Nucleosome positioning changes during human embryonic stem cell differentiation

References

• Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998; 282:1145-7; PMID:9804556; http://dx.doi.org/10.1126/science.282.5391.1145
   PubMed Web of Science ®Google Scholar
• Menendez L, Kulik MJ, Page AT, Park SS, Lauderdale JD, Cunningham ML, Dalton S. Directed differentiation of human pluripotent cells to neural crest stem cells. Nat Protoc 2013; 8:203-12; PMID:23288320; http://dx.doi.org/10.1038/nprot.2012.156
   PubMed Web of Science ®Google Scholar
• Funk WD, Labat I, Sampathkumar J, Gourraud PA, Oksenberg JR, Rosler E, Steiger D, Sheibani N, Caillier S, Stache-Crain B, et al. Evaluating the genomic and sequence integrity of human ES cell lines; comparison to normal genomes. Stem Cell Res 2012; 8:154-64; PMID:22265736; http://dx.doi.org/10.1016/j.scr.2011.10.001
   PubMed Web of Science ®Google Scholar
• Maitra A, Arking DE, Shivapurkar N, Ikeda M, Stastny V, Kassauei K, Sui G, Cutler DJ, Liu Y, Brimble SN, et al. Genomic alterations in cultured human embryonic stem cells. Nat Genet 2005; 37:1099-103; PMID:16142235; http://dx.doi.org/10.1038/ng1631
   PubMed Web of Science ®Google Scholar
• Therizols P, Illingworth RS, Courilleau C, Boyle S, Wood AJ, Bickmore WA. Chromatin decondensation is sufficient to alter nuclear organization in embryonic stem cells. Science 2014; 346:1238-42; PMID:25477464; http://dx.doi.org/10.1126/science.1259587
   PubMed Web of Science ®Google Scholar
• Lee HJ, Hore TA, Reik W. Reprogramming the methylome: erasing memory and creating diversity. Cell Stem Cell 2014; 14:710-9; PMID:24905162; http://dx.doi.org/10.1016/j.stem.2014.05.008
   PubMed Web of Science ®Google Scholar
• Gopalakrishnan S, Van Emburgh BO, Robertson KD. DNA methylation in development and human disease. Mutat Res 2008; 647:30-8; PMID:18778722; http://dx.doi.org/10.1016/j.mrfmmm.2008.08.006
   PubMed Web of Science ®Google Scholar
• Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009; 462:315-22; PMID:19829295; http://dx.doi.org/10.1038/nature08514
   PubMed Web of Science ®Google Scholar
• Xiao S, Xie D, Cao X, Yu P, Xing X, Chen CC, Musselman M, Xie M, West FD, Lewin HA, et al. Comparative epigenomic annotation of regulatory DNA. Cell 2012; 149:1381-92; PMID:22682255; http://dx.doi.org/10.1016/j.cell.2012.04.029
   PubMed Web of Science ®Google Scholar
• Hiratani I, Gilbert DM. Replication timing as an epigenetic mark. Epigenetics : official journal of the DNA Methylation Society 2009; 4:93-7; http://dx.doi.org/10.4161/epi.4.2.7772
   PubMed Web of Science ®Google Scholar
• Consortium EP, Dunham I, Kundaje A, Aldred SF, Collins PJ, Davis CA, Doyle F, Epstein CB, Frietze S, Harrow J, et al. An integrated encyclopedia of DNA elements in the human genome. Nature 2012; 489:57-74; PMID:22955616; http://dx.doi.org/10.1038/nature11247
   PubMed Web of Science ®Google Scholar
• Hu G, Cui K, Northrup D, Liu C, Wang C, Tang Q, Ge K, Levens D, Crane-Robinson C, Zhao K. H2A.Z Facilitates Access of Active and Repressive Complexes to Chromatin in Embryonic Stem Cell Self-Renewal and Differentiation. Cell Stem Cell 2013; 12:180-92; PMID:23260488; http://dx.doi.org/10.1016/j.stem.2012.11.003
   PubMed Web of Science ®Google Scholar
• Laurent L, Wong E, Li G, Huynh T, Tsirigos A, Ong CT, Low HM, Kin Sung KW, Rigoutsos I, Loring J, et al. Dynamic changes in the human methylome during differentiation. Genome Res 2010; 20:320-31; PMID:20133333; http://dx.doi.org/10.1101/gr.101907.109
   PubMed Web of Science ®Google Scholar
• Biterge B, Schneider R. Histone variants: key players of chromatin. Cell Tissue Res 2014; 356:457-66; PMID:24781148; http://dx.doi.org/10.1007/s00441-014-1862-4
   PubMed Web of Science ®Google Scholar
• Combes AN, Whitelaw E. Epigenetic reprogramming: enforcer or enabler of developmental fate? Dev Growth Differ 2010; 52:483-91; PMID:20608951; http://dx.doi.org/10.1111/j.1440-169X.2010.01185.x
   PubMed Web of Science ®Google Scholar
• Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, Fry B, Meissner A, Wernig M, Plath K, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006; 125:315-26; PMID:16630819; http://dx.doi.org/10.1016/j.cell.2006.02.041
   PubMed Web of Science ®Google Scholar
• Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G, Alvarez P, Brockman W, Kim TK, Koche RP, et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007; 448:553-60; PMID:17603471; http://dx.doi.org/10.1038/nature06008
   PubMed Web of Science ®Google Scholar
• Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W, Zhao K. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 2009; 4:80-93; PMID:19128795; http://dx.doi.org/10.1016/j.stem.2008.11.011
   PubMed Web of Science ®Google Scholar
• Ruzov A, Tsenkina Y, Serio A, Dudnakova T, Fletcher J, Bai Y, Chebotareva T, Pells S, Hannoun Z, Sullivan G, et al. Lineage-specific distribution of high levels of genomic 5-hydroxymethylcytosine in mammalian development. Cell Res 2011; 21:1332-42; PMID:21747414; http://dx.doi.org/10.1038/cr.2011.113
   PubMed Web of Science ®Google Scholar
• Wu H, D'Alessio AC, Ito S, Wang Z, Cui K, Zhao K, Sun YE, Zhang Y. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev 2011; 25:679-84; PMID:21460036; http://dx.doi.org/10.1101/gad.2036011
   PubMed Web of Science ®Google Scholar
• Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, Marques CJ, Andrews S, Reik W. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 2011; 473:398-402; PMID:21460836; http://dx.doi.org/10.1038/nature10008
   PubMed Web of Science ®Google Scholar
• Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, Laiho A, Tahiliani M, Sommer CA, Mostoslavsky G, et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 2011; 8:200-13; PMID:21295276; http://dx.doi.org/10.1016/j.stem.2011.01.008
   PubMed Web of Science ®Google Scholar
• Zhao XD, Han X, Chew JL, Liu J, Chiu KP, Choo A, Orlov YL, Sung WK, Shahab A, Kuznetsov VA, et al. Whole-genome mapping of histone H3 Lys4 and 27 trimethylations reveals distinct genomic compartments in human embryonic stem cells. Cell Stem Cell 2007; 1:286-98; PMID:18371363; http://dx.doi.org/10.1016/j.stem.2007.08.004
   PubMed Web of Science ®Google Scholar
• Peric-Hupkes D, Meuleman W, Pagie L, Bruggeman SW, Solovei I, Brugman W, Graf S, Flicek P, Kerkhoven RM, van Lohuizen M, et al. Molecular maps of the reorganization of genome-nuclear lamina interactions during differentiation. Mol Cell 2010; 38:603-13; PMID:20513434; http://dx.doi.org/10.1016/j.molcel.2010.03.016
   PubMed Web of Science ®Google Scholar
• Richmond TJ, Davey CA. The structure of DNA in the nucleosome core. Nature 2003; 423:145-50; PMID:12736678; http://dx.doi.org/10.1038/nature01595
   PubMed Web of Science ®Google Scholar
• Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997; 389:251-60; PMID:9305837; http://dx.doi.org/10.1038/38444
   PubMed Web of Science ®Google Scholar
• Venters BJ, Pugh BF. How eukaryotic genes are transcribed. Crit Rev Biochem Mol 2009; 44:117-41; http://dx.doi.org/10.1080/10409230902858785
   PubMed Web of Science ®Google Scholar
• North JA, Amunugama R, Klajner M, Bruns AN, Poirier MG, Fishel R. ATP-dependent nucleosome unwrapping catalyzed by human RAD51. Nucleic Acids Res 2013; 41:7302-12; PMID:23757189; http://dx.doi.org/10.1093/nar/gkt411
   PubMed Web of Science ®Google Scholar
• Chadwick BP, Willard HF. Barring gene expression after XIST: maintaining facultative heterochromatin on the inactive X. Semin Cell Dev Biol 2003; 14:359-67; PMID:15015743; http://dx.doi.org/10.1016/j.semcdb.2003.09.016
   PubMed Web of Science ®Google Scholar
• Schones DE, Cui K, Cuddapah S, Roh TY, Barski A, Wang Z, Wei G, Zhao K. Dynamic regulation of nucleosome positioning in the human genome. Cell 2008; 132:887-98; PMID:18329373; http://dx.doi.org/10.1016/j.cell.2008.02.022
   PubMed Web of Science ®Google Scholar
• Ozsolak F, Song JS, Liu XS, Fisher DE. High-throughput mapping of the chromatin structure of human promoters. Nat Biotechnol 2007; 25:244-8; PMID:17220878; http://dx.doi.org/10.1038/nbt1279
   PubMed Web of Science ®Google Scholar
• Jiang C, Pugh BF. Nucleosome positioning and gene regulation: advances through genomics. Nature Rev Genet 2009; 10:161-72; PMID:19204718; http://dx.doi.org/10.1038/nrg2522
   PubMed Web of Science ®Google Scholar
• Teif VB, Vainshtein Y, Caudron-Herger M, Mallm JP, Marth C, Hofer T, Rippe K. Genome-wide nucleosome positioning during embryonic stem cell development. Nat Struct Mol Biol 2012; 19:1185-92; PMID:23085715; http://dx.doi.org/10.1038/nsmb.2419
   PubMed Web of Science ®Google Scholar
• Gaffney DJ, McVicker G, Pai AA, Fondufe-Mittendorf YN, Lewellen N, Michelini K, Widom J, Gilad Y, Pritchard JK. Controls of nucleosome positioning in the human genome. PLoS Genet 2012; 8:e1003036; PMID:23166509; http://dx.doi.org/10.1371/journal.pgen.1003036
   PubMed Web of Science ®Google Scholar
• Valouev A, Johnson SM, Boyd SD, Smith CL, Fire AZ, Sidow A. Determinants of nucleosome organization in primary human cells. Nature 2011; 474:516-20; PMID:21602827; http://dx.doi.org/10.1038/nature10002
   PubMed Web of Science ®Google Scholar
• Prendergast JG, Semple CA. Widespread signatures of recent selection linked to nucleosome positioning in the human lineage. Genome Res 2011; 21:1777-87; PMID:21903742; http://dx.doi.org/10.1101/gr.122275.111
   PubMed Web of Science ®Google Scholar
• Struhl K, Segal E. Determinants of nucleosome positioning. Nat Struct Mol Biol 2013; 20:267-73; PMID:23463311; http://dx.doi.org/10.1038/nsmb.2506
   PubMed Web of Science ®Google Scholar
• West JA, Cook A, Alver BH, Stadtfeld M, Deaton AM, Hochedlinger K, Park PJ, Tolstorukov MY, Kingston RE. Nucleosomal occupancy changes locally over key regulatory regions during cell differentiation and reprogramming. Nat Commun 2014; 5:4719; PMID:25158628; http://dx.doi.org/10.1038/ncomms5719
   PubMed Web of Science ®Google Scholar
• Hainer SJ, Fazzio TG. Regulation of Nucleosome Architecture and Factor Binding Revealed by Nuclease Footprinting of the ESC Genome. Cell Rep 2015; 13:61-9; PMID:26411677; http://dx.doi.org/10.1016/j.celrep.2015.08.071
   PubMed Web of Science ®Google Scholar
• Teif VB, Beshnova DA, Vainshtein Y, Marth C, Mallm JP, Hofer T, Rippe K. Nucleosome repositioning links DNA (de)methylation and differential CTCF binding during stem cell development. Genome Res 2014; 24:1285-95; PMID:24812327; http://dx.doi.org/10.1101/gr.164418.113
   PubMed Web of Science ®Google Scholar
• Thurman RE, Rynes E, Humbert R, Vierstra J, Maurano MT, Haugen E, Sheffield NC, Stergachis AB, Wang H, Vernot B, et al. The accessible chromatin landscape of the human genome. Nature 2012; 489:75-82; PMID:22955617; http://dx.doi.org/10.1038/nature11232
   PubMed Web of Science ®Google Scholar
• Zhong JLK, Winter PS, Crawford GE, Iversen ES, Hartemink AJ. Mapping nucleosome positions using DNase-seq. Genome Res 2016; 26:351-64; PMID:26772197
   PubMed Web of Science ®Google Scholar
• Galan A, Diaz-Gimeno P, Poo ME, Valbuena D, Sanchez E, Ruiz V, Dopazo J, Montaner D, Conesa A, Simon C. Defining the Genomic Signature of Totipotency and Pluripotency during Early Human Development. PloS One 2013; 8:e62135; PMID:23614026; http://dx.doi.org/10.1371/journal.pone.0062135
   PubMedGoogle Scholar
• Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, Moore IK, Wang JP, Widom J. A genomic code for nucleosome positioning. Nature 2006; 442:772-8; PMID:16862119; http://dx.doi.org/10.1038/nature04979
   PubMed Web of Science ®Google Scholar
• Sharova LV, Sharov AA, Nedorezov T, Piao Y, Shaik N, Ko MS. Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res 2009; 16:45-58; PMID:19001483; http://dx.doi.org/10.1093/dnares/dsn030
   PubMed Web of Science ®Google Scholar
• Rada-Iglesias A, Bajpai R, Swigut T, Brugmann SA, Flynn RA, Wysocka J. A unique chromatin signature uncovers early developmental enhancers in humans. Nature 2011; 470:279-83; PMID:21160473; http://dx.doi.org/10.1038/nature09692
   PubMed Web of Science ®Google Scholar
• Hnisz D, Abraham BJ, Lee TI, Lau A, Saint-Andre V, Sigova AA, Hoke HA, Young RA. Super-enhancers in the control of cell identity and disease. Cell 2013; 155:934-47; PMID:24119843; http://dx.doi.org/10.1016/j.cell.2013.09.053
   PubMed Web of Science ®Google Scholar
• Chodavarapu RK, Feng S, Bernatavichute YV, Chen PY, Stroud H, Yu Y, Hetzel JA, Kuo F, Kim J, Cokus SJ, et al. Relationship between nucleosome positioning and DNA methylation. Nature 2010; 466:388-92; PMID:20512117; http://dx.doi.org/10.1038/nature09147
   PubMed Web of Science ®Google Scholar
• Kaplan N, Moore IK, Fondufe-Mittendorf Y, Gossett AJ, Tillo D, Field Y, LeProust EM, Hughes TR, Lieb JD, Widom J, et al. The DNA-encoded nucleosome organization of a eukaryotic genome. Nature 2009; 458:362-6; PMID:19092803; http://dx.doi.org/10.1038/nature07667
   PubMed Web of Science ®Google Scholar
• Xing K, He XL. Mutation Bias, rather than Binding Preference, Underlies the Nucleosome-Associated G plus C% Variation in Eukaryotes. Genome Biol Evol 2015; 7:1033-8; PMID:25786433; http://dx.doi.org/10.1093/gbe/evv053
   PubMed Web of Science ®Google Scholar
• Tillo D, Hughes TR. G+C content dominates intrinsic nucleosome occupancy. BMC Bioinformatics 2009; 10:442; PMID:20028554; http://dx.doi.org/10.1186/1471-2105-10-442
   PubMed Web of Science ®Google Scholar
• International Stem Cell I, Amps K, Andrews PW, Anyfantis G, Armstrong L, Avery S, Baharvand H, Baker J, Baker D, Munoz MB, et al. Screening ethnically diverse human embryonic stem cells identifies a chromosome 20 minimal amplicon conferring growth advantage. Nat Biotechnol 2011; 29:1132-44; PMID:22119741; http://dx.doi.org/10.1038/nbt.2051
   PubMed Web of Science ®Google Scholar
• Wang J, Wang W, Li R, Li Y, Tian G, Goodman L, Fan W, Zhang J, Li J, Guo Y, et al. The diploid genome sequence of an Asian individual. Nature 2008; 456:60-5; PMID:18987735; http://dx.doi.org/10.1038/nature07484
   PubMed Web of Science ®Google Scholar
• Ley TJ, Mardis ER, Ding L, Fulton B, McLellan MD, Chen K, Dooling D, Dunford-Shore BH, McGrath S, Hickenbotham M, et al. DNA sequencing of a cytogenetically normal acute myeloid leukaemia genome. Nature 2008; 456:66-72; PMID:18987736; http://dx.doi.org/10.1038/nature07485
   PubMed Web of Science ®Google Scholar
• Locke G, Haberman D, Johnson SM, Morozov AV. Global remodeling of nucleosome positions in C. elegans. BMC genomics 2013; 14:284; PMID:23622142; http://dx.doi.org/10.1186/1471-2164-14-284
   PubMed Web of Science ®Google Scholar
• Dixon JR, Jung I, Selvaraj S, Shen Y, Antosiewicz-Bourget JE, Lee AY, Ye Z, Kim A, Rajagopal N, Xie W, et al. Chromatin architecture reorganization during stem cell differentiation. Nature 2015; 518:331-6; PMID:25693564; http://dx.doi.org/10.1038/nature14222
   PubMed Web of Science ®Google Scholar
• Bregman A, Avraham-Kelbert M, Barkai O, Duek L, Guterman A, Choder M. Promoter elements regulate cytoplasmic mRNA decay. Cell 2011; 147:1473-83; PMID:22196725; http://dx.doi.org/10.1016/j.cell.2011.12.005
   PubMed Web of Science ®Google Scholar
• Trcek T, Larson DR, Moldon A, Query CC, Singer RH. Single-molecule mRNA decay measurements reveal promoter- regulated mRNA stability in yeast. Cell 2011; 147:1484-97; PMID:22196726; http://dx.doi.org/10.1016/j.cell.2011.11.051
   PubMed Web of Science ®Google Scholar
• Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Borresen-Dale AL, et al. Signatures of mutational processes in human cancer. Nature 2013; 500:415-21; PMID:23945592; http://dx.doi.org/10.1038/nature12477
   PubMed Web of Science ®Google Scholar
• Allan J, Fraser RM, Owen-Hughes T, Keszenman-Pereyra D. Micrococcal Nuclease Does Not Substantially Bias Nucleosome Mapping. J Mol Biol 2012; 417:152-64; PMID:22310051; http://dx.doi.org/10.1016/j.jmb.2012.01.043
   PubMed Web of Science ®Google Scholar
• Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; 3:Article3; PMID:16646809; http://dx.doi.org/10.2202/1544-6115.1027
   PubMedGoogle Scholar
• Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001; 125:279-84; PMID:11682119; http://dx.doi.org/10.1016/S0166-4328(01)00297-2
   PubMed Web of Science ®Google Scholar
• Spetman B, Lueking S, Roberts B, Dennis JH. Microarray mapping of nucleosome position. Epigenetics: A Reference Manual. J Craig and N Wong, eds, Norwich, UK: Horizon Scientific Press, 2011
   Google Scholar
• Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25:1754-60; PMID:19451168; http://dx.doi.org/10.1093/bioinformatics/btp324
   PubMed Web of Science ®Google Scholar
• Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4:44-57; PMID:19131956; http://dx.doi.org/10.1038/nprot.2008.211
   PubMed Web of Science ®Google Scholar
• Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078-9; PMID:19505943; http://dx.doi.org/10.1093/bioinformatics/btp352
   PubMed Web of Science ®Google Scholar
• McKenna A, Hanna M, Banks E, Sivachenko A, Cibulskis K, Kernytsky A, Garimella K, Altshuler D, Gabriel S, Daly M, et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20:1297-303; PMID:20644199; http://dx.doi.org/10.1101/gr.107524.110
   PubMed Web of Science ®Google Scholar
• Tang J, Le S, Sun L, Yan X, Zhang M, Macleod J, Leroy B, Northrup N, Ellis A, Yeatman TJ, et al. Copy number abnormalities in sporadic canine colorectal cancers. Genome Res 2010; 20:341-50; PMID:20086242; http://dx.doi.org/10.1101/gr.092726.109
   PubMed Web of Science ®Google Scholar
• Liu D, Xiong H, Ellis AE, Northrup NC, Dobbin KK, Shin DM, Zhao S. Canine spontaneous head and neck squamous cell carcinomas represent their human counterparts at the molecular level. PLoS Genet 2015; 11:e1005277; PMID:26030765; http://dx.doi.org/10.1371/journal.pgen.1005277
   PubMedGoogle Scholar
• Liu D, Xiong H, Ellis AE, Northrup NC, Rodriguez CO, Jr., O'Regan RM, Dalton S, Zhao S. Molecular homology and difference between spontaneous canine mammary cancer and human breast cancer. Cancer Res 2014; 74:5045-56; PMID:25082814
   PubMed Web of Science ®Google Scholar