UTX and UTY Demonstrate Histone Demethylase-Independent Function in Mouse Embryonic Development

PLoS Genetics

Volumn 8, Issue 9, 2012, Pages

  Shpargel, Karl B ^a   Sengoku, Toru ^b   Yokoyama, Shigeyuki ^b,c   Magnuson, Terry ^a  

^a UNIVERSITY OF NORTH CAROLINA HOSPITALS   (United States)

^b RIKEN   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE DEMETHYLASE; HISTONE DEMETHYLASE UTX; HISTONE DEMETHYLASE UTY; UNCLASSIFIED DRUG;

ADULTHOOD; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CATALYSIS; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO VIABILITY; ENZYME ACTIVITY; FEMALE; GENE ACTIVITY; HEART DEVELOPMENT; HEMIZYGOTE; HISTONE DEMETHYLATION; HISTONE MODIFICATION; HOMOZYGOTE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LETHAL MUTANT; MALE; MOUSE; MOUSE MUTANT; MUTATION; NEURAL TUBE; NONHUMAN; PERINATAL PERIOD; SURVIVAL RATE; YOLK SAC;

ANIMALS; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMIZYGOTE; HISTONE DEMETHYLASES; HOMOZYGOTE; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MALE; METHYLATION; MICE; MUTATION; PROTEINS;

EID: 84866912634     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002964     Document Type: Article

References (72)

1. Martin C, Zhang Y, (2005) The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 6: 838-849.
2. Cao R, Wang L, Wang H, Xia L, Erdjument-Bromage H, et al. (2002) Role of histone H3 lysine 27 methylation in Polycomb-group silencing. Science 298: 1039-1043.
3. Muller J, Hart CM, Francis NJ, Vargas ML, Sengupta A, et al. (2002) Histone methyltransferase activity of a Drosophila Polycomb group repressor complex. Cell 111: 197-208.
4. Czermin B, Melfi R, McCabe D, Seitz V, Imhof A, et al. (2002) Drosophila enhancer of Zeste/ESC complexes have a histone H3 methyltransferase activity that marks chromosomal Polycomb sites. Cell 111: 185-196.
5. Kuzmichev A, Nishioka K, Erdjument-Bromage H, Tempst P, Reinberg D, (2002) Histone methyltransferase activity associated with a human multiprotein complex containing the Enhancer of Zeste protein. Genes Dev 16: 2893-2905.
6. Montgomery ND, Yee D, Chen A, Kalantry S, Chamberlain SJ, et al. (2005) The murine polycomb group protein Eed is required for global histone H3 lysine-27 methylation. Curr Biol 15: 942-947.
7. 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.
8. Cao R, Zhang Y, (2004) SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Mol Cell 15: 57-67.
9. Shen X, Liu Y, Hsu YJ, Fujiwara Y, Kim J, et al. (2008) EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol Cell 32: 491-502.
10. Margueron R, Li G, Sarma K, Blais A, Zavadil J, et al. (2008) Ezh1 and Ezh2 maintain repressive chromatin through different mechanisms. Mol Cell 32: 503-518.
11. Ezhkova E, Pasolli HA, Parker JS, Stokes N, Su IH, et al. (2009) Ezh2 orchestrates gene expression for the stepwise differentiation of tissue-specific stem cells. Cell 136: 1122-1135.
12. Ezhkova E, Lien WH, Stokes N, Pasolli HA, Silva JM, et al. (2011) EZH1 and EZH2 cogovern histone H3K27 trimethylation and are essential for hair follicle homeostasis and wound repair. Genes Dev 25: 485-498.
13. Margueron R, Reinberg D, (2011) The Polycomb complex PRC2 and its mark in life. Nature 469: 343-349.
14. 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.
15. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, et al. (2006) Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125: 301-313.
16. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, et al. (2006) Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
17. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K, (2006) Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev 20: 1123-1136.
18. 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.
19. 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.
20. 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 doi:10.1371/journal.pgen.1000242.
21. Faust C, Schumacher A, Holdener B, Magnuson T, (1995) The eed mutation disrupts anterior mesoderm production in mice. Development 121: 273-285.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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 doi:10.1371/journal.pone.0003034.
28. Greenfield A, Carrel L, Pennisi D, Philippe C, Quaderi N, et al. (1998) The UTX gene escapes X inactivation in mice and humans. Hum Mol Genet 7: 737-742.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. De Santa F, Narang V, Yap ZH, Tusi BK, Burgold T, et al. (2009) Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J 28: 3341-3352.
37. 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.
38. Jegalian K, Page DC, (1998) A proposed path by which genes common to mammalian X and Y chromosomes evolve to become X inactivated. Nature 394: 776-780.
39. 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.
40. Hayashi S, Lewis P, Pevny L, McMahon AP, (2002) Efficient gene modulation in mouse epiblast using a Sox2Cre transgenic mouse strain. Mech Dev 119 (Suppl 1):: S97-S101.
41. Cloonan N, Forrest AR, Kolle G, Gardiner BB, Faulkner GJ, et al. (2008) Stem cell transcriptome profiling via massive-scale mRNA sequencing. Nat Methods 5: 613-619.
42. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B, (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5: 621-628.
43. Sengoku T, Yokoyama S, (2011) Structural basis for histone H3 Lys 27 demethylation by UTX/KDM6A. Genes Dev 25: 2266-2277.
44. Cho YW, Hong T, Hong S, Guo H, Yu H, et al. (2007) PTIP associates with MLL3- and MLL4-containing histone H3 lysine 4 methyltransferase complex. J Biol Chem 282: 20395-20406.
45. Lee J, Saha PK, Yang QH, Lee S, Park JY, et al. (2008) Targeted inactivation of MLL3 histone H3-Lys-4 methyltransferase activity in the mouse reveals vital roles for MLL3 in adipogenesis. Proc Natl Acad Sci U S A 105: 19229-19234.
46. Chen S, Ma J, Wu F, Xiong LJ, Ma H, et al. (2012) The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation. Genes Dev 26: 1364-1375.
47. Tie F, Banerjee R, Conrad PA, Scacheri PC, Harte PJ, (2012) Histone Demethylase UTX and Chromatin Remodeler BRM Bind Directly to CBP and Modulate Acetylation of Histone H3 Lysine 27. Mol Cell Biol 32: 2323-2334.
48. Luoh SW, Bain PA, Polakiewicz RD, Goodheart ML, Gardner H, et al. (1997) Zfx mutation results in small animal size and reduced germ cell number in male and female mice. Development 124: 2275-2284.
49. Galan-Caridad JM, Harel S, Arenzana TL, Hou ZE, Doetsch FK, et al. (2007) Zfx controls the self-renewal of embryonic and hematopoietic stem cells. Cell 129: 345-357.
50. Arenzana TL, Smith-Raska MR, Reizis B, (2009) Transcription factor Zfx controls BCR-induced proliferation and survival of B lymphocytes. Blood 113: 5857-5867.
51. Weiss J, Meeks JJ, Hurley L, Raverot G, Frassetto A, et al. (2003) Sox3 is required for gonadal function, but not sex determination, in males and females. Mol Cell Biol 23: 8084-8091.
52. Rizzoti K, Lovell-Badge R, (2007) SOX3 activity during pharyngeal segmentation is required for craniofacial morphogenesis. Development 134: 3437-3448.
53. Rizzoti K, Brunelli S, Carmignac D, Thomas PQ, Robinson IC, et al. (2004) SOX3 is required during the formation of the hypothalamo-pituitary axis. Nat Genet 36: 247-255.
54. Barron MJ, Brookes SJ, Kirkham J, Shore RC, Hunt C, et al. (2010) A mutation in the mouse Amelx tri-tyrosyl domain results in impaired secretion of amelogenin and phenocopies human X-linked amelogenesis imperfecta. Hum Mol Genet 19: 1230-1247.
55. Adler DA, Bressler SL, Chapman VM, Page DC, Disteche CM, (1991) Inactivation of the Zfx gene on the mouse X chromosome. Proc Natl Acad Sci U S A 88: 4592-4595.
56. Yang F, Babak T, Shendure J, Disteche CM, Global survey of escape from X inactivation by RNA-sequencing in mouse. Genome Res 20: 614-622.
57. Ehrmann IE, Ellis PS, Mazeyrat S, Duthie S, Brockdorff N, et al. (1998) Characterization of genes encoding translation initiation factor eIF-2gamma in mouse and human: sex chromosome localization, escape from X-inactivation and evolution. Hum Mol Genet 7: 1725-1737.
58. Agulnik AI, Mitchell MJ, Mattei MG, Borsani G, Avner PA, et al. (1994) A novel X gene with a widely transcribed Y-linked homologue escapes X-inactivation in mouse and human. Hum Mol Genet 3: 879-884.
59. Christensen J, Agger K, Cloos PA, Pasini D, Rose S, et al. (2007) RBP2 belongs to a family of demethylases, specific for tri-and dimethylated lysine 4 on histone 3. Cell 128: 1063-1076.
60. Iwase S, Lan F, Bayliss P, de la Torre-Ubieta L, Huarte M, et al. (2007) The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128: 1077-1088.
61. Lee MG, Norman J, Shilatifard A, Shiekhattar R, (2007) Physical and functional association of a trimethyl H3K4 demethylase and Ring6a/MBLR, a polycomb-like protein. Cell 128: 877-887.
62. Eissenberg JC, Lee MG, Schneider J, Ilvarsonn A, Shiekhattar R, et al. (2007) The trithorax-group gene in Drosophila little imaginal discs encodes a trimethylated histone H3 Lys4 demethylase. Nat Struct Mol Biol 14: 344-346.
63. Vandamme J, Lettier G, Sidoli S, Di Schiavi E, Norregaard Jensen O, et al. The C. elegans H3K27 demethylase UTX-1 is essential for normal development, independent of its enzymatic activity. PLoS Genet 8: e1002647 doi:10.1371/journal.pgen.1002647.
64. Garg V, Kathiriya IS, Barnes R, Schluterman MK, King IN, et al. (2003) GATA4 mutations cause human congenital heart defects and reveal an interaction with TBX5. Nature 424: 443-447.
65. Tucker KE, Berciano MT, Jacobs EY, LePage DF, Shpargel KB, et al. (2001) Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. J Cell Biol 154: 293-307.
66. Shechter D, Dormann HL, Allis CD, Hake SB, (2007) Extraction, purification and analysis of histones. Nat Protoc 2: 1445-1457.
67. Hebert MD, Szymczyk PW, Shpargel KB, Matera AG, (2001) Coilin forms the bridge between Cajal bodies and SMN, the spinal muscular atrophy protein. Genes Dev 15: 2720-2729.
68. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, et al. c-Myc regulates transcriptional pause release. Cell 141: 432-445.
69. Argentin S, Ardati A, Tremblay S, Lihrmann I, Robitaille L, et al. (1994) Developmental stage-specific regulation of atrial natriuretic factor gene transcription in cardiac cells. Mol Cell Biol 14: 777-790.
70. 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.
71. Chandler RL, Chandler KJ, McFarland KA, Mortlock DP, (2007) Bmp2 transcription in osteoblast progenitors is regulated by a distant 3′ enhancer located 156.3 kilobases from the promoter. Mol Cell Biol 27: 2934-2951.
72. Xu J, Deng X, Watkins R, Disteche CM, (2008) Sex-specific differences in expression of histone demethylases Utx and Uty in mouse brain and neurons. J Neurosci 28: 4521-4527.