Co-motif discovery identifies an esrrb-Sox2-DNA ternary complex as a mediator of transcriptional differences between mouse embryonic and epiblast stem cells

Stem Cells

Volumn 31, Issue 2, 2013, Pages 269-281

  Hutchins, Andrew Paul ^a   Choo, Siew Hua ^a   Mistri, Tapan Kumar ^a   Rahmani, Mehran ^a,c   Woon, Chow Thai ^a   Ng, Calista Keow Leng ^a,b   Jauch, Ralf ^a,d   Robson, Paul ^a,c  

^a GENOME INSTITUTE OF SINGAPORE   (Singapore)

^b Department of Chemistry ^*  (Singapore)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Bioinformatics; Embryonic stem cells; Epiblast stem cells; Esrrb Sox2; Transcription factors

Indexed keywords

TERNARY COMPLEX FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ESSRB; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; DNA BINDING; DNA STRUCTURE; DOWN REGULATION; EMBRYONIC STEM CELL; EPIBLAST STEM CELL; GENE SILENCING; GENETIC TRANSFECTION; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN ANALYSIS; PROTEIN MOTIF; PROTEIN PURIFICATION; STEM CELL;

ALGORITHMS; ANIMALS; BASE SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; DAX-1 ORPHAN NUCLEAR RECEPTOR; DNA; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GERM LAYERS; MICE; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN INTERACTION MAPPING; RECEPTORS, ESTROGEN; SOXB1 TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84874292408     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1279     Document Type: Article

References (54)

1. Marino-Ramirez L, Tharakaraman K, Spouge JL et al. Promoter analysis: Gene regulatory motif identification with A-GLAM. Methods Mol Biol 2009;537:263-276.
2. Bailey TL, Boden M, Buske FA et al. MEME SUITE: Tools for motif discovery and searching. Nucleic Acids Res 2009;37:W202-208.
3. Whitington T, Frith MC, Johnson J et al. Inferring transcription factor complexes from ChIP-seq data. Nucleic Acids Res 2011;39:e98.
4. Sharov AA, Ko MS. Exhaustive search for over-represented DNA sequence motifs with CisFinder. DNA Res 2009;16:261-273.
5. Berger MF, Badis G, Gehrke AR et al. Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell 2008;133:1266-1276. (Pubitemid 351852913)
6. Badis G, Berger MF, Philippakis AA et al. Diversity and complexity in DNA recognition by transcription factors. Science 2009;324: 1720-1723.
7. Avilion AA, Nicolis SK, Pevny LH et al. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003;17:126-140. (Pubitemid 36062514)
8. Tanaka S, Kamachi Y, Tanouchi A et al. Interplay of SOX and POU factors in regulation of the Nestin gene in neural primordial cells. Mol Cell Biol 2004;24:8834-8846. (Pubitemid 39313890)
9. Spence JR, Lange AW, Lin SC et al. Sox17 regulates organ lineage segregation of ventral foregut progenitor cells. Dev Cell 2009;17:62-74.
10. Niakan KK, Ji H, Maehr R et al. Sox17 promotes differentiation in mouse embryonic stem cells by directly regulating extraembryonic gene expression and indirectly antagonizing self-renewal. Genes Dev 2010;24:312-326.
11. Morris SA, Teo RT, Li H et al. Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo. Proc Natl Acad Sci USA 2010;107:6364-6369.
12. Jauch R, Aksoy I, Hutchins AP et al. Conversion of Sox17 into a pluripotency reprogramming factor by reengineering its association with Oct4 on DNA. Stem Cells 2011;29:940-951.
13. Nakagawa M, Koyanagi M, Tanabe K et al. Generation of induced pluripotent stem cells without Myc from mouse and human fibroblasts. Nat Biotechnol 2008;26:101-106.
14. Kondoh H, Uchikawa M, Kamachi Y. Interplay of Pax6 and SOX2 in lens development as a paradigm of genetic switch mechanisms for cell differentiation. Int J Dev Biol 2004;48:819-827. (Pubitemid 40039173)
15. Luster TA, Rizzino A. Regulation of the FGF-4 gene by a complex distal enhancer that functions in part as an enhanceosome. Gene 2003; 323:163-172. (Pubitemid 37501096)
16. Chen X, Xu H, Yuan P et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 2008;133:1106-1117. (Pubitemid 351787745)
17. Kim J, Chu J, Shen X et al. An extended transcriptional network for pluripotency of embryonic stem cells. Cell 2008;132:1049-1061. (Pubitemid 351381745)
18. Wang J, Zhuang J, Iyer S et al. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res 2012;22:1798-1812.
19. Castro DS, Skowronska-Krawczyk D, Armant O et al. Proneural bHLH and Brn proteins coregulate a neurogenic program through cooperative binding to a conserved DNA motif. Dev Cell 2006;11: 831-844. (Pubitemid 44804278)
20. Gearhart MD, Holmbeck SM, Evans RM et al. Monomeric complex of human orphan estrogen related receptor-2 with DNA: A pseudodimer interface mediates extended half-site recognition. J Mol Biol 2003;327:819-832. (Pubitemid 36315921)
21. Narasimhan K, Pillay S, Bin Ahmad NR et al. Identification of a polyoxometalate inhibitor of the DNA binding activity of Sox2. ACS Chem Biol 2011;6:573-581.
22. BabuRajendran N, Palasingam P, Narasimhan K et al. Structure of Smad1 MH1/DNA complex reveals distinctive rearrangements of BMP and TGF-beta effectors. Nucleic Acids Res 2010;38:3477-3488.
23. Rodda DJ, Chew JL, Lim LH et al. Transcriptional regulation of nanog by OCT4 and SOX2. J Biol Chem 2005;280:24731-24737. (Pubitemid 40934562)
24. Ng CK, Li NX, Chee S et al. Deciphering the Sox-Oct partner code by quantitative cooperativity measurements. Nucleic Acids Res 2012; 40:4933-4941.
25. Andrews NC, Faller DV. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res 1991;19:2499.
26. Hayashi K, Ohta H, Kurimoto K et al. Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells. Cell 2011;146:519-532.
27. Feng B, Jiang J, Kraus P et al. Reprogramming of fibroblasts into induced pluripotent stem cells with orphan nuclear receptor Esrrb. Nat Cell Biol 2009;11:197-203.
28. Kidder BL, Palmer S. HDAC1 regulates pluripotency and lineage specific transcriptional networks in embryonic and trophoblast stem cells. Nucleic Acids Res 2012;40:2925-2939.
29. Paca A, Seguin CA, Clements M et al. BMP signaling induces visceral endoderm differentiation of XEN cells and parietal endoderm. Dev Biol 2012;361:90-102.
30. Garte S. Fractal properties of the human genome. J Theor Biol 2004; 230:251-260. (Pubitemid 39078410)
31. Bryne JC, Valen E, Tang MH et al. JASPAR, the open access database of transcription factor-binding profiles: New content and tools in the 2008 update. Nucleic Acids Res 2008;36:D102-D106. (Pubitemid 351149704)
32. Baburajendran N, Jauch R, Tan CY et al. Structural basis for the cooperative DNA recognition by Smad4 MH1 dimers. Nucleic Acids Res 2011;39:8213-8222.
33. Johnson K, Kirkpatrick H, Comer A et al. Interaction of Smad complexes with tripartite DNA-binding sites. J Biol Chem 1999;274: 20709-20716.
34. Trompouki E, Bowman TV, Lawton LN et al. Lineage regulators direct BMP and Wnt pathways to cell-specific programs during differentiation and regeneration. Cell 2011;147:577-589.
35. Remenyi A, Lins K, Nissen LJ et al. Crystal structure of a POU/ HMG/DNA ternary complex suggests differential assembly of Oct4 and Sox2 on two enhancers. Genes Dev 2003;17:2048-2059. (Pubitemid 36999330)
36. Palasingam P, Jauch R, Ng CK et al. The structure of Sox17 bound to DNA reveals a conserved bending topology but selective protein interaction platforms. J Mol Biol 2009;388:619-630.
37. Tanaka S, Kunath T, Hadjantonakis AK et al. Promotion of trophoblast stem cell proliferation by FGF4. Science 1998;282:2072-2075. (Pubitemid 29001261)
38. Tesar PJ, Chenoweth JG, Brook FA et al. New cell lines from mouse epiblast share defining features with human embryonic stem cells. Nature 2007;448:196-199. (Pubitemid 47067378)
39. Brons IG, Smithers LE, Trotter MW et al. Derivation of pluripotent epiblast stem cells from mammalian embryos. Nature 2007;448: 191-195. (Pubitemid 47067373)
40. Kunath T, Arnaud D, Uy GD et al. Imprinted X-inactivation in extraembryonic endoderm cell lines from mouse blastocysts. Development 2005;132:1649-1661. (Pubitemid 40575865)
41. Luo J, Sladek R, Bader JA et al. Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-beta. Nature 1997; 388:778-782. (Pubitemid 27375157)
42. Kidder BL, Palmer S. Examination of transcriptional networks reveals an important role for TCFAP2C, SMARCA4, and Eomes in trophoblast stem cell maintenance. Genome Res 2010;20:458-472.
43. Su AI, Wiltshire T, Batalov S et al. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc Natl Acad Sci USA 2004;101:6062-6067. (Pubitemid 38520528)
44. Osorno R, Chambers I. Transcription factor heterogeneity and epiblast pluripotency. Philos Trans Roy Soc Lond Series B, Biol Sci 2011; 366:2230-2237.
45. Khalfallah O, Rouleau M, Barbry P et al. Dax-1 knockdown in mouse embryonic stem cells induces loss of pluripotency and multilineage differentiation. Stem Cells 2009;27:1529-1537.
46. Ivanova N, Dobrin R, Lu R et al. Dissecting self-renewal in stem cells with RNA interference. Nature 2006;442:533-538. (Pubitemid 44167907)
47. Robson P, Stein P, Zhou B et al. Inner cell mass-specific expression of a cell adhesion molecule (PECAM-1/CD31) in the mouse blastocyst. Dev Biol 2001;234:317-329. (Pubitemid 32552661)
48. Ferraris L, Stewart AP, Kang J et al. Combinatorial binding of transcription factors in the pluripotency control regions of the genome. Genome Res 2011;21:1055-1064.
49. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006;126:663-676. (Pubitemid 44233629)
50. Masui S, Nakatake Y, Toyooka Y et al. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol 2007;9:625-635. (Pubitemid 47214724)
51. Guo G, Huss M, Tong GQ et al. Resolution of cell fate decisions revealed by single-cell gene expression analysis from zygote to blastocyst. Dev Cell 2010;18:675-685.
52. Buganim Y, Faddah DA, Cheng AW et al. Single-cell expression analyses during cellular reprogramming reveal an early stochastic and a late hierarchic phase. Cell 2012;150:1209-1222.
53. Guo G, Yang J, Nichols J et al. Klf4 reverts developmentally programmed restriction of ground state pluripotency. Development 2009; 136:1063-1069.
54. Guo G, Smith A. A genome-wide screen in EpiSCs identifies Nr5a nuclear receptors as potent inducers of ground state pluripotency. Development 2010;137:3185-3192.