TET-mediated DNA demethylation controls gastrulation by regulating Lefty-Nodal signalling

Nature

Volumn 538, Issue 7626, 2016, Pages 528-532

  Dai, Hai Qiang ^a,h   Wang, Bang An ^a,h   Yang, Lu ^b,c   Chen, Jia Jia ^a,h   Zhu, Guo Chun ^a,h   Sun, Mei Ling ^d   Ge, Hao ^b   Wang, Rui ^b,c   Chapman, Deborah L ^e   Tang, Fuchou ^b,c   Sun, Xin ^f,g   Xu, Guo Liang ^a,d,h  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b PEKING UNIVERSITY   (China)

^c Peking University   (China)

^d SHANGHAITECH UNIVERSITY   (China)

^e UNIVERSITY OF PITTSBURGH   (United States)

^f UNIVERSITY OF WISCONSIN MADISON   (United States)

^g UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^h UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

[No Author keywords available]

Indexed keywords

5 METHYLCYTOSINE; DIOXYGENASE; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; LEFTY1 PROTEIN; LEFTY2 PROTEIN; NODAL SIGNALING PROTEIN; TEN ELEVEN TRANSLOCATION PROTEIN; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA BINDING PROTEIN; LEFT RIGHT DETERMINATION FACTOR; NODAL PROTEIN, MOUSE; ONCOPROTEIN; PROTEIN NODAL; TET1 PROTEIN, MOUSE; TET2 PROTEIN, MOUSE; TET3 PROTEIN, MOUSE;

ENZYME ACTIVITY; GENE EXPRESSION; METHYLATION; MORPHOGENESIS; MUTATION; OXIDATION; PHENOTYPE; REDUCTION; RODENT;

ALLELE; ARTICLE; CONTROLLED STUDY; DNA ALKYLATION; DNA DEMETHYLATION; DNA METHYLATION; EMBRYO; ENZYME ACTIVITY; EPIGENETICS; GAIN OF FUNCTION MUTATION; GASTRULATION; GENE EXPRESSION; GENE INACTIVATION; GENE MUTATION; MESODERM; MORPHOGENESIS; MOUSE; MOUSE EMBRYO; NONHUMAN; NULL MUTATION; OXIDATION; PHENOTYPE; POINT MUTATION; PRIMITIVE STREAK; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; DEFICIENCY; EMBRYOLOGY; ENHANCER REGION; ENZYMOLOGY; FEMALE; GENETIC EPIGENESIS; GENETICS; MALE; MAMMALIAN EMBRYO; METABOLISM; OXIDATION REDUCTION REACTION; PROMOTER REGION;

MAMMALIA; MUS;

5-METHYLCYTOSINE; ANIMALS; DIOXYGENASES; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA-BINDING PROTEINS; EMBRYO, MAMMALIAN; ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; FEMALE; GASTRULATION; LEFT-RIGHT DETERMINATION FACTORS; MALE; MESODERM; MICE; NODAL PROTEIN; OXIDATION-REDUCTION; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION;

EID: 84994051865     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature20095     Document Type: Article

References (51)

1. Hackett, J. A. & Surani, M. A. DNA methylation dynamics during the mammalian life cycle. Phil. Trans. R. Soc. Lond. B 368, 20110328 (2013).
2. Pastor, W. A., Aravind, L. & Rao, A. TETonic shift: biological roles of TET proteins in DNA demethylation and transcription. Nat. Rev. Mol. Cell Biol. 14, 341-356 (2013).
3. Seisenberger, S. et al. Reprogramming DNA methylation in the mammalian life cycle: building and breaking epigenetic barriers. Phil. Trans. R. Soc. Lond. B 368, 20110330 (2013).
4. Jaenisch, R. & Bird, A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat. Genet. 33 (Suppl), 245-254 (2003).
5. Li, E. & Zhang, Y. DNA methylation in mammals. Cold Spring Harb. Perspect. Biol. 6, a019133 (2014).
6. Goll, M. G. & Bestor, T. H. Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 74, 481-514 (2005).
7. Bestor, T. H., Edwards, J. R. & Boulard, M. Notes on the role of dynamic DNA methylation in mammalian development. Proc. Natl Acad. Sci. USA 112, 6796-6799 (2015).
8. Schübeler, D. Function and information content of DNA methylation. Nature 517, 321-326 (2015).
9. Smith, Z. D. & Meissner, A. DNA methylation: roles in mammalian development. Nat. Rev. Genet. 14, 204-220 (2013).
10. Meno, C. et al. Mouse Lefty2 and zebrafish antivin are feedback inhibitors of nodal signaling during vertebrate gastrulation. Mol. Cell 4, 287-298 (1999).
11. Tam, P. P., Loebel, D. A. & Tanaka, S. S. Building the mouse gastrula: signals, asymmetry and lineages. Curr. Opin. Genet. Dev. 16, 419-425 (2006).
12. Takaoka, K. & Hamada, H. Cell fate decisions and axis determination in the early mouse embryo. Development 139, 3-14 (2012).
13. Arnold, S. J. & Robertson, E. J. Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat. Rev. Mol. Cell Biol. 10, 91-103 (2009).
14. Rivera-Pérez, J. A. & Hadjantonakis, A. K. The Dynamics of Morphogenesis in the Early Mouse Embryo. Cold Spring Harb. Perspect. Biol. 7, a015867 (2014).
15. Parfitt, D. E. & Shen, M. M. From blastocyst to gastrula: gene regulatory networks of embryonic stem cells and early mouse embryogenesis. Phil. Trans. R. Soc. Lond. B 369, 20130542 (2014).
16. Tahiliani, M. et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324, 930-935 (2009).
17. Ito, S. et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300-1303 (2011).
18. He, Y. F. et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307 (2011).
19. Dawlaty, M. M. et al. Loss of Tet enzymes compromises proper differentiation of embryonic stem cells. Dev. Cell 29, 102-111 (2014).
20. Hu, X. et al. Tet and TDG mediate DNA demethylation essential for mesenchymal-to-epithelial transition in somatic cell reprogramming. Cell Stem Cell 14, 512-522 (2014).
21. Zhou, X., Sasaki, H., Lowe, L., Hogan, B. L. & Kuehn, M. R. Nodal is a novel TGF-beta-like gene expressed in the mouse node during gastrulation. Nature 361, 543-547 (1993).
22. Meno, C. et al. lefty-1 is required for left-right determination as a regulator of lefty-2 and nodal. Cell 94, 287-297 (1998).
23. Saijoh, Y. et al. Distinct transcriptional regulatory mechanisms underlie left-right asymmetric expression of lefty-1 and lefty-2. Genes Dev. 13, 259-269 (1999).
24. Wu, H. et al. Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 473, 389-393 (2011).
25. Chen, Q., Chen, Y., Bian, C., Fujiki, R. & Yu, X. TET2 promotes histone O-GlcN Acylation during gene transcription. Nature 493, 561-564 (2013).
26. Okano, M., Bell, D. W., Haber, D. A. & Li, E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257 (1999).
27. Auclair, G., Guibert, S., Bender, A. & Weber, M. Ontogeny of CpG island methylation and specificity of DNMT3 methyltransferases during embryonic development in the mouse. Genome Biol. 15, 545 (2014).
28. Gu, T. P. et al. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477, 606-610 (2011).
29. Dawlaty, M. M. et al. Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev. Cell 24, 310-323 (2013).
30. Li, C. et al. Overlapping requirements for Tet2 and Tet3 in normal development and hematopoietic stem cell emergence. Cell Reports 12, 1133-1143 (2015).
31. Zhang, R.-R. et al. Tet1 regulates adult hippocampal neurogenesis and cognition. Cell Stem Cell 13, 237-245 (2013).
32. Sadate-Ngatchou, P. I., Payne, C. J., Dearth, A. T. & Braun, R. E. Cre recombinase activity specific to postnatal, premeiotic male germ cells in transgenic mice. Genesis 46, 738-742 (2008).
33. de Vries, W. N. et al. Expression of Cre recombinase in mouse oocytes: a means to study maternal effect genes. Genesis 26, 110-112 (2000).
34. Yin, R. et al. Ascorbic acid enhances Tet-mediated 5-methylcytosine oxidation and promotes DNA demethylation in mammals. J. Am. Chem. Soc. 135, 10396-10403 (2013).
35. Li, J. Y. et al. Synergistic function of DNA methyltransferases Dnmt3a and Dnmt3b in the methylation of Oct4 and Nanog. Mol. Cell. Biol. 27, 8748-8759 (2007).
36. Wang, H. et al. One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153, 910-918 (2013).
37. Yang, H. et al. One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154, 1370-1379 (2013).
38. Yang, H., Wang, H. & Jaenisch, R. Generating genetically modified mice using CRISPR/Cas-mediated genome engineering. Nat. Protocols 9, 1956-1968 (2014).
39. Rohde, C., Zhang, Y., Reinhardt, R. & Jeltsch, A. BISMA-fast and accurate bisulfite sequencing data analysis of individual clones from unique and repetitive sequences. BMC Bioinformatics 11, 230 (2010).
40. Tang, F. et al. RNA-Seq analysis to capture the transcriptome landscape of a single cell. Nat. Protocols 5, 516-535 (2010).
41. Tang, F. et al. mRNA-Seq whole-transcriptome analysis of a single cell. Nat. Methods 6, 377-382 (2009).
42. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
43. Trapnell, C. et al. Transcript assembly and quantification by RNA-seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28, 511-515 (2010).
44. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
45. Miura, F., Enomoto, Y., Dairiki, R. & Ito, T. Amplification-free whole-genome bisulfite sequencing by post-bisulfite adaptor tagging. Nucleic Acids Res. 40, e136 (2012).
46. Smallwood, S. A. et al. Single-cell genome-wide bisulfite sequencing for assessing epigenetic heterogeneity. Nat. Methods 11, 817-820 (2014).
47. Guo, F. et al. The transcriptome and DNA methylome landscapes of human primordial germ cells. Cell 161, 1437-1452 (2015).
48. Krueger, F. & Andrews, S. R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics 27, 1571-1572 (2011).
49. Li, H. et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
50. Song, Q. et al. A reference methylome database and analysis pipeline to facilitate integrative and comparative epigenomics. PLoS One 8, e81148 (2013).
51. Shen, Y. et al. A map of the cis-regulatory sequences in the mouse genome. Nature 488, 116-120 (2012).