Epigenetic priming of enhancers predicts developmental competence of hESC-derived endodermal lineage intermediates

Cell Stem Cell

Volumn 16, Issue 4, 2015, Pages 386-399

  Wang, Allen ^a,b   Yue, Feng ^c   Li, Yan ^d   Xie, Ruiyu ^a,b   Harper, Thomas ^a,b   Patel, Nisha A ^a,b   Muth, Kayla ^a,b   Palmer, Jeffrey ^a,b   Qiu, Yunjiang ^d   Wang, Jinzhao ^a,b   Lam, Dieter K ^a,b   Raum, Jeffrey C ^e   Stoffers, Doris A ^e   Ren, Bing ^d,f,g,h   Sander, Maike ^a,b,f,g,h  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b SANFORD CONSORTIUM FOR REGENERATIVE MEDICINE   (United States)

^c PENN STATE COLLEGE OF MEDICINE   (United States)

^d LUDWIG INSTITUTE FOR CANCER RESEARCH   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g University of California San Diego   (United States)

^h UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 3ALPHA; HEPATOCYTE NUCLEAR FACTOR 3BETA; TRANSCRIPTION FACTOR PDX 1; BIOLOGICAL MARKER; FOXA1 PROTEIN, HUMAN; FOXA2 PROTEIN, HUMAN; HISTONE; HOMEODOMAIN PROTEIN; PANCREATIC AND DUODENAL HOMEOBOX 1 PROTEIN; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; CHROMATIN; EMBRYONIC STEM CELL; EMBRYONIC STRUCTURES; ENDODERM; EPIGENETICS; GENE; GUT TUBE; HUMAN; HUMAN CELL; PANCREAS ISLET CELL; PRIORITY JOURNAL; ANTIBODY SPECIFICITY; CELL LINE; CHROMATIN ASSEMBLY AND DISASSEMBLY; ENHANCER REGION; GASTRULA; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; HIGH THROUGHPUT SEQUENCING; METABOLISM; PANCREAS; PHYSIOLOGY;

BIOMARKERS; CELL DIFFERENTIATION; CELL LINE; CELL LINEAGE; CHROMATIN ASSEMBLY AND DISASSEMBLY; EMBRYONIC STEM CELLS; ENDODERM; ENHANCER ELEMENTS, GENETIC; EPIGENESIS, GENETIC; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HEPATOCYTE NUCLEAR FACTOR 3-BETA; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HISTONES; HOMEODOMAIN PROTEINS; HUMANS; ORGAN SPECIFICITY; PANCREAS; RNA, SMALL INTERFERING; TRANS-ACTIVATORS;

EID: 84926180401     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2015.02.013     Document Type: Article

References (53)

1. U. Ahlgren, J. Jonsson, and H. Edlund The morphogenesis of the pancreatic mesenchyme is uncoupled from that of the pancreatic epithelium in IPF1/PDX1-deficient mice Development 122 1996 1409 1416
2. B.E. Bernstein, T.S. Mikkelsen, X. Xie, M. Kamal, D.J. Huebert, J. Cuff, B. Fry, A. Meissner, M. Wernig, and K. Plath A bivalent chromatin structure marks key developmental genes in embryonic stem cells Cell 125 2006 315 326
3. S.F. Boj, D. Petrov, and J. Ferrer Epistasis of transcriptomes reveals synergism between transcriptional activators Hnf1alpha and Hnf4alpha PLoS Genet. 6 2010 e1000970
4. C. Buecker, and J. Wysocka Enhancers as information integration hubs in development: lessons from genomics Trends Genet. 28 2012 276 284
5. A. Carr, and M.D. Biggin A comparison of in vivo and in vitro DNA-binding specificities suggests a new model for homeoprotein DNA binding in Drosophila embryos EMBO J. 18 1999 1598 1608
6. M.P. Creyghton, A.W. Cheng, G.G. Welstead, T. Kooistra, B.W. Carey, E.J. Steine, J. Hanna, M.A. Lodato, G.M. Frampton, and P.A. Sharp Histone H3K27ac separates active from poised enhancers and predicts developmental state Proc. Natl. Acad. Sci. USA 107 2010 21931 21936
7. N. Gao, J. LeLay, M.Z. Vatamaniuk, S. Rieck, J.R. Friedman, and K.H. Kaestner Dynamic regulation of Pdx1 enhancers by Foxa1 and Foxa2 is essential for pancreas development Genes Dev. 22 2008 3435 3448
8. N. Hah, S. Murakami, A. Nagari, C.G. Danko, and W.L. Kraus Enhancer transcripts mark active estrogen receptor binding sites Genome Res. 23 2013 1210 1223
9. R.D. Hawkins, G.C. Hon, L.K. Lee, Q. Ngo, R. Lister, M. Pelizzola, L.E. Edsall, S. Kuan, Y. Luu, and S. Klugman Distinct epigenomic landscapes of pluripotent and lineage-committed human cells Cell Stem Cell 6 2010 479 491
10. N.D. Heintzman, G.C. Hon, R.D. Hawkins, P. Kheradpour, A. Stark, L.F. Harp, Z. Ye, L.K. Lee, R.K. Stuart, and C.W. Ching Histone modifications at human enhancers reflect global cell-type-specific gene expression Nature 459 2009 108 112
11. S. Heinz, C. Benner, N. Spann, E. Bertolino, Y.C. Lin, P. Laslo, J.X. Cheng, C. Murre, H. Singh, and C.K. Glass Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities Mol. Cell 38 2010 576 589
12. S. Heinz, C.E. Romanoski, C. Benner, K.A. Allison, M.U. Kaikkonen, L.D. Orozco, and C.K. Glass Effect of natural genetic variation on enhancer selection and function Nature 503 2013 487 492
13. P. Huang, Z. He, S. Ji, H. Sun, D. Xiang, C. Liu, Y. Hu, X. Wang, and L. Hui Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors Nature 475 2011 386 389
14. S.X. Huang, M.N. Islam, J. O'Neill, Z. Hu, Y.G. Yang, Y.W. Chen, M. Mumau, M.D. Green, G. Vunjak-Novakovic, J. Bhattacharya, and H.W. Snoeck Efficient generation of lung and airway epithelial cells from human pluripotent stem cells Nat. Biotechnol. 32 2014 84 91
15. V.R. Iyer, C.E. Horak, C.S. Scafe, D. Botstein, M. Snyder, and P.O. Brown Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF Nature 409 2001 533 538
16. F. Jin, Y. Li, B. Ren, and R. Natarajan PU.1 and C/EBP(alpha) synergistically program distinct response to NF-kappaB activation through establishing monocyte specific enhancers Proc. Natl. Acad. Sci. USA 108 2011 5290 5295
17. J. Jonsson, L. Carlsson, T. Edlund, and H. Edlund Insulin-promoter-factor 1 is required for pancreas development in mice Nature 371 1994 606 609
18. T.K. Kim, M. Hemberg, J.M. Gray, A.M. Costa, D.M. Bear, J. Wu, D.A. Harmin, M. Laptewicz, K. Barbara-Haley, and S. Kuersten Widespread transcription at neuronal activity-regulated enhancers Nature 465 2010 182 187
19. C.M. Koch, R.M. Andrews, P. Flicek, S.C. Dillon, U. Karaöz, G.K. Clelland, S. Wilcox, D.M. Beare, J.C. Fowler, and P. Couttet The landscape of histone modifications across 1% of the human genome in five human cell lines Genome Res. 17 2007 691 707
20. E. Kroon, L.A. Martinson, K. Kadoya, A.G. Bang, O.G. Kelly, S. Eliazer, H. Young, M. Richardson, N.G. Smart, and J. Cunningham Pancreatic endoderm derived from human embryonic stem cells generates glucose-responsive insulin-secreting cells in vivo Nat. Biotechnol. 26 2008 443 452
21. B. Langmead, C. Trapnell, M. Pop, and S.L. Salzberg Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Genome Biol. 10 2009 R25
22. H. Lango Allen, S.E. Flanagan, C. Shaw-Smith, E. De Franco, I. Akerman, R. Caswell, J. Ferrer, A.T. Hattersley, S. Ellard International Pancreatic Agenesis Consortium GATA6 haploinsufficiency causes pancreatic agenesis in humans Nat. Genet. 44 2012 20 22
23. C.S. Lee, J.R. Friedman, J.T. Fulmer, and K.H. Kaestner The initiation of liver development is dependent on Foxa transcription factors Nature 435 2005 944 947
24. J.E. Lee, C. Wang, S. Xu, Y.W. Cho, L. Wang, X. Feng, A. Baldridge, V. Sartorelli, L. Zhuang, W. Peng, and K. Ge H3K4 mono- and di-methyltransferase MLL4 is required for enhancer activation during cell differentiation eLife 2 2013 e01503
25. J. Li, G. Ning, and S.A. Duncan Mammalian hepatocyte differentiation requires the transcription factor HNF-4alpha Genes Dev. 14 2000 464 474
26. Z. Li, P. Gadue, K. Chen, Y. Jiao, G. Tuteja, J. Schug, W. Li, and K.H. Kaestner Foxa2 and H2A.Z mediate nucleosome depletion during embryonic stem cell differentiation Cell 151 2012 1608 1616
27. C. Linker, and C.D. Stern Neural induction requires BMP inhibition only as a late step, and involves signals other than FGF and Wnt antagonists Development 131 2004 5671 5681
28. M. Lupien, J. Eeckhoute, C.A. Meyer, Q. Wang, Y. Zhang, W. Li, J.S. Carroll, X.S. Liu, and M. Brown FoxA1 translates epigenetic signatures into enhancer-driven lineage-specific transcription Cell 132 2008 958 970
29. F. Martino, S. Kueng, P. Robinson, M. Tsai-Pflugfelder, F. van Leeuwen, M. Ziegler, F. Cubizolles, M.M. Cockell, D. Rhodes, and S.M. Gasser Reconstitution of yeast silent chromatin: multiple contact sites and O-AADPR binding load SIR complexes onto nucleosomes in vitro Mol. Cell 33 2009 323 334
30. T.S. Mikkelsen, M. Ku, D.B. Jaffe, B. Issac, E. Lieberman, G. Giannoukos, P. Alvarez, W. Brockman, T.K. Kim, and R.P. Koche Genome-wide maps of chromatin state in pluripotent and lineage-committed cells Nature 448 2007 553 560
31. A. Rada-Iglesias, R. Bajpai, T. Swigut, S.A. Brugmann, R.A. Flynn, and J. Wysocka A unique chromatin signature uncovers early developmental enhancers in humans Nature 470 2011 279 283
32. N. Rajagopal, W. Xie, Y. Li, U. Wagner, W. Wang, J. Stamatoyannopoulos, J. Ernst, M. Kellis, and B. Ren RFECS: a random-forest based algorithm for enhancer identification from chromatin state PLoS Comput. Biol. 9 2013 e1002968
33. T.C. Schulz, H.Y. Young, A.D. Agulnick, M.J. Babin, E.E. Baetge, A.G. Bang, A. Bhoumik, I. Cepa, R.M. Cesario, and C. Haakmeester A scalable system for production of functional pancreatic progenitors from human embryonic stem cells PLoS ONE 7 2012 e37004
34. Y. Shen, F. Yue, D.F. McCleary, Z. Ye, L. Edsall, S. Kuan, U. Wagner, J. Dixon, L. Lee, V.V. Lobanenkov, and B. Ren A map of the cis-regulatory sequences in the mouse genome Nature 488 2012 116 120
35. H.P. Shih, A. Wang, and M. Sander Pancreas organogenesis: from lineage determination to morphogenesis Annu. Rev. Cell Dev. Biol. 29 2013 81 105
36. M. Shogren-Knaak, H. Ishii, J.M. Sun, M.J. Pazin, J.R. Davie, and C.L. Peterson Histone H4-K16 acetylation controls chromatin structure and protein interactions Science 311 2006 844 847
37. S.B. Smith, H.Q. Qu, N. Taleb, N.Y. Kishimoto, D.W. Scheel, Y. Lu, A.M. Patch, R. Grabs, J. Wang, and F.C. Lynn Rfx6 directs islet formation and insulin production in mice and humans Nature 463 2010 775 780
38. A. Soufi, G. Donahue, and K.S. Zaret Facilitators and impediments of the pluripotency reprogramming factors' initial engagement with the genome Cell 151 2012 994 1004
39. D.A. Stoffers, N.T. Zinkin, V. Stanojevic, W.L. Clarke, and J.F. Habener Pancreatic agenesis attributable to a single nucleotide deletion in the human IPF1 gene coding sequence Nat. Genet. 15 1997 106 110
40. K.G. Storey, J.M. Crossley, E.M. De Robertis, W.E. Norris, and C.D. Stern Neural induction and regionalisation in the chick embryo Development 114 1992 729 741
41. M. van Hoek, A. Dehghan, J.C. Witteman, C.M. van Duijn, A.G. Uitterlinden, B.A. Oostra, A. Hofman, E.J. Sijbrands, and A.C. Janssens Predicting type 2 diabetes based on polymorphisms from genome-wide association studies: a population-based study Diabetes 57 2008 3122 3128
42. A. Visel, M.J. Blow, Z. Li, T. Zhang, J.A. Akiyama, A. Holt, I. Plajzer-Frick, M. Shoukry, C. Wright, and F. Chen ChIP-seq accurately predicts tissue-specific activity of enhancers Nature 457 2009 854 858
43. C.H. Waddington Organisers & Genes 1940 The University Press Cambridge, England
44. A. Wang, and M. Sander Generating cells of the gastrointestinal system: current approaches and applications for the differentiation of human pluripotent stem cells J. Mol. Med. (Berl) 90 2012 763 771
45. D. Wang, I. Garcia-Bassets, C. Benner, W. Li, X. Su, Y. Zhou, J. Qiu, W. Liu, M.U. Kaikkonen, and K.A. Ohgi Reprogramming transcription by distinct classes of enhancers functionally defined by eRNA Nature 474 2011 390 394
46. O.L. Wapinski, T. Vierbuchen, K. Qu, Q.Y. Lee, S. Chanda, D.R. Fuentes, P.G. Giresi, Y.H. Ng, S. Marro, and N.F. Neff Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons Cell 155 2013 621 635
47. A.J. Watt, R. Zhao, J. Li, and S.A. Duncan Development of the mammalian liver and ventral pancreas is dependent on GATA4 BMC Dev. Biol. 7 2007 37
48. M.N. Weedon, I. Cebola, A.M. Patch, S.E. Flanagan, E. De Franco, R. Caswell, S.A. Rodríguez-Seguí, C. Shaw-Smith, C.H. Cho, H. Lango Allen International Pancreatic Agenesis Consortium Recessive mutations in a distal PTF1A enhancer cause isolated pancreatic agenesis Nat. Genet. 46 2014 61 64
49. J.M. Wells, and D.A. Melton Early mouse endoderm is patterned by soluble factors from adjacent germ layers Development 127 2000 1563 1572
50. R. Xie, L.J. Everett, H.W. Lim, N.A. Patel, J. Schug, E. Kroon, O.G. Kelly, A. Wang, K.A. D'Amour, and A.J. Robins Dynamic chromatin remodeling mediated by polycomb proteins orchestrates pancreatic differentiation of human embryonic stem cells Cell Stem Cell 12 2013 224 237
51. A. Yang, Z. Zhu, P. Kapranov, F. McKeon, G.M. Church, T.R. Gingeras, and K. Struhl Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells Mol. Cell 24 2006 593 602
52. K.S. Zaret, and J.S. Carroll Pioneer transcription factors: establishing competence for gene expression Genes Dev. 25 2011 2227 2241
53. Y. Zhang, T. Liu, C.A. Meyer, J. Eeckhoute, D.S. Johnson, B.E. Bernstein, C. Nusbaum, R.M. Myers, M. Brown, W. Li, and X.S. Liu Model-based analysis of ChIP-Seq (MACS) Genome Biol. 9 2008 R137