DNA Methylation Restricts Lineage-specific Functions of Transcription Factor Gata4 during Embryonic Stem Cell Differentiation

PLoS Genetics

Volumn 9, Issue 6, 2013, Pages

  Oda, Masaaki ^a,b   Kumaki, Yuichi ^a,c   Shigeta, Masaki ^a   Jakt, Lars Martin ^a,d   Matsuoka, Chisa ^a   Yamagiwa, Akiko ^a   Niwa, Hitoshi ^a   Okano, Masaki ^a  

^a RIKEN   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c KYOTO UNIVERSITY   (Japan)

^d KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; TRANSCRIPTION FACTOR GATA 4;

ANIMAL CELL; ARTICLE; BINDING SITE; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; DNA METHYLATION; EMBRYONIC STEM CELL; ENDODERM; EPIGENETICS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENETIC TRANSCRIPTION; MESODERM; MOUSE; NONHUMAN; PROTEIN FUNCTION; REGULATORY MECHANISM; SOMATIC CELL; TRANSCRIPTION INITIATION; TRANSCRIPTOMICS; WILD TYPE;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA-BINDING PROTEINS; EMBRYONIC STEM CELLS; ENDODERM; EPIGENESIS, GENETIC; GATA4 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MESODERM; MICE; MICROSCOPY, ELECTRON, SCANNING TRANSMISSION;

MAMMALIA;

EID: 84879660620     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003574     Document Type: Article

References (90)

1. Niwa H, (2007) Open conformation chromatin and pluripotency. Genes Dev 21: 2671-2676.
2. Jaenisch R, Young R, (2008) Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132: 567-582.
3. Davis RL, Weintraub H, Lassar AB, (1987) Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51: 987-1000.
4. Takahashi K, Yamanaka S, (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
5. Graf T, Enver T, (2009) Forcing cells to change lineages. Nature 462: 587-594.
6. Bernstein BE, Meissner A, Lander ES, (2007) The mammalian epigenome. Cell 128: 669-681.
7. John S, Sabo PJ, Thurman RE, Sung MH, Biddie SC, et al. (2011) Chromatin accessibility pre-determines glucocorticoid receptor binding patterns. Nat Genet 43: 264-268.
8. Whyte WA, Bilodeau S, Orlando DA, Hoke HA, Frampton GM, et al. (2012) Enhancer decommissioning by LSD1 during embryonic stem cell differentiation. Nature 482: 221-225.
9. Huangfu D, Maehr R, Guo W, Eijkelenboom A, Snitow M, et al. (2008) Induction of pluripotent stem cells by defined factors is greatly improved by small-molecule compounds. Nat Biotechnol 26: 795-797.
10. Mikkelsen TS, Hanna J, Zhang X, Ku M, Wernig M, et al. (2008) Dissecting direct reprogramming through integrative genomic analysis. Nature 454: 49-55.
11. Takeuchi JK, Bruneau BG, (2009) Directed transdifferentiation of mouse mesoderm to heart tissue by defined factors. Nature 459: 708-711.
12. Tursun B, Patel T, Kratsios P, Hobert O, (2011) Direct conversion of C. elegans germ cells into specific neuron types. Science 331: 304-308.
13. Bird A, (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16: 6-21.
14. Meissner A, Mikkelsen TS, Gu H, Wernig M, Hanna J, et al. (2008) Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature 454: 766-770.
15. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, et al. (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322.
16. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, et al. (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480: 490-495.
17. Reik W, (2007) Stability and flexibility of epigenetic gene regulation in mammalian development. Nature 447: 425-432.
18. Sasaki H, Matsui Y, (2008) Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 9: 129-140.
19. Saitou M, Kagiwada S, Kurimoto K, (2012) Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 139: 15-31.
20. Goll MG, Bestor TH, (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74: 481-514.
21. Wu SC, Zhang Y, (2010) Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 11: 607-620.
22. Li E, Bestor TH, Jaenisch R, (1992) Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69: 915-926.
23. Lei H, Oh SP, Okano M, Juttermann R, Goss KA, et al. (1996) De novo DNA cytosine methyltransferase activities in mouse embryonic stem cells. Development 122: 3195-3205.
24. Okano M, Bell DW, Haber DA, Li E, (1999) DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99: 247-257.
25. Taylor SM, Jones PA, (1979) Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell 17: 771-779.
26. Takizawa T, Nakashima K, Namihira M, Ochiai W, Uemura A, et al. (2001) DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain. Dev Cell 1: 749-758.
27. Ng RK, Dean W, Dawson C, Lucifero D, Madeja Z, et al. (2008) Epigenetic restriction of embryonic cell lineage fate by methylation of Elf5. Nat Cell Biol 10: 1280-1290.
28. Lee PP, Fitzpatrick DR, Beard C, Jessup HK, Lehar S, et al. (2001) A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15: 763-774.
29. Dhawan S, Georgia S, Tschen SI, Fan G, Bhushan A, (2011) Pancreatic beta cell identity is maintained by DNA methylation-mediated repression of Arx. Dev Cell 20: 419-429.
30. Molkentin JD, (2000) The zinc finger-containing transcription factors GATA-4,-5, and-6. Ubiquitously expressed regulators of tissue-specific gene expression. J Biol Chem 275: 38949-38952.
31. Narita N, Bielinska M, Wilson DB, (1997) Wild-type endoderm abrogates the ventral developmental defects associated with GATA-4 deficiency in the mouse. Dev Biol 189: 270-274.
32. Kuo CT, Morrisey EE, Anandappa R, Sigrist K, Lu MM, et al. (1997) GATA4 transcription factor is required for ventral morphogenesis and heart tube formation. Genes Dev 11: 1048-1060.
33. 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.
34. Bosse T, Piaseckyj CM, Burghard E, Fialkovich JJ, Rajagopal S, et al. (2006) Gata4 is essential for the maintenance of jejunal-ileal identities in the adult mouse small intestine. Mol Cell Biol 26: 9060-9070.
35. Cirillo LA, Lin FR, Cuesta I, Friedman D, Jarnik M, et al. (2002) Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol Cell 9: 279-289.
36. Miranda-Carboni GA, Guemes M, Bailey S, Anaya E, Corselli M, et al. (2011) GATA4 regulates estrogen receptor-alpha-mediated osteoblast transcription. Mol Endocrinol 25: 1126-1136.
37. Peterkin T, Gibson A, Loose M, Patient R, (2005) The roles of GATA-4,-5 and-6 in vertebrate heart development. Semin Cell Dev Biol 16: 83-94.
38. Fujikura J, Yamato E, Yonemura S, Hosoda K, Masui S, et al. (2002) Differentiation of embryonic stem cells is induced by GATA factors. Genes Dev 16: 784-789.
39. Shimosato D, Shiki M, Niwa H, (2007) Extra-embryonic endoderm cells derived from ES cells induced by GATA factors acquire the character of XEN cells. BMC Dev Biol 7: 80.
40. Nakano T, Kodama H, Honjo T, (1996) In vitro development of primitive and definitive erythrocytes from different precursors. Science 272: 722-724.
41. Nishikawa SI, Nishikawa S, Hirashima M, Matsuyoshi N, Kodama H, (1998) Progressive lineage analysis by cell sorting and culture identifies FLK1+VE-cadherin+ cells at a diverging point of endothelial and hemopoietic lineages. Development 125: 1747-1757.
42. Tada S, Era T, Furusawa C, Sakurai H, Nishikawa S, et al. (2005) Characterization of mesendoderm: a diverging point of the definitive endoderm and mesoderm in embryonic stem cell differentiation culture. Development 132: 4363-4374.
43. Yamashita J, Itoh H, Hirashima M, Ogawa M, Nishikawa S, et al. (2000) Flk1-positive cells derived from embryonic stem cells serve as vascular progenitors. Nature 408: 92-96.
44. Oda M, Yamagiwa A, Yamamoto S, Nakayama T, Tsumura A, et al. (2006) DNA methylation regulates long-range gene silencing of an X-linked homeobox gene cluster in a lineage-specific manner. Genes Dev 20: 3382-3394.
45. Bachman KE, Rountree MR, Baylin SB, (2001) Dnmt3a and Dnmt3b are transcriptional repressors that exhibit unique localization properties to heterochromatin. J Biol Chem 276: 32282-32287.
46. Fuks F, Burgers WA, Godin N, Kasai M, Kouzarides T, (2001) Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. Embo J 20: 2536-2544.
47. Borgel J, Guibert S, Li Y, Chiba H, Schubeler D, et al. (2010) Targets and dynamics of promoter DNA methylation during early mouse development. Nat Genet 42: 1093-1100.
48. Wu C, Orozco C, Boyer J, Leglise M, Goodale J, et al. (2009) BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources. Genome Biol 10: R130.
49. Martin-Puig S, Wang Z, Chien KR, (2008) Lives of a heart cell: tracing the origins of cardiac progenitors. Cell Stem Cell 2: 320-331.
50. Machanick P, Bailey TL, (2011) MEME-ChIP: motif analysis of large DNA datasets. Bioinformatics 27: 1696-1697.
51. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, et al. (2010) JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 38: D105-110.
52. Newburger DE, Bulyk ML, (2009) UniPROBE: an online database of protein binding microarray data on protein-DNA interactions. Nucleic Acids Res 37: D77-82.
53. Bailey TL, (2011) DREME: motif discovery in transcription factor ChIP-seq data. Bioinformatics 27: 1653-1659.
54. Bailey TL, Machanick P, (2012) Inferring direct DNA binding from ChIP-seq. Nucleic Acids Res 40: e128.
55. Mohn F, Weber M, Rebhan M, Roloff TC, Richter J, et al. (2008) Lineage-Specific Polycomb Targets and De Novo DNA Methylation Define Restriction and Potential of Neuronal Progenitors. Mol Cell 30: 755-766.
56. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, et al. (2010) Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature 464: 927-931.
57. Feldman N, Gerson A, Fang J, Li E, Zhang Y, et al. (2006) G9a-mediated irreversible epigenetic inactivation of Oct-3/4 during early embryogenesis. Nat Cell Biol 8: 188-194.
58. Svensson EC, Huggins GS, Dardik FB, Polk CE, Leiden JM, (2000) A functionally conserved N-terminal domain of the friend of GATA-2 (FOG-2) protein represses GATA4-dependent transcription. J Biol Chem 275: 20762-20769.
59. Hirabayashi Y, Gotoh Y, (2010) Epigenetic control of neural precursor cell fate during development. Nat Rev Neurosci 11: 377-388.
60. Hitoshi S, Ishino Y, Kumar A, Jasmine S, Tanaka KF, et al. (2011) Mammalian Gcm genes induce Hes5 expression by active DNA demethylation and induce neural stem cells. Nat Neurosci 14: 957-964.
61. Broske AM, Vockentanz L, Kharazi S, Huska MR, Mancini E, et al. (2009) DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction. Nat Genet 41: 1207-1215.
62. Trowbridge JJ, Snow JW, Kim J, Orkin SH, (2009) DNA methyltransferase 1 is essential for and uniquely regulates hematopoietic stem and progenitor cells. Cell Stem Cell 5: 442-449.
63. Challen GA, Sun D, Jeong M, Luo M, Jelinek J, et al. (2012) Dnmt3a is essential for hematopoietic stem cell differentiation. Nat Genet 44: 23-31.
64. Ieda M, Fu JD, Delgado-Olguin P, Vedantham V, Hayashi Y, et al. (2010) Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142: 375-386.
65. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Sudhof TC, et al. (2010) Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463: 1035-1041.
66. Huang P, He Z, Ji S, Sun H, Xiang D, et al. (2011) Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors. Nature 475: 386-389.
67. Sekiya S, Suzuki A, (2011) Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors. Nature 475: 390-393.
68. Kim K, Doi A, Wen B, Ng K, Zhao R, et al. (2010) Epigenetic memory in induced pluripotent stem cells. Nature 467: 285-290.
69. Polo JM, Liu S, Figueroa ME, Kulalert W, Eminli S, et al. (2010) Cell type of origin influences the molecular and functional properties of mouse induced pluripotent stem cells. Nat Biotechnol 28: 848-855.
70. Bock C, Kiskinis E, Verstappen G, Gu H, Boulting G, et al. (2011) Reference Maps of Human ES and iPS Cell Variation Enable High-Throughput Characterization of Pluripotent Cell Lines. Cell 144: 439-452.
71. Ohi Y, Qin H, Hong C, Blouin L, Polo JM, et al. (2011) Incomplete DNA methylation underlies a transcriptional memory of somatic cells in human iPS cells. Nat Cell Biol 13: 541-549.
72. Jones PA, (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13: 484-492.
73. Wu H, Coskun V, Tao J, Xie W, Ge W, et al. (2010) Dnmt3a-dependent nonpromoter DNA methylation facilitates transcription of neurogenic genes. Science 329: 444-448.
74. Wiench M, John S, Baek S, Johnson TA, Sung MH, et al. (2011) DNA methylation status predicts cell type-specific enhancer activity. EMBO J 30: 3028-3039.
75. Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, et al. (2007) The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450: 908-912.
76. Gautier L, Cope L, Bolstad BM, Irizarry RA, (2004) affy-analysis of Affymetrix GeneChip data at the probe level. Bioinformatics 20: 307-315.
77. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
78. Sakurai H, Era T, Jakt LM, Okada M, Nakai S, et al. (2006) In vitro modeling of paraxial and lateral mesoderm differentiation reveals early reversibility. Stem Cells 24: 575-586.
79. R Development Core Team (2007) R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. URL http://www.R-project.org/.
80. Tusher VG, Tibshirani R, Chu G, (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98: 5116-5121.
81. Smyth GK (2005) limma: Linear Models for Microarray Data. In: Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S, editors. Bioinformatics and Computational Biology Solutions Using R and Bioconductor. New York: Springer. pp. 397-420.
82. Smyth GK, (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3.
83. de Hoon MJ, Imoto S, Nolan J, Miyano S, (2004) Open source clustering software. Bioinformatics 20: 1453-1454.
84. Saldanha AJ, (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20: 3246-3248.
85. Hulsen T, de Vlieg J, Alkema W, (2008) BioVenn- a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9: 488.
86. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
87. Smith ZD, Gu H, Bock C, Gnirke A, Meissner A, (2009) High-throughput bisulfite sequencing in mammalian genomes. Methods 48: 226-232.
88. Li LC, Dahiya R, (2002) MethPrimer: designing primers for methylation PCRs. Bioinformatics 18: 1427-1431.
89. Kumaki Y, Oda M, Okano M, (2008) QUMA: quantification tool for methylation analysis. Nucleic Acids Res 36: W170-175.
90. Murakami A, Grinberg D, Thurlow J, Dickson C, (1993) Identification of positive and negative regulatory elements involved in the retinoic acid/cAMP induction of Fgf-3 transcription in F9 cells. Nucleic Acids Res 21: 5351-5359.