Home LiteratureArticle Details
PMID: 20479220 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo.

Proceedings of the National Academy of Sciences of the United States of America ·Vol. 107 ·No. 24 ·2010-06-15 ·Pages 10783-90

Rugg-Gunn PJ, Cox BJ, Ralston A, Rossant J

Abstract

A unique property of the mammalian embryo is that stem cells can be derived from its early tissue lineages. These lineages will give rise to the fetus as well as essential extraembryonic tissues. Understanding how chromatin regulation participates in establishment of these lineages in the embryo and their derived stem cells provides insight that will critically inform our understanding of embryogenesis and stem cell biology. Here, we compare the genomewide location of active and repressive histone modifications in embryonic stem cells, trophoblast stem cells, and extraembryonic endoderm stem cells from the mouse. Our results show that the active modification H3K4me3 has a similar role in the three stem cell types, but the repressive modification H3K27me3 varies in abundance and genomewide distribution. Thus, alternative mechanisms mediate transcriptional repression in stem cells from the embryo. In addition, using carrier chromatin immunoprecipitation we show that bivalent histone domains seen in embryonic stem cells exist in pluripotent cells of the early embryo. However, the epigenetic status of extraembryonic progenitor cells in the embryo did not entirely reflect the extraembryonic stem cell lines. These studies indicate that histone modification mechanisms may differ between early embryo lineages and emphasize the importance of examining in vivo and in vitro progenitor cells.

MeSH Terms
Animals Cell Line Chromatin Immunoprecipitation Embryo, Mammalian/cytology,metabolism Embryonic Stem Cells/cytology,metabolism Endoderm/cytology,embryology,metabolism Epigenesis, Genetic Female Gene Expression Regulation, Developmental Histones/chemistry,genetics,metabolism In Vitro Techniques Methylation Mice Mice, Inbred ICR Mice, Transgenic Pregnancy Trophoblasts/cytology,metabolism
Chemicals
Histones
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Rugg-Gunn Peter J
Program in Developmental and Stem Cell Biology, Hospital for Sick Children Research Institute, Toronto, ON, Canada.
Cox Brian J
Ralston Amy
Rossant Janet
References (61)
61 references, click to expand
  1. Imprinted X inactivation maintained by a mouse Polycomb group gene.
    Nat Genet. 2001 Aug;28(4):371-5 PMID: 11479595
  2. Derivation of pluripotent epiblast stem cells from mammalian embryos.
    Nature. 2007 Jul 12;448(7150):191-5 PMID: 17597762
  3. G9a histone methyltransferase plays a dominant role in euchromatic histone H3 lysine 9 methylation and is essential for early embryogenesis.
    Genes Dev. 2002 Jul 15;16(14):1779-91 PMID: 12130538
  4. Histone methyltransferase activity of a Drosophila Polycomb group repressor complex.
    Cell. 2002 Oct 18;111(2):197-208 PMID: 12408864
  5. Rnf2 (Ring1b) deficiency causes gastrulation arrest and cell cycle inhibition.
    Proc Natl Acad Sci U S A. 2003 Mar 4;100(5):2468-73 PMID: 12589020
  6. Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency.
    Stem Cells. 2008 Jun;26(6):1496-505 PMID: 18403752
  7. Prospective isolation and global gene expression analysis of definitive and visceral endoderm.
    Dev Biol. 2007 Apr 15;304(2):541-55 PMID: 17328885
  8. Imprinting along the Kcnq1 domain on mouse chromosome 7 involves repressive histone methylation and recruitment of Polycomb group complexes.
    Nat Genet. 2004 Dec;36(12):1296-300 PMID: 15516932
  9. The mouse PcG gene eed is required for Hox gene repression and extraembryonic development.
    Mamm Genome. 2002 Sep;13(9):493-503 PMID: 12370779
  10. An assessment of the developmental potential of embryonic stem cells in the midgestation mouse embryo.
    Development. 1989 Apr;105(4):733-7 PMID: 2598811
  11. Generating green fluorescent mice by germline transmission of green fluorescent ES cells.
    Mech Dev. 1998 Aug;76(1-2):79-90 PMID: 9867352
  12. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming.
    Cell. 2008 Feb 22;132(4):567-82 PMID: 18295576
  13. The Polycomb group protein Eed protects the inactive X-chromosome from differentiation-induced reactivation.
    Nat Cell Biol. 2006 Feb;8(2):195-202 PMID: 16415857
  14. Polycomb group proteins Ezh2 and Rnf2 direct genomic contraction and imprinted repression in early mouse embryos.
    Dev Cell. 2008 Nov;15(5):668-79 PMID: 18848501
  15. Genetic and epigenetic regulators of pluripotency.
    Cell. 2007 Feb 23;128(4):747-62 PMID: 17320511
  16. Dynamic reprogramming of DNA methylation in the early mouse embryo.
    Dev Biol. 2002 Jan 1;241(1):172-82 PMID: 11784103
  17. Epigenetic dynamics of the Kcnq1 imprinted domain in the early embryo.
    Development. 2006 Nov;133(21):4203-10 PMID: 17021040
  18. Role of histone H3 lysine 27 methylation in Polycomb-group silencing.
    Science. 2002 Nov 1;298(5595):1039-43 PMID: 12351676
  19. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency.
    Mol Cell. 2008 Nov 21;32(4):491-502 PMID: 19026780
  20. Establishment in culture of pluripotential cells from mouse embryos.
    Nature. 1981 Jul 9;292(5819):154-6 PMID: 7242681
  21. Dynamic alterations of specific histone modifications during early murine development.
    J Cell Sci. 2004 Sep 1;117(Pt 19):4449-59 PMID: 15316069
  22. Epigenetic dynamics of stem cells and cell lineage commitment: digging Waddington's canal.
    Nat Rev Mol Cell Biol. 2009 Aug;10(8):526-37 PMID: 19603040
  23. Chromatin signatures of pluripotent cell lines.
    Nat Cell Biol. 2006 May;8(5):532-8 PMID: 16570078
  24. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells.
    Nature. 2007 Aug 2;448(7153):553-60 PMID: 17603471
  25. Epigenetic characterization of the early embryo with a chromatin immunoprecipitation protocol applicable to small cell populations.
    Nat Genet. 2006 Jul;38(7):835-41 PMID: 16767102
  26. Consequences of the depletion of zygotic and embryonic enhancer of zeste 2 during preimplantation mouse development.
    Development. 2003 Sep;130(18):4235-48 PMID: 12900441
  27. Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein.
    Genes Dev. 2002 Nov 15;16(22):2893-905 PMID: 12435631
  28. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains.
    PLoS Genet. 2008 Oct;4(10):e1000242 PMID: 18974828
  29. The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation.
    Curr Biol. 2005 May 24;15(10):942-7 PMID: 15916951
  30. New cell lines from mouse epiblast share defining features with human embryonic stem cells.
    Nature. 2007 Jul 12;448(7150):196-9 PMID: 17597760
  31. Cell lineage-specific undermethylation of mouse repetitive DNA.
    Nature. 1984 Jan 19-25;307(5948):284-6 PMID: 6694730
  32. A bivalent chromatin structure marks key developmental genes in embryonic stem cells.
    Cell. 2006 Apr 21;125(2):315-26 PMID: 16630819
  33. Epigenetic reprogramming in mammals.
    Hum Mol Genet. 2005 Apr 15;14 Spec No 1:R47-58 PMID: 15809273
  34. PRC1 and Suv39h specify parental asymmetry at constitutive heterochromatin in early mouse embryos.
    Nat Genet. 2008 Apr;40(4):411-20 PMID: 18311137
  35. The Polycomb group protein EED is dispensable for the initiation of random X-chromosome inactivation.
    PLoS Genet. 2006 May;2(5):e66 PMID: 16680199
  36. Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites.
    Cell. 2002 Oct 18;111(2):185-96 PMID: 12408863
  37. Promotion of trophoblast stem cell proliferation by FGF4.
    Science. 1998 Dec 11;282(5396):2072-5 PMID: 9851926
  38. Early lineage segregation between epiblast and primitive endoderm in mouse blastocysts through the Grb2-MAPK pathway.
    Dev Cell. 2006 May;10(5):615-24 PMID: 16678776
  39. The N terminus of Drosophila ESC binds directly to histone H3 and is required for E(Z)-dependent trimethylation of H3 lysine 27.
    Mol Cell Biol. 2007 Mar;27(6):2014-26 PMID: 17210640
  40. Epigenetic landscape required for placental development.
    Cell Mol Life Sci. 2007 Sep;64(18):2422-36 PMID: 17585370
  41. Loss of the Suv39h histone methyltransferases impairs mammalian heterochromatin and genome stability.
    Cell. 2001 Nov 2;107(3):323-37 PMID: 11701123
  42. Ubiquitin E3 ligase Ring1b/Rnf2 of polycomb repressive complex 1 contributes to stable maintenance of mouse embryonic stem cells.
    PLoS One. 2008 May 21;3(5):e2235 PMID: 18493325
  43. Lineage allocation and asymmetries in the early mouse embryo.
    Philos Trans R Soc Lond B Biol Sci. 2003 Aug 29;358(1436):1341-8; discussion 1349 PMID: 14511480
  44. SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state.
    Genes Dev. 2009 Nov 1;23(21):2484-9 PMID: 19884255
  45. Global mapping of DNA methylation in mouse promoters reveals epigenetic reprogramming of pluripotency genes.
    PLoS Genet. 2008 Jun 27;4(6):e1000116 PMID: 18584034
  46. Histone H3 modifications associated with differentiation and long-term culture of mesenchymal adipose stem cells.
    Stem Cells Dev. 2009 Jun;18(5):725-36 PMID: 18771397
  47. 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. 1981 Dec;78(12):7634-8 PMID: 6950406
  48. Imprinting on distal chromosome 7 in the placenta involves repressive histone methylation independent of DNA methylation.
    Nat Genet. 2004 Dec;36(12):1291-5 PMID: 15516931
  49. Epigenetic marking prepares the human HOXA cluster for activation during differentiation of pluripotent cells.
    Stem Cells. 2008 May;26(5):1174-85 PMID: 18292213
  50. Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing.
    Nat Methods. 2007 Aug;4(8):651-7 PMID: 17558387
  51. Imprinted X-inactivation in extra-embryonic endoderm cell lines from mouse blastocysts.
    Development. 2005 Apr;132(7):1649-61 PMID: 15753215
  52. FindPeaks 3.1: a tool for identifying areas of enrichment from massively parallel short-read sequencing technology.
    Bioinformatics. 2008 Aug 1;24(15):1729-30 PMID: 18599518
  53. Site-specific analysis of histone methylation and acetylation.
    Methods Mol Biol. 2004;287:99-120 PMID: 15273407
  54. Preferential inactivation of the paternally derived X chromosome in the extraembryonic membranes of the mouse.
    Nature. 1975 Aug 21;256(5519):640-2 PMID: 1152998
  55. Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5.
    Nat Cell Biol. 2008 Nov;10(11):1280-90 PMID: 18836439
  56. Eset partners with Oct4 to restrict extraembryonic trophoblast lineage potential in embryonic stem cells.
    Genes Dev. 2009 Nov 1;23(21):2507-20 PMID: 19884257
  57. The polycomb group protein Suz12 is required for embryonic stem cell differentiation.
    Mol Cell Biol. 2007 May;27(10):3769-79 PMID: 17339329
  58. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells.
    Nat Cell Biol. 2007 Dec;9(12):1428-35 PMID: 18037880
  59. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity.
    EMBO J. 2004 Oct 13;23(20):4061-71 PMID: 15385962
  60. The polycomb-group gene Ezh2 is required for early mouse development.
    Mol Cell Biol. 2001 Jul;21(13):4330-6 PMID: 11390661
  61. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin.
    Mol Cell. 2003 Dec;12(6):1577-89 PMID: 14690609
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
DOI
10.1073/pnas.0914507107
Published
2010-06-15
Epub
2010-00-17
Pages
10783-90
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2890770
Subset
IM
Grants
Canadian Institutes of Health Research · MOP77803 · Canada
Databases
GEO
GSE15519
External Links
PubMed source DOI: 10.1073/pnas.0914507107 PMC Full Text View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2