EsBAF facilitates pluripotency by conditioning the genome for LIF/STAT3 signalling and by regulating polycomb function

Nature Cell Biology

Volumn 13, Issue 8, 2011, Pages 903-913

  Ho, Lena ^a   Miller, Erik L ^a   Ronan, Jehnna L ^a   Ho, Wen Qi ^a   Jothi, Raja ^b   Crabtree, Gerald R ^c  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BARRIER TO AUTOINTEGRATION FACTOR; BRG1 PROTEIN; HISTONE H3; HOX PROTEIN; LEUKEMIA INHIBITORY FACTOR; OCTAMER TRANSCRIPTION FACTOR 4; POLYCOMB GROUP PROTEIN; STAT3 PROTEIN; TRANSCRIPTION FACTOR SOX2;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL TYPE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME SUBUNIT; GENE LOCUS; GENE SILENCING; MOUSE; NONHUMAN; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA HELICASES; EMBRYONIC STEM CELLS; FEMALE; GENE EXPRESSION REGULATION; GENES, HOMEOBOX; HISTONES; LEUKEMIA INHIBITORY FACTOR; MALE; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; PLURIPOTENT STEM CELLS; PREGNANCY; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS;

EID: 79961002967     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2285     Document Type: Article

References (50)

1. Jaenisch, R. & Young, R. Stem cells, the molecular circuitry of pluripotency and nuclear reprogramming. Cell 132, 567-582 (2008). (Pubitemid 351253686)
2. Ho, L. & Crabtree, G. R. Chromatin remodelling during development. Nature 463, 474-484 (2010).
3. Khavari, P. A., Peterson, C. L., Tamkun, J. W., Mendel, D. B. & Crabtree, G. R. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366, 170-174 (1993). (Pubitemid 23351822)
4. Ho, L. & Crabtree, G. R. Chromatin remodelling during development. Nature 463, 474-484 (2010).
5. Ho, L. et al. An embryonic stem cell chromatin remodeling complex, esBAF, is essential for embryonic stem cell self-renewal and pluripotency. Proc. Natl Acad. Sci. USA 105, 5181-5186 (2009).
6. Gao, X. et al. ES cell pluripotency and germ-layer formation require the SWI/SNF chromatin remodeling component BAF250a. Proc. Natl Acad. Sci. USA 105, 6656-6661 (2008). (Pubitemid 351754562)
7. Kaeser, M. D., Aslanian, A., Dong, M. Q., Yates, J. R. 3rd & Emerson, B. M. BRD7, a novel PBAF-specic SWI/SNF subunit, is required for target gene activation and repression in embryonic stem cells. J. Biol. Chem. 283, 32254-32263 (2008).
8. Singhal, N. et al. Chromatin-remodeling components of the BAF complex facilitate reprogramming. Cell 141, 943-955 (2010).
9. Lessard, J. et al. An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55, 201-215 (2007). (Pubitemid 47048906)
10. Kidder, B. L., Palmer, S. & Knott, J. G. SWI/SNF-Brg1 regulates self-renewal and occupies core pluripotency-related genes in embryonic stem cells. Stem Cells 27, 317-328 (2009).
11. Ho, L. et al. An embryonic stem cell chromatin remodeling complex, esBAF, is an essential component of the core pluripotency transcriptional network. Proc. Natl Acad. Sci. USA 106, 5187-5191 (2009).
12. Bilodeau, S., Kagey, M. H., Frampton, G. M., Rahl, P. B. & Young, R. A. SetDB1 contributes to repression of genes encoding developmental regulators and maintenance of ES cell state. Genes Dev. 23, 2484-2489 (2009).
13. Schaniel, C. et al. Smarcc1/Baf155 couples self-renewal gene repression with changes in chromatin structure in mouse embryonic stem cells. Stem Cells 27, 2979-2991 (2009).
14. Fazzio, T. G., Huff, J. T. & Panning, B. An RNAi screen of chromatin proteins identies Tip60-p400 as a regulator of embryonic stem cell identity. Cell 134, 162-174 (2008). (Pubitemid 351905738)
15. Yang, J. et al. Stat3 activation is limiting for reprogramming to ground state pluripotency. Cell Stem Cell 7, 319-328 (2010).
16. Buecker, C. et al. A murine ESC-like state facilitates transgenesis and homologous recombination in human pluripotent stem cells. Cell Stem Cell 6, 535-546 (2010).
17. Hanna, J. et al. Human embryonic stem cells with biological and epigenetic characteristics similar to those of mouse ESCs. Proc. Natl Acad. Sci. USA 107, 9222-9227 (2010).
18. Ying, Q. L. et al. The ground state of embryonic stem cell self-renewal. Nature 453, 519-523 (2008).
19. Morey, L. & Helin, K. Polycomb group protein-mediated repression of transcription. Trends Biochem. Sci. 35, 323-332 (2010).
20. Liu, J. et al. Bmi1 regulates mitochondrial function and the DNA damage response pathway. Nature 459, 387-392 (2009).
21. Shao, Z. et al. Stabilization of chromatin structure by PRC1, a Polycomb complex. Cell 98, 37-46 (1999). (Pubitemid 29331194)
22. Kia, S., Gorski, M., Giannakopoulos, S. & Verrijzer, C. SWI/SNF mediates Polycomb eviction and epigenetic reprogramming of the INK4b-ARF-INK4a locus. Mol. Cell Biol. 28, 3457-3464 (2008). (Pubitemid 351657107)
23. Wilson, B. G. et al. Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell 18, 316-328 (2010).
24. Loh, Y. et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nature Genet. 38, 431-440 (2006).
25. Masui, S. et al. Pluripotency governed by Sox2 via regulation of Oct3/4 expression in mouse embryonic stem cells. Nat Cell Biol. 9, 625-635 (2007). (Pubitemid 47214724)
26. Matsuda, T. et al. STAT3 activation is sufcient to maintain an undifferentiated state of mouse embryonic stem cells. EMBO J. 18, 4261-4269 (1999). (Pubitemid 29364128)
27. Jothi, R., Cuddapah, S., Barski, A., Cui, K. & Zhao, K. Genome-wide identication of in vivo protein-DNA binding sites from ChIP-Seq data. Nucleic Acids Res. 36, 5221-5231 (2008).
28. Burns, L. G. & Peterson, C. L. The yeast SWI-SNF complex facilitates binding of a transcriptional activator to nucleosomal sites in vivo. Mol. Cell Biol. 17, 4811-4819 (1997). (Pubitemid 27318156)
29. Chen, X. et al. Integration of external signaling pathways with the core transcriptional network in embryonic stem cells. Cell 133, 1106-1117 (2008). (Pubitemid 351787745)
30. Schnetz, M. P. et al. CHD7 targets active gene enhancer elements to modulate ES cell-specic gene expression. PLoS Genet. 6, e1001023 (2010).
31. Dorschner, M. O. et al. High-throughput localization of functional elements by quantitative chromatin proling. Nat. Methods 1, 219-225 (2004).
32. Lee, T. I. et al. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125, 301-313 (2006). (Pubitemid 44313811)
33. Ku, M. et al. Genomewide analysis of PRC1 and PRC2 occupancy identies two classes of bivalent domains. PLoS Genet. 4, e1000242 (2008).
34. Pasini, D., Bracken, A. P., Hansen, J. B., Capillo, M. & Helin, K. The polycomb group protein Suz12 is required for embryonic stem cell differentiation. Mol. Cell Biol. 27, 3769-3779 (2007). (Pubitemid 46726184)
35. Li, G. et al. Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 24, 368-380 (2010).
36. Shen, X. et al. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 139, 1303-1314 (2009).
37. Pasini, D. et al. JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464, 306-310 (2010).
38. Peng, J. C. et al. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139, 1290-1302 (2009).
39. Pasini, D., Bracken, A. P., Jensen, M. R., Lazzerini Denchi, E. & Helin, K. Suz12 is essential for mouse development and for EZH2 histone methyltransferase activity. EMBO J. 23, 4061-4071 (2004). (Pubitemid 39472427)
40. Cosma, M. P., Tanaka, T. & Nasmyth, K. Ordered recruitment of transcription and chromatin remodeling factors to a cell cycle-and developmentally regulated promoter. Cell 97, 299-311 (1999). (Pubitemid 29214587)
41. Ni, Z. & Bremner, R. Brahma-related gene 1-dependent STAT3 recruitment at IL-6-inducible genes. J. Immunol. 178, 345-351 (2007). (Pubitemid 46033618)
42. Giraud, S., Hurlstone, A., Avril, S. & Coqueret, O. Implication of BRG1 and cdk9 in the STAT3-mediated activation of the p21waf1 gene. Oncogene 23, 7391-7398 (2004). (Pubitemid 39382141)
43. Kia, S. K., Gorski, M. M., Giannakopoulos, S. & Verrijzer, C. P. SWI/SNF mediates polycomb eviction and epigenetic reprogramming of the INK4b-ARF-INK4a locus. Mol. Cell Biol. 28, 3457-3464 (2008). (Pubitemid 351657107)
44. Tamkun, J.W. et al. Brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell 68, 561-572 (1992).
45. Bailey, T. L., Williams, N., Misleh, C. & Li, W. W. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 34, W369-W373 (2006). (Pubitemid 44529795)
46. Marson, A. et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134, 521-533 (2008).
47. Bultman, S. et al. A Brg1 null mutation in the mouse reveals functional differences among mammalian SWI/SNF complexes. Mol. Cell 6, 1287-1295 (2000). (Pubitemid 32045922)
48. Visel, A. et al. ChIP-seq accurately predicts tissue-specic activity of enhancers. Nature 457, 854-858 (2009).
49. Okita, K. & Yamanaka, S. Intracellular signaling pathways regulating pluripotency of embryonic stem cells. Curr. Stem Cell Res. Ther. 1, 103-111 (2006).
50. Sene, K. et al. Gene function in early mouse embryonic stem cell differentiation. BMC Genomics 8, 85 (2007).