Abstract
Pioneered by the classical mouse embryonic stem cells (ESCs), various stem cell lines representing the peri- and postimplantation stages of embryogenesis have been established. To gain insight into the gene regulatory network operating in these cells, we first investigated epiblast stem cells (EpiSCs), performing ChIP-seq analysis for five major transcription factors (TFs) involved in epiblast regulation. The analysis indicated that SOX2-POU5F1 TF pairs highlighted in mouse ESCs are not the major players in other stem cells. The major acting transcription factors shift from SOX2/POU5F1 in mouse ESCs to ZIC2/OTX2 in EpiSCs, and this shift is primed in ESCs by binding of ZIC2 at relevant genomic positions that later function as enhancers.
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References
Aruga J (2004) The role of Zic genes in neural development. Mol Cell Neurosci 26:205–221
Aruga J, Yokota N, Hashimoto M, Furuichi T, Fukuda M, Mikoshiba K (1994) A novel zinc finger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells. J Neurochem 63:1880–1890
Brons IG, Smithers LE, Trotter MW, Rugg-Gunn P, Sun B, Chuva de Sousa Lopes SM, Howlett SK, Clarkson A, Ahrlund-Richter L, Pedersen RA, Vallier L (2007) Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 448:191–195
Brown L, Brown S (2009) Zic2 is expressed in pluripotent cells in the blastocyst and adult brain expression overlaps with makers of neurogenesis. Gene Expr Patterns 9:43–49
Calo E, Wysocka J (2013) Modification of enhancer chromatin: what, how, and why? Mol Cell 49:825–837
Chen JR, Cheng JG, Shatzer T, Sewell L, Hernandez L, Stewart CL (2000) Leukemia inhibitory factor can substitute for nidatory estrogen and is essential to inducing a receptive uterus for implantation but is not essential for subsequent embryogenesis. Endocrinology 141:4365–4372
Chen X, Xu H, Yuan P et al (2008) Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133:1106–1117
Elms P, Scurry A, Davies J, Willoughby C, Hacker T, Bogani D, Arkell R (2004) Overlapping and distinct expression domains of Zic2 and Zic3 during mouse gastrulation. Gene Expr Patterns 4:505–511
Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–156
Factor DC, Corradin O, Zentner GE, Saiakhova A, Song L, Chenoweth JG, McKay RD, Crawford GE, Scacheri PC, Tesar PJ (2014) Epigenomic comparison reveals activation of “seed” enhancers during transition from naive to primed pluripotency. Cell Stem Cell 14:854–863
Hayashi K, Ohta H, Kurimoto K, Aramaki S, Saitou M (2011) Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 146:519–532
Inoue T, Ota M, Mikoshiba K, Aruga J (2007) Zic2 and Zic3 synergistically control neurulation and segmentation of paraxial mesoderm in mouse embryo. Dev Biol 306:669–684
Iwafuchi-Doi M, Matsuda K, Murakami K, Niwa H, Tesar PJ, Aruga J, Matsuo I, Kondoh H (2012) Transcriptional regulatory networks in epiblast cells and during anterior neural plate development as modeled in epiblast stem cells. Development 139:3926–3937
Lim LS, Loh YH, Zhang W, Li Y, Chen X, Wang Y, Bakre M, Ng HH, Stanton LW (2007) Zic3 is required for maintenance of pluripotency in embryonic stem cells. Mol Biol Cell 18:1348–1358
Lodato MA, Ng CW, Wamstad JA, Cheng AW, Thai KK, Fraenkel E, Jaenisch R, Boyer LA (2013) SOX2 co-occupies distal enhancer elements with distinct POU factors in ESCs and NPCs to specify cell state. PLoS Genet 9:e1003288
Luo Z, Gao X, Lin C, Smith ER, Marshall SA, Swanson SK, Florens L, Washburn MP, Shilatifard A (2015) Zic2 is an enhancer-binding factor required for embryonic stem cell specification. Mol Cell 57:685–694
Martin GR (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A 78:7634–7638
Matsuda K, Mikami T, Oki S, Iida H, Andrabi M, Boss J, Yamaguchi K, Shigenobu S, Kondoh H (2017) ChIP-seq analysis of genomic binding regions of five major transcription factors highlights a central role for ZIC2 in the mouse epiblast stem cell gene regulatory network. Development 144:1948–1958
Nagai T, Aruga J, Minowa O, Sugimoto T, Ohno Y, Noda T, Mikoshiba K (2000) Zic2 regulates the kinetics of neurulation. Proc Natl Acad Sci U S A 97:1618–1623
Nagy J, Gertsenstein M, Vintersten K, Behringer R (2003) Manipulating the mouse embryo: a lobaoratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
Ong CT, Corces VG (2012) Enhancers: emerging roles in cell fate specification. EMBO Rep 13:423–430
Robertson EJ (1987) Teratocarcinomas and embryonic stem cells: a practical approach. IRL Press, Oxford
Shen MM (2007) Nodal signaling: developmental roles and regulation. Development 134:1023–1034
Sumi T, Oki S, Kitajima K, Meno C (2013) Epiblast ground state is controlled by canonical Wnt/beta-catenin signaling in the postimplantation mouse embryo and epiblast stem cells. PLoS One 8:e63378
Tesar PJ, Chenoweth JG, Brook FA, Davies TJ, Evans EP, Mack DL, Gardner RL, McKay RD (2007) New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 448:196–199
Vallier L, Mendjan S, Brown S, Chng Z, Teo A, Smithers LE, Trotter MW, Cho CH, Martinez A, Rugg-Gunn P, Brons G, Pedersen RA (2009) Activin/Nodal signalling maintains pluripotency by controlling Nanog expression. Development 136:1339–1349
Ware SM, Harutyunyan KG, Belmont JW (2006) Zic3 is critical for early embryonic patterning during gastrulation. Dev Dyn 235:776–785
Warr N, Powles-Glover N, Chappell A, Robson J, Norris D, Arkell RM (2008) Zic2-associated holoprosencephaly is caused by a transient defect in the organizer region during gastrulation. Hum Mol Genet 17:2986–2996
Yang SH, Kalkan T, Morissroe C, Marks H, Stunnenberg H, Smith A, Sharrocks AD (2014) Otx2 and Oct4 drive early enhancer activation during embryonic stem cell transition from naive pluripotency. Cell Rep 7:1968–1981
Zaret KS, Mango SE (2016) Pioneer transcription factors, chromatin dynamics, and cell fate control. Curr Opin Genet Dev 37:76–81
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This study was supported by JSPS Kakenhi Grant P26251024 and JP17H03680.
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Kondoh, H. (2018). Roles of ZIC2 in Regulation of Pluripotent Stem Cells. In: Aruga, J. (eds) Zic family. Advances in Experimental Medicine and Biology, vol 1046. Springer, Singapore. https://doi.org/10.1007/978-981-10-7311-3_17
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DOI: https://doi.org/10.1007/978-981-10-7311-3_17
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