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Article

BRG1 Governs Nanog Transcription in Early Mouse Embryos and Embryonic Stem Cells via Antagonism of Histone H3 Lysine 9/14 Acetylation

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Pages 4158-4169 | Received 29 May 2015, Accepted 22 Sep 2015, Published online: 20 Mar 2023

REFERENCES

  • Cockburn K, Rossant J. 2010. Making the blastocyst: lessons from the mouse. J Clin Invest 120:995–1003. http://dx.doi.org/10.1172/JCI41229.
  • Paul S, Knott JG. 2014. Epigenetic control of cell fate in mouse blastocysts: the role of covalent histone modifications and chromatin remodeling. Mol Reprod Dev 81:171–182. http://dx.doi.org/10.1002/mrd.22219.
  • Oron E., Ivanova N. 2012. Cell fate regulation in early mammalian development. Phys Biol 9:045002. http://dx.doi.org/10.1088/1478-3975/9/4/045002.
  • Strumpf D, Mao CA, Yamanaka Y, Ralston A, Chawengsaksophak K, Beck F, Rossant J. 2005. Cdx2 is required for correct cell fate specification and differentiation of trophectoderm in the mouse blastocyst. Development 132:2093–2102. http://dx.doi.org/10.1242/dev.01801.
  • Mitsui K, Tokuzawa Y, Itoh H, Segawa K, Murakami M, Takahashi K, Maruyama M, Maeda M, Yamanaka S. 2003. The Homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113:631–642. http://dx.doi.org/10.1016/S0092-8674(03)00393-3.
  • Dietrich JE, Hiiragi T. 2007. Stochastic patterning in the mouse pre-implantation embryo. Development 134:4219–4231. http://dx.doi.org/10.1242/dev.003798.
  • Choi I, Carey TS, Wilson CA, Knott JG. 2012. Transcription factor AP-2gamma is a core regulator of tight junction biogenesis and cavity formation during mouse early embryogenesis. Development 139:4623–4632. http://dx.doi.org/10.1242/dev.086645.
  • Kuckenberg P, Buhl S, Woynecki T, van Furden B, Tolkunova E, Seiffe F, Moser M, Tomilin A, Winterhager E, Schorle H. 2010. The transcription factor TCFAP2C/AP-2gamma cooperates with CDX2 to maintain trophectoderm formation. Mol Cell Biol 30:3310–3320. http://dx.doi.org/10.1128/MCB.01215-09.
  • Home P, Ray S, Dutta D, Bronshteyn I, Larson M, Paul S. 2009. GATA3 is selectively expressed in the trophectoderm of peri-implantation embryo and directly regulates Cdx2 gene expression. J Biol Chem 284:28729–28737. http://dx.doi.org/10.1074/jbc.M109.016840.
  • Wicklow E, Blij S, Frum T, Hirate Y, Lang RA, Sasaki H, Ralston A. 2014. HIPPO pathway members restrict SOX2 to the inner cell mass where it promotes ICM fates in the mouse blastocyst. PLoS Genet 10: e1004618. http://dx.doi.org/10.1371/journal.pgen.1004618.
  • Cao Z, Carey TS, Ganguly A, Wilson CA, Paul S, Knott JG. 2015. Transcription factor AP-2gamma induces early Cdx2 expression and represses HIPPO signaling to specify the trophectoderm lineage. Development 142:1606–1615. http://dx.doi.org/10.1242/dev.120238.
  • Nishioka N, Inoue K, Adachi K, Kiyonari H, Ota M, Ralston A, Yabuta N, Hirahara S, Stephenson RO, Ogonuki N, Makita R, Kurihara H, Morin-Kensicki EM, Nojima H, Rossant J, Nakao K, Niwa H, Sasaki H. 2009. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev Cell 16:398–410. http://dx.doi.org/10.1016/j.devcel.2009.02.003.
  • Niwa H, Toyooka Y, Shimosato D, Strumpf D, Takahashi K, Yagi R, Rossant J. 2005. Interaction between Oct3/4 and Cdx2 determines trophectoderm differentiation. Cell 123:917–929. http://dx.doi.org/10.1016/j.cell.2005.08.040.
  • Yuan P, Han J, Guo G, Orlov YL, Huss M, Loh YH, Yaw LP, Robson P, Lim B, Ng HH. 2009. Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells. Genes Dev 23:2507–2520. http://dx.doi.org/10.1101/gad.1831909.
  • Wang K, Sengupta S, Magnani L, Wilson CA, Henry RW, Knott JG. 2010. Brg1 is required for Cdx2-mediated repression of Oct4 expression in mouse blastocysts. PLoS One 5: e10622. http://dx.doi.org/10.1371/journal.pone.0010622.
  • Saha B, Home P, Ray S, Larson M, Paul A, Rajendran G, Behr B, Paul S. 2013. EED and KDM6B coordinate the first mammalian cell lineage commitment to ensure embryo implantation. Mol Cell Biol 33:2691–2705. http://dx.doi.org/10.1128/MCB.00069-13.
  • Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. 2010. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466:1129–1133. http://dx.doi.org/10.1038/nature09303.
  • Torres-Padilla ME, Parfitt DE, Kouzarides T, Zernicka-Goetz M. 2007. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445:214–218. http://dx.doi.org/10.1038/nature05458.
  • Kidder BL, Palmer S, Knott JG. 2009. SWI/SNF-Brg1 regulates self-renewal and occupies core pluripotency-related genes in embryonic stem cells. Stem Cells 27:317–328. http://dx.doi.org/10.1634/stemcells.2008-0710.
  • Ho L, Jothi R, Ronan JL, Cui K, Zhao K, Crabtree GR. 2009. An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc Natl Acad Sci U S A 106:5187–5191. http://dx.doi.org/10.1073/pnas.0812888106.
  • Choi I, Carey TS, Wilson CA, Knott JG. 2013. Evidence that transcription factor AP-2gamma is not required for Oct4 repression in mouse blastocysts. PLoS One 8: e65771. http://dx.doi.org/10.1371/journal.pone.0065771.
  • Carey TS, Choi I, Wilson CA, Floer M, Knott JG. 2014. Transcriptional reprogramming and chromatin remodeling accompanies Oct4 and Nanog silencing in mouse trophoblast lineage. Stem Cells Dev 23:219–229. http://dx.doi.org/10.1089/scd.2013.0328.
  • Ho L, Ronan JL, Wu J, Staahl BT, Chen L, Kuo A, Lessard J, Nesvizhskii AI, Ranish J, Crabtree GR. 2009. An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc Natl Acad Sci U S A 106:5181–5186. http://dx.doi.org/10.1073/pnas.0812889106.
  • Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307:1098–1101. http://dx.doi.org/10.1126/science.1106148.
  • Gévry N, Svotelis A, Larochelle M, Gaudreau L. 2009. Nucleosome mapping. Methods Mol Biol 543:281–291. http://dx.doi.org/10.1007/978-1-60327-015-1_19.
  • Infante JJ, Law GL, Young ET. 2012. Analysis of nucleosome positioning using a nucleosome-scanning assay. Methods Mol Biol 833:63–87. http://dx.doi.org/10.1007/978-1-61779-477-3_5.
  • Bultman S, Gebuhr T, Yee D, La Mantia C, Nicholson J, Gilliam A, Randazzo F, Metzger D, Chambon P, Crabtree G, Magnuson T. 2000. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol Cell 6:1287–1295. http://dx.doi.org/10.1016/S1097-2765(00)00127-1.
  • Tolkunova E, Cavaleri F, Eckardt S, Reinbold R, Christenson LK, Scholer HR, Tomilin A. 2006. The caudal-related protein cdx2 promotes trophoblast differentiation of mouse embryonic stem cells. Stem Cells 24:139–144. http://dx.doi.org/10.1634/stemcells.2005-0240.
  • Koch CM, Andrews RM, Flicek P, Dillon SC, Karaoz U, Clelland GK, Wilcox S, Beare DM, Fowler JC, Couttet P, James KD, Lefebvre GC, Bruce AW, Dovey OM, Ellis PD, Dhami P, Langford CF, Weng Z, Birney E, Carter NP, Vetrie D, Dunham I. 2007. The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res 17:691–707. http://dx.doi.org/10.1101/gr.5704207.
  • Roh TY, Cuddapah S, Zhao K. 2005. Active chromatin domains are defined by acetylation islands revealed by genome-wide mapping. Genes Dev 19:542–552. http://dx.doi.org/10.1101/gad.1272505.
  • Karmodiya K, Krebs AR, Oulad-Abdelghani M, Kimura H, Tora L. 2012. H3K9 and H3K14 acetylation co-occur at many gene regulatory elements, while H3K14ac marks a subset of inactive inducible promoters in mouse embryonic stem cells. BMC Genomics 13:424. http://dx.doi.org/10.1186/1471-2164-13-424.
  • Kidder BL, Palmer S. 2012. HDAC1 regulates pluripotency and lineage specific transcriptional networks in embryonic and trophoblast stem cells. Nucleic Acids Res 40:2925–2939. http://dx.doi.org/10.1093/nar/gkr1151.
  • Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA. 2007. A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130:77–88. http://dx.doi.org/10.1016/j.cell.2007.05.042.
  • de la Serna IL, Ohkawa Y, Imbalzano AN. 2006. Chromatin remodelling in mammalian differentiation: lessons from ATP-dependent remodellers. Nat Rev Genet 7:461–473. http://dx.doi.org/10.1038/nrg1882.
  • Trotter KW, Archer TK. 2008. The BRG1 transcriptional coregulator. Nucl Recept Signal 6: e004. http://dx.doi.org/10.1621/nrs.06004.
  • Ware CB, Wang L, Mecham BH, Shen L, Nelson AM, Bar M, Lamba DA, Dauphin DS, Buckingham B, Askari B, Lim R, Tewari M, Gartler SM, Issa JP, Pavlidis P, Duan Z, Blau CA. 2009. Histone deacetylase inhibition elicits an evolutionarily conserved self-renewal program in embryonic stem cells. Cell Stem Cell 4:359–369. http://dx.doi.org/10.1016/j.stem.2009.03.001.
  • Bai L, Morozov AV. 2010. Gene regulation by nucleosome positioning. Trends Genet 26:476–483. http://dx.doi.org/10.1016/j.tig.2010.08.003.
  • Voss TC, Hager GL. 2014. Dynamic regulation of transcriptional states by chromatin and transcription factors. Nat Rev Genet 15:69–81. http://dx.doi.org/10.1038/nrg3623.
  • Chambers I, Colby D, Robertson M, Nichols J, Lee S, Tweedie S, Smith A. 2003. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113:643–655. http://dx.doi.org/10.1016/S0092-8674(03)00392-1.
  • Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z, Reik W, Hemberger M. 2008. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 10:1280–1290. http://dx.doi.org/10.1038/ncb1786.
  • Hyslop L, Stojkovic M, Armstrong L, Walter T, Stojkovic P, Przyborski S, Herbert M, Murdoch A, Strachan T, Lako M. 2005. Downregulation of NANOG induces differentiation of human embryonic stem cells to extraembryonic lineages. Stem Cells 23:1035–1043. http://dx.doi.org/10.1634/stemcells.2005-0080.
  • Chen L, Yabuuchi A, Eminli S, Takeuchi A, Lu CW, Hochedlinger K, Daley GQ. 2009. Cross-regulation of the Nanog and Cdx2 promoters. Cell Res 19:1052–1061. http://dx.doi.org/10.1038/cr.2009.79.
  • Cho LT, Wamaitha SE, Tsai IJ, Artus J, Sherwood RI, Pedersen RA, Hadjantonakis AK, Niakan KK. 2012. Conversion from mouse embryonic to extra-embryonic endoderm stem cells reveals distinct differentiation capacities of pluripotent stem cell states. Development 139:2866–2877. http://dx.doi.org/10.1242/dev.078519.
  • Hirschhorn JN, Brown SA, Clark CD, Winston F. 1992. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev 6:2288–2298. http://dx.doi.org/10.1101/gad.6.12a.2288.
  • Winston F, Carlson M. 1992. Yeast SNF/SWI transcriptional activators and the SPT/SIN chromatin connection. Trends Genet 8:387–391.
  • Zhang B, Chambers KJ, Faller DV, Wang S. 2007. Reprogramming of the SWI/SNF complex for co-activation or co-repression in prohibitin-mediated estrogen receptor regulation. Oncogene 26:7153–7157. http://dx.doi.org/10.1038/sj.onc.1210509.
  • Xu Z, Meng X, Cai Y, Koury MJ, Brandt SJ. 2006. Recruitment of the SWI/SNF protein Brg1 by a multiprotein complex effects transcriptional repression in murine erythroid progenitors. Biochem J 399:297–304. http://dx.doi.org/10.1042/BJ20060873.
  • Xu W, Cho H, Kadam S, Banayo EM, Anderson S, Yates JR 3rd, Emerson BM, Evans RM. 2004. A methylation-mediator complex in hormone signaling. Genes Dev 18:144–156. http://dx.doi.org/10.1101/gad.1141704.
  • Darr H, Mayshar Y, Benvenisty N. 2006. Overexpression of NANOG in human ES cells enables feeder-free growth while inducing primitive ectoderm features. Development 133:1193–1201. http://dx.doi.org/10.1242/dev.02286.
  • Zhang X, Li B, Li W, Ma L, Zheng D, Li L, Yang W, Chu M, Chen W, Mailman RB, Zhu J, Fan G, Archer TK, Wang Y. 2014. Transcriptional repression by the BRG1-SWI/SNF complex affects the pluripotency of human embryonic stem cells. Stem Cell Reports 3:460–474. http://dx.doi.org/10.1016/j.stemcr.2014.07.004.
  • Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, Zhao K. 2009. Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138:1019–1031. http://dx.doi.org/10.1016/j.cell.2009.06.049.

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