell proliferation in the mammary gland and in ER+ breast cancer cells. Int J Oncol. 2011;38:1267–77.
PubMed
CAS
Google Scholar
Zou MR, Cao J, Liu Z, Huh SJ, 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. 2014;289:17620–33.
Article
PubMed
PubMed Central
CAS
Google Scholar
Yamamoto S, Wu Z, Russnes HG, Takagi S, Peluffo G, Vaske C, Zhao X, Moen Vollan HK, Maruyama R, Ekram MB, et al. JARID1B is a luminal lineage-driving oncogene in breast cancer. Cancer Cell. 2014;25:762–77.
Article
PubMed
PubMed Central
CAS
Google Scholar
Klein BJ, Piao L, Xi Y, Rincon-Arano H, Rothbart SB, Peng D, Wen H, Larson C, Zhang X, Zheng X, et al. The histone-H3K4-specific demethylase KDM5B binds to its substrate and product through distinct PHD fingers. Cell Rep. 2014;6:325–35.
Article
PubMed
PubMed Central
CAS
Google Scholar
Kawazu M, Saso K, Tong KI, McQuire T, Goto K, Son DO, Wakeham A, Miyagishi M, Mak TW, Okada H. Histone demethylase JMJD2B functions as a co-factor of estrogen receptor in breast cancer proliferation and mammary gland development. PLoS One. 2011;6:e17830.
Article
PubMed
PubMed Central
CAS
Google Scholar
Yoo KH, Oh S, Kang K, Wang C, Robinson GW, Ge K, Hennighausen L. Histone demethylase KDM6A controls the mammary luminal lineage through enzyme-independent mechanisms. Mol Cell Biol. 2016;36:2108–20.
Article
PubMed
PubMed Central
CAS
Google Scholar
Belenkaya TY, Han C, Standley HJ, Lin X, Houston DW, Heasman J, Lin X. Pygopus encodes a nuclear protein essential for wingless/Wnt signaling. Development. 2002;129:4089–101.
PubMed
CAS
Google Scholar
Gu B, Sun P, Yuan Y, Moraes RC, Li A, Teng A, Agrawal A, Rheaume C, Bilanchone V, Veltmaat JM, et al. Pygo2 expands mammary progenitor cells by facilitating histone H3 K4 methylation. J Cell Biol. 2009;185:811–26.
Article
PubMed
PubMed Central
CAS
Google Scholar
Gu B, Watanabe K, Sun P, Fallahi M, Dai X. Chromatin effector Pygo2 mediates Wnt-notch crosstalk to suppress luminal/alveolar potential of mammary stem and basal cells. Cell Stem Cell. 2013;13:48–61.
Article
PubMed
PubMed Central
CAS
Google Scholar
Bouras T, Pal B, Vaillant F, Harburg G, Asselin-Labat ML, Oakes SR, Lindeman GJ, Visvader JE. Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell. 2008;3:429–41.
Article
PubMed
CAS
Google Scholar
Visvader JE. Cells of origin in cancer. Nature. 2011;469:314–22.
Article
PubMed
CAS
Google Scholar
Locke WJ, Clark SJ. Epigenome remodelling in breast cancer: insights from an early in vitro model of carcinogenesis. Breast Cancer Res. 2012;14:215.
Article
PubMed
PubMed Central
Google Scholar
Robertson KD. DNA methylation and human disease. Nat Rev Genet. 2005;6:597–610.
Article
PubMed
CAS
Google Scholar
Jones PA, Issa JP, Baylin S. Targeting the cancer epigenome for therapy. Nat Rev Genet. 2016;17:630–41.
Article
PubMed
CAS
Google Scholar
Pathania R, Ramachandran S, Mariappan G, Thakur P, Shi H, Choi JH, Manicassamy S, Kolhe R, Prasad PD, Sharma S, et al. Combined inhibition of DNMT and HDAC blocks the tumorigenicity of cancer stem-like cells and attenuates mammary tumor growth. Cancer Res. 2016;76:3224–35.
Article
PubMed
PubMed Central
CAS
Google Scholar
Kleer CG, Cao Q, Varambally S, Shen R, Ota I, Tomlins SA, Ghosh D, Sewalt RG, Otte AP, Hayes DF, et al. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci U S A. 2003;100:11606–11.
Article
PubMed
PubMed Central
CAS
Google Scholar
Guo BH, Feng Y, Zhang R, Xu LH, Li MZ, Kung HF, Song LB, Zeng MS. Bmi-1 promotes invasion and metastasis, and its elevated expression is correlated with an advanced stage of breast cancer. Mol Cancer. 2011;10:10.
Article
PubMed
PubMed Central
CAS
Google Scholar
Paranjape AN, Balaji SA, Mandal T, Krushik EV, Nagaraj P, Mukherjee G, Rangarajan A. Bmi1 regulates self-renewal and epithelial to mesenchymal transition in breast cancer cells through Nanog. BMC Cancer. 2014;14:785.
Article
PubMed
PubMed Central
CAS
Google Scholar
Noguchi-Yachide T. BET bromodomain as a target of epigenetic therapy. Chem Pharm Bull. 2016;64:540–7.
Article
PubMed
CAS
Google Scholar
Nagarajan S, Bedi U, Budida A, Hamdan FH, Mishra VK, Najafova Z, Xie W, Alawi M, Indenbirken D, Knapp S, et al. BRD4 promotes p63 and GRHL3 expression downstream of FOXO in mammary epithelial cells. Nucleic Acids Res. 2016;45:3130–45
Shu S, Lin CY, He HH, Witwicki RM, Tabassum DP, Roberts JM, Janiszewska M, Huh SJ, Liang Y, Ryan J, et al. Response and resistance to BET bromodomain inhibitors in triple-negative breast cancer. Nature. 2016;529:413–7.
Article
PubMed
PubMed Central
CAS
Google Scholar
Soysal SD, Tzankov A, Muenst SE. Role of the tumor microenvironment in breast cancer. Pathobiology. 2015;82:142–52.
Article
PubMed
CAS
Google Scholar
Dunn J, Rao S. Epigenetics and immunotherapy: the current state of play. Mol Immunol. 2017;87:227–39.
Article
PubMed
CAS
Google Scholar
Emens LA. Breast cancer immunotherapy: facts and hopes. Clin Cancer Res. 2018;24:511–20.
Article
PubMed
CAS
Google Scholar
Bach K, Pensa S, Grzelak M, Hadfield J, Adams DJ, Marioni JC, Khaled WT. Differentiation dynamics of mammary epithelial cells revealed by single-cell RNA sequencing. Nat Commun. 2017;8:2128.
Article
PubMed
PubMed Central
CAS
Google Scholar
Clark SJ, Lee HJ, Smallwood SA, Kelsey G, Reik W. Single-cell epigenomics: powerful new methods for understanding gene regulation and cell identity. Genome Biol. 2016;17:72.
Article
PubMed
PubMed Central
CAS
Google Scholar