KDM6 Demethylase Independent Loss of Histone H3 Lysine 27 Trimethylation during Early Embryonic Development

PLoS Genetics

Volumn 10, Issue 8, 2014, Pages

  Shpargel, Karl B ^a   Starmer, Joshua ^a   Yee, Della ^a   Pohlers, Michael ^a   Magnuson, Terry ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEMETHYLASE; HISTONE H3; KDM6 DEMETHYLASE; RETINOIC ACID; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; CHROMATIN; KDM6B PROTEIN, MOUSE; UTX PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYONIC STEM CELL; FEMALE; FIBROBLAST; GENE; GENE ACTIVATION; GENE EXPRESSION; GENE REPRESSION; HISTONE DEMETHYLATION; HISTONE METHYLATION; HOX GENE; JMJD3 GENE; KDM6 GENE; MALE; MOUSE; NONHUMAN; PROMOTER REGION; TRANSCRIPTION INITIATION; UTX GENE; Y CHROMOSOME; ANIMAL; BIOSYNTHESIS; CHROMATIN; GENE EXPRESSION REGULATION; GENETICS; MAMMALIAN EMBRYO; MUTATION; PREGNANCY;

ANIMALS; CELL DIFFERENTIATION; CHROMATIN; EMBRYO, MAMMALIAN; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HISTONE DEMETHYLASES; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MALE; MICE; MUTATION; PREGNANCY;

EID: 84930654857     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004507     Document Type: Article

References (75)

1. Azuara V, Perry P, Sauer S, Spivakov M, Jorgensen HF, et al. (2006) Chromatin signatures of pluripotent cell lines. Nat Cell Biol 8: 532–538.
2. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, et al. (2006) A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315–326.
3. Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, et al. (2008) Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet 4: e1000242.
4. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, et al. (2007) Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 448: 553–560.
5. Rugg-Gunn PJ, Cox BJ, Ralston A, Rossant J, (2010) Distinct histone modifications in stem cell lines and tissue lineages from the early mouse embryo. Proc Natl Acad Sci U S A 107: 10783–10790.
6. Sachs M, Onodera C, Blaschke K, Ebata KT, Song JS, et al. (2013) Bivalent Chromatin Marks Developmental Regulatory Genes in the Mouse Embryonic Germline In Vivo. Cell Rep 3: 1777–84 doi: 10.1016/j.celrep.2013.04.032
7. Hammoud SS, Nix DA, Zhang H, Purwar J, Carrell DT, et al. (2009) Distinctive chromatin in human sperm packages genes for embryo development. Nature 460: 473–478.
8. Lindeman LC, Andersen IS, Reiner AH, Li N, Aanes H, et al. (2011) Prepatterning of developmental gene expression by modified histones before zygotic genome activation. Dev Cell 21: 993–1004.
9. Dahl JA, Reiner AH, Klungland A, Wakayama T, Collas P, (2010) Histone H3 lysine 27 methylation asymmetry on developmentally-regulated promoters distinguish the first two lineages in mouse preimplantation embryos. PLoS One 5: e9150.
10. Alder O, Lavial F, Helness A, Brookes E, Pinho S, et al. (2010) Ring1B and Suv39h1 delineate distinct chromatin states at bivalent genes during early mouse lineage commitment. Development 137: 2483–2492.
11. Cui K, Zang C, Roh TY, Schones DE, Childs RW, et al. (2009) Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 4: 80–93.
12. van Arensbergen J, Garcia-Hurtado J, Moran I, Maestro MA, Xu X, et al. (2010) Derepression of Polycomb targets during pancreatic organogenesis allows insulin-producing beta-cells to adopt a neural gene activity program. Genome Res 20: 722–732.
13. Roh TY, Cuddapah S, Cui K, Zhao K, (2006) The genomic landscape of histone modifications in human T cells. Proc Natl Acad Sci U S A 103: 15782–15787.
14. Zhao XD, Han X, Chew JL, Liu J, Chiu KP, et al. (2007) Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 1: 286–298.
15. Pan G, Tian S, Nie J, Yang C, Ruotti V, et al. (2007) Whole-genome analysis of histone H3 lysine 4 and lysine 27 methylation in human embryonic stem cells. Cell Stem Cell 1: 299–312.
16. Wang AH, Zare H, Mousavi K, Wang C, Moravec CE, et al. (2013) The histone chaperone Spt6 coordinates histone H3K27 demethylation and myogenesis. EMBO J 32: 1075–1086.
17. Kartikasari AE, Zhou JX, Kanji MS, Chan DN, Sinha A, et al. (2013) The histone demethylase Jmjd3 sequentially associates with the transcription factors Tbx3 and Eomes to drive endoderm differentiation. EMBO J 32: 1393–1408.
18. Ramadoss S, Chen X, Wang CY, (2012) Histone demethylase KDM6B promotes epithelial-mesenchymal transition. J Biol Chem 287: 44508–44517.
19. Jiang W, Wang J, Zhang Y, (2012) Histone H3K27me3 demethylases KDM6A and KDM6B modulate definitive endoderm differentiation from human ESCs by regulating WNT signaling pathway. Cell Res 23: 122–130.
20. Wang JK, Tsai MC, Poulin G, Adler AS, Chen S, et al. (2010) The histone demethylase UTX enables RB-dependent cell fate control. Genes Dev 24: 327–332.
21. Seenundun S, Rampalli S, Liu QC, Aziz A, Palii C, et al. (2010) UTX mediates demethylation of H3K27me3 at muscle-specific genes during myogenesis. EMBO J 29: 1401–1411.
22. Burgold T, Spreafico F, De Santa F, Totaro MG, Prosperini E, et al. (2008) The histone H3 lysine 27-specific demethylase Jmjd3 is required for neural commitment. PLoS One 3: e3034.
23. Satoh T, Takeuchi O, Vandenbon A, Yasuda K, Tanaka Y, et al. (2010) The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat Immunol 11: 936–944.
24. Sen GL, Webster DE, Barragan DI, Chang HY, Khavari PA, (2008) Control of differentiation in a self-renewing mammalian tissue by the histone demethylase JMJD3. Genes Dev 22: 1865–1870.
25. Barradas M, Anderton E, Acosta JC, Li S, Banito A, et al. (2009) Histone demethylase JMJD3 contributes to epigenetic control of INK4a/ARF by oncogenic RAS. Genes Dev 23: 1177–1182.
26. Agger K, Cloos PA, Rudkjaer L, Williams K, Andersen G, et al. (2009) The H3K27me3 demethylase JMJD3 contributes to the activation of the INK4A-ARF locus in response to oncogene- and stress-induced senescence. Genes Dev 23: 1171–1176.
27. Lan F, Bayliss PE, Rinn JL, Whetstine JR, Wang JK, et al. (2007) A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449: 689–694.
28. De Santa F, Totaro MG, Prosperini E, Notarbartolo S, Testa G, et al. (2007) The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130: 1083–1094.
29. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, et al. (2007) UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449: 731–734.
30. Lee MG, Villa R, Trojer P, Norman J, Yan KP, et al. (2007) Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318: 447–450.
31. Shpargel KB, Sengoku T, Yokoyama S, Magnuson T, (2012) UTX and UTY demonstrate histone demethylase-independent function in mouse embryonic development. PLoS Genet 8: e1002964.
32. Wang C, Lee JE, Cho YW, Xiao Y, Jin Q, et al. (2012) UTX regulates mesoderm differentiation of embryonic stem cells independent of H3K27 demethylase activity. Proc Natl Acad Sci U S A 109: 15324–15329.
33. Hong S, Cho YW, Yu LR, Yu H, Veenstra TD, et al. (2007) Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc Natl Acad Sci U S A 104: 18439–18444.
34. Walport LJ, Hopkinson RJ, Vollmar M, Madden SK, Gileadi C, et al. (2014) Human UTY(KDM6C) is a Male-Specific N-Methyl Lysyl-Demethylase. J Biol Chem 289: 18302–18313.
35. Burgold T, Voituron N, Caganova M, Tripathi PP, Menuet C, et al. (2012) The H3K27 demethylase JMJD3 is required for maintenance of the embryonic respiratory neuronal network, neonatal breathing, and survival. Cell Rep 2: 1244–1258.
36. Chamberlain SJ, Yee D, Magnuson T, (2008) Polycomb repressive complex 2 is dispensable for maintenance of embryonic stem cell pluripotency. Stem Cells 26: 1496–1505.
37. Faust C, Schumacher A, Holdener B, Magnuson T, (1995) The eed mutation disrupts anterior mesoderm production in mice. Development 121: 273–285.
38. Pasini D, Bracken AP, Jensen MR, Lazzerini Denchi E, Helin K, (2004) Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J 23: 4061–4071.
39. O'Carroll D, Erhardt S, Pagani M, Barton SC, Surani MA, et al. (2001) The polycomb-group gene Ezh2 is required for early mouse development. Mol Cell Biol 21: 4330–4336.
40. Copur O, Muller J, (2013) The histone H3-K27 demethylase Utx regulates HOX gene expression in Drosophila in a temporally restricted manner. Development 140: 3478–3485.
41. Hayashi S, McMahon AP, (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305–318.
42. Walker E, Chang WY, Hunkapiller J, Cagney G, Garcha K, et al. (2010) Polycomb-like 2 associates with PRC2 and regulates transcriptional networks during mouse embryonic stem cell self-renewal and differentiation. Cell Stem Cell 6: 153–166.
43. Zhang H, Bradley A, (1996) Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122: 2977–2986.
44. Meyers EN, Lewandoski M, Martin GR, (1998) An Fgf8 mutant allelic series generated by Cre- and Flp-mediated recombination. Nat Genet 18: 136–141.
45. Molkentin JD, Lin Q, Duncan SA, Olson EN, (1997) Requirement of the transcription factor GATA4 for heart tube formation and ventral morphogenesis. Genes Dev 11: 1061–1072.
46. Morrisey EE, Tang Z, Sigrist K, Lu MM, Jiang F, et al. (1998) GATA6 regulates HNF4 and is required for differentiation of visceral endoderm in the mouse embryo. Genes Dev 12: 3579–3590.
47. Arnold SJ, Hofmann UK, Bikoff EK, Robertson EJ, (2008) Pivotal roles for eomesodermin during axis formation, epithelium-to-mesenchyme transition and endoderm specification in the mouse. Development 135: 501–511.
48. Russ AP, Wattler S, Colledge WH, Aparicio SA, Carlton MB, et al. (2000) Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404: 95–99.
49. Herrmann BG, (1991) Expression pattern of the Brachyury gene in whole-mount TWis/TWis mutant embryos. Development 113: 913–917.
50. Winnier G, Blessing M, Labosky PA, Hogan BL, (1995) Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 9: 2105–2116.
51. Liu P, Wakamiya M, Shea MJ, Albrecht U, Behringer RR, et al. (1999) Requirement for Wnt3 in vertebrate axis formation. Nat Genet 22: 361–365.
52. Carver EA, Jiang R, Lan Y, Oram KF, Gridley T, (2001) The mouse snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol Cell Biol 21: 8184–8188.
53. Xie W, Schultz MD, Lister R, Hou Z, Rajagopal N, et al. (2013) Epigenomic analysis of multilineage differentiation of human embryonic stem cells. Cell 153: 1134–1148.
54. Gifford CA, Ziller MJ, Gu H, Trapnell C, Donaghey J, et al. (2013) Transcriptional and Epigenetic Dynamics during Specification of Human Embryonic Stem Cells. Cell 153: 1149–1163.
55. Mansour AA, Gafni O, Weinberger L, Zviran A, Ayyash M, et al. (2012) The H3K27 demethylase Utx regulates somatic and germ cell epigenetic reprogramming. Nature 488: 409–413.
56. Welstead GG, Creyghton MP, Bilodeau S, Cheng AW, Markoulaki S, et al. (2012) X-linked H3K27me3 demethylase Utx is required for embryonic development in a sex-specific manner. Proc Natl Acad Sci U S A 109: 13004–13009.
57. Morales Torres C, Laugesen A, Helin K, (2013) Utx is required for proper induction of ectoderm and mesoderm during differentiation of embryonic stem cells. PLoS One 8: e60020.
58. Shahhoseini M, Taghizadeh Z, Hatami M, Baharvand H, (2013) Retinoic acid dependent histone 3 demethylation of the clustered HOX genes during neural differentiation of human embryonic stem cells. Biochem Cell Biol 91: 116–122.
59. Lee S, Lee JW, Lee SK, (2012) UTX, a Histone H3-Lysine 27 Demethylase, Acts as a Critical Switch to Activate the Cardiac Developmental Program. Dev Cell
60. Huang C, Xiang Y, Wang Y, Li X, Xu L, et al. (2010) Dual-specificity histone demethylase KIAA1718 (KDM7A) regulates neural differentiation through FGF4. Cell Res 20: 154–165.
61. Loenarz C, Ge W, Coleman ML, Rose NR, Cooper CD, et al. (2010) PHF8, a gene associated with cleft lip/palate and mental retardation, encodes for an Nepsilon-dimethyl lysine demethylase. Hum Mol Genet 19: 217–222.
62. Yu L, Wang Y, Huang S, Wang J, Deng Z, et al. (2010) Structural insights into a novel histone demethylase PHF8. Cell Res 20: 166–173.
63. Sengoku T, Yokoyama S, (2011) Structural basis for histone H3 Lys 27 demethylation by UTX/KDM6A. Genes Dev 25: 2266–2277.
64. Chen Z, Zang J, Kappler J, Hong X, Crawford F, et al. (2007) Structural basis of the recognition of a methylated histone tail by JMJD2A. Proc Natl Acad Sci U S A 104: 10818–10823.
65. Deal RB, Henikoff JG, Henikoff S, (2010) Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328: 1161–1164.
66. Hansen KH, Bracken AP, Pasini D, Dietrich N, Gehani SS, et al. (2008) A model for transmission of the H3K27me3 epigenetic mark. Nat Cell Biol 10: 1291–1300.
67. Petruk S, Sedkov Y, Johnston DM, Hodgson JW, Black KL, et al. (2012) TrxG and PcG proteins but not methylated histones remain associated with DNA through replication. Cell 150: 922–933.
68. Francis NJ, Follmer NE, Simon MD, Aghia G, Butler JD, (2009) Polycomb proteins remain bound to chromatin and DNA during DNA replication in vitro. Cell 137: 110–122.
69. Inoue A, Zhang Y, (2011) Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334: 194.
70. Ohno R, Nakayama M, Naruse C, Okashita N, Takano O, et al. (2013) A replication-dependent passive mechanism modulates DNA demethylation in mouse primordial germ cells. Development 140: 2892–903 doi: 10.1242/dev.093229
71. Miller SA, Mohn SE, Weinmann AS, (2010) Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Mol Cell 40: 594–605.
72. Vandamme J, Lettier G, Sidoli S, Di Schiavi E, Norregaard Jensen O, et al. (2012) The C. elegans H3K27 demethylase UTX-1 is essential for normal development, independent of its enzymatic activity. PLoS Genet 8: e1002647.
73. Gallardo T, Shirley L, John GB, Castrillon DH, (2007) Generation of a germ cell-specific mouse transgenic Cre line, Vasa-Cre. Genesis 45: 413–417.
74. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, et al. (2010) c-Myc regulates transcriptional pause release. Cell 141: 432–445.
75. Calabrese JM, Sun W, Song L, Mugford JW, Williams L, et al. (2012) Site-specific silencing of regulatory elements as a mechanism of X inactivation. Cell 151: 951–963.