Evidence that gene activation and silencing during stem cell differentiation requires a transcriptionally paused intermediate state

PLoS ONE

Volumn 6, Issue 8, 2011, Pages

  Golob, Jonathan L ^a   Kumar, Roshan M ^b   Guenther, Matthew G ^b   Pabon, Lil M ^a   Pratt, Gabriel A ^a   Loring, Jeanne F ^c   Laurent, Louise C ^c,d   Young, Richard A ^b   Murry, Charles E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; HISTONE H3 LYSINE 4; NEUROTRANSMITTER RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL POPULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; CROSS LINKING; EMBRYO; EMBRYONIC STEM CELL; GENE ACTIVATION; GENE EXPRESSION; GENE LOCUS; GENE SILENCING; GENETIC TRANSCRIPTION; HEART CONTRACTION; HUMAN; HUMAN CELL; HUMAN GENOME; KERATINIZATION; MESODERM; PLURIPOTENT STEM CELL; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; TRANSCRIPTION PAUSING; ANIMAL; BIOLOGICAL MODEL; CELL LINE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOUSE; OPEN READING FRAME;

MAMMALIA;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; EMBRYONIC STEM CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE SILENCING; GENETIC LOCI; GENOME, HUMAN; HUMANS; MICE; MODELS, GENETIC; OPEN READING FRAMES; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 80051830097     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0022416     Document Type: Article

References (36)

1. Levine M, (2011) Paused RNA Polymerase II as a Developmental Checkpoint. Cell 145: 502-511.
2. Krumm A, Hickey LB, Groudine M, (1995) Promoter-proximal pausing of RNA polymerase II defines a general rate-limiting step after transcription initiation. Genes Dev 9: 559-572.
3. Guenther MG, Levine SS, Boyer LA, Jaenisch R, Young RA, (2007) A chromatin landmark and transcription initiation at most promoters in human cells. Cell 130: 77-88.
4. Muse GW, Gilchrist DA, Nechaev S, Shah R, Parker JS, et al. (2007) RNA polymerase is poised for activation across the genome. Nat Genet 39: 1507-1511.
5. Gilmour DS, (2009) Promoter proximal pausing on genes in metazoans. Chromosoma 118: 1-10.
6. Chiba K, Yamamoto J, Yamaguchi Y, Handa H, (2010) Promoter-proximal pausing and its release: molecular mechanisms and physiological functions. Exp Cell Res 316: 2723-2730.
7. Min IM, Waterfall JJ, Core LJ, Munroe RJ, Schimenti J, et al. (2011) Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells. Genes Dev 25: 742-754.
8. Hendrix DA, Hong JW, Zeitlinger J, Rokhsar DS, Levine MS, (2008) Promoter elements associated with RNA Pol II stalling in the Drosophila embryo. Proc Natl Acad Sci U S A 105: 7762-7767.
9. Zeitlinger J, Stark A, Kellis M, Hong JW, Nechaev S, et al. (2007) RNA polymerase stalling at developmental control genes in the Drosophila melanogaster embryo. Nat Genet 39: 1512-1516.
10. Seila AC, Calabrese JM, Levine SS, Yeo GW, Rahl PB, et al. (2008) Divergent transcription from active promoters. Science 322: 1849-1851.
11. Core LJ, Waterfall JJ, Lis JT, (2008) Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science 322: 1845-1848.
12. Gilchrist DA, Dos Santos G, Fargo DC, Xie B, Gao Y, et al. (2010) Pausing of RNA polymerase II disrupts DNA-specified nucleosome organization to enable precise gene regulation. Cell 143: 540-551.
13. Nussbaum J, Minami E, Laflamme MA, Virag JA, Ware CB, et al. (2007) Transplantation of undifferentiated murine embryonic stem cells in the heart: teratoma formation and immune response. Faseb J 21: 1345-1357.
14. Paige SL, Osugi T, Afanasiev OK, Pabon L, Reinecke H, et al. (2010) Endogenous Wnt/beta-catenin signaling is required for cardiac differentiation in human embryonic stem cells. PLoS One 5: e11134.
15. Fernandes S, Naumova AV, Zhu WZ, Laflamme MA, Gold J, et al. (2010) Human embryonic stem cell-derived cardiomyocytes engraft but do not alter cardiac remodeling after chronic infarction in rats. J Mol Cell Cardiol 49: 941-949.
16. Stevens KR, Kreutziger KL, Dupras SK, Korte FS, Regnier M, et al. (2009) Physiological function and transplantation of scaffold-free and vascularized human cardiac muscle tissue. Proc Natl Acad Sci U S A 106: 16568-16573.
17. Laflamme MA, Chen KY, Naumova AV, Muskheli V, Fugate JA, et al. (2007) Cardiomyocytes derived from human embryonic stem cells in pro-survival factors enhance function of infarcted rat hearts. Nat Biotechnol 25: 1015-1024.
18. Tulloch NL, Muskheli V, Razumova MV, Korte FS, Regnier M, et al. (2011) Growth of Engineered Human Myocardium With Mechanical Loading and Vascular Coculture. Circ Res.
19. Nelson JD, Denisenko O, Sova P, Bomsztyk K, (2006) Fast chromatin immunoprecipitation assay. Nucleic Acids Res 34: e2.
20. Golob JL, Paige SL, Muskheli V, Pabon L, Murry CE, (2008) Chromatin remodeling during mouse and human embryonic stem cell differentiation. Dev Dyn 237: 1389-1398.
21. Lee TI, Johnstone SE, Young RA, (2006) Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat Protoc 1: 729-748.
22. Bolstad BM, Irizarry RA, Astrand M, Speed TP, (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19: 185-193.
23. Barnes M, Freudenberg J, Thompson S, Aronow B, Pavlidis P, (2005) Experimental comparison and cross-validation of the Affymetrix and Illumina gene expression analysis platforms. Nucleic Acids Res 33: 5914-5923.
24. Izumi N, Era T, Akimaru H, Yasunaga M, Nishikawa S, (2007) Dissecting the molecular hierarchy for mesendoderm differentiation through a combination of embryonic stem cell culture and RNA interference. Stem Cells 25: 1664-1674.
25. Morkin E, (2000) Control of cardiac myosin heavy chain gene expression. Microsc Res Tech 50: 522-531.
26. Cho JH, Tsai MJ, (2004) The role of BETA2/NeuroD1 in the development of the nervous system. Mol Neurobiol 30: 35-47.
27. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
28. Nechaev S, Adelman K, (2011) Pol II waiting in the starting gates: Regulating the transition from transcription initiation into productive elongation. Biochim Biophys Acta 1809: 34-45.
29. Cho S, Schroeder S, Ott M, (2010) CYCLINg through transcription: posttranslational modifications of P-TEFb regulate transcription elongation. Cell Cycle 9: 1697-1705.
30. Rahl PB, Lin CY, Seila AC, Flynn RA, McCuine S, et al. (2010) c-Myc regulates transcriptional pause release. Cell 141: 432-445.
31. Sampath P, Pritchard DK, Pabon L, Reinecke H, Schwartz SM, et al. (2008) A hierarchical network controls protein translation during murine embryonic stem cell self-renewal and differentiation. Cell Stem Cell 2: 448-460.
32. Ueno S, Weidinger G, Osugi T, Kohn AD, Golob JL, et al. (2007) Biphasic role for Wnt/beta-catenin signaling in cardiac specification in zebrafish and embryonic stem cells. Proc Natl Acad Sci U S A 104: 9685-9690.
33. Nakamura T, Sano M, Songyang Z, Schneider MD, (2003) A Wnt- and beta-catenin-dependent pathway for mammalian cardiac myogenesis. Proc Natl Acad Sci U S A 100: 5834-5839.
34. Naito AT, Shiojima I, Akazawa H, Hidaka K, Morisaki T, et al. (2006) Developmental stage-specific biphasic roles of Wnt/beta-catenin signaling in cardiomyogenesis and hematopoiesis. Proc Natl Acad Sci U S A 103: 19812-19817.
35. Xu C, Inokuma MS, Denham J, Golds K, Kundu P, et al. (2001) Feeder-free growth of undifferentiated human embryonic stem cells. Nat Biotechnol 19: 971-974.
36. Laflamme MA, Gold J, Xu C, Hassanipour M, Rosler E, et al. (2005) Formation of Human Myocardium in the Rat Heart from Human Embryonic Stem Cells. Am J Pathol 167: 663-671.