Accurate prediction of cis-regulatory modules reveals a prevalent regulatory genome of humans

Abstract cis-regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying phenotypes of humans. It is essential to categorize all CRMs and constituent TFBSs in the genome. In contrast to most existing methods that p...

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Published inNAR genomics and bioinformatics Vol. 3; no. 2; p. lqab052
Main Authors Ni, Pengyu, Su, Zhengchang
Format Journal Article
LanguageEnglish
Published Oxford Oxford University Press 01.06.2021
Subjects
Enhancers
Epigenetics
Genomes
Phenotypes
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ISSN2631-9268
2631-9268
DOI10.1093/nargab/lqab052

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Abstract Abstract cis-regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying phenotypes of humans. It is essential to categorize all CRMs and constituent TFBSs in the genome. In contrast to most existing methods that predict CRMs in specific cell types using epigenetic marks, we predict a largely cell type agonistic but more comprehensive map of CRMs and constituent TFBSs in the gnome by integrating all available TF ChIP-seq datasets. Our method is able to partition 77.47% of genome regions covered by available 6092 datasets into a CRM candidate (CRMC) set (56.84%) and a non-CRMC set (43.16%). Intriguingly, the predicted CRMCs are under strong evolutionary constraints, while the non-CRMCs are largely selectively neutral, strongly suggesting that the CRMCs are likely cis-regulatory, while the non-CRMCs are not. Our predicted CRMs are under stronger evolutionary constraints than three state-of-the-art predictions (GeneHancer, EnhancerAtlas and ENCODE phase 3) and substantially outperform them for recalling VISTA enhancers and non-coding ClinVar variants. We estimated that the human genome might encode about 1.47M CRMs and 68M TFBSs, comprising about 55% and 22% of the genome, respectively; for both of which, we predicted 80%. Therefore, the cis-regulatory genome appears to be more prevalent than originally thought.
AbstractList cis -regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying phenotypes of humans. It is essential to categorize all CRMs and constituent TFBSs in the genome. In contrast to most existing methods that predict CRMs in specific cell types using epigenetic marks, we predict a largely cell type agonistic but more comprehensive map of CRMs and constituent TFBSs in the gnome by integrating all available TF ChIP-seq datasets. Our method is able to partition 77.47% of genome regions covered by available 6092 datasets into a CRM candidate (CRMC) set (56.84%) and a non-CRMC set (43.16%). Intriguingly, the predicted CRMCs are under strong evolutionary constraints, while the non-CRMCs are largely selectively neutral, strongly suggesting that the CRMCs are likely cis -regulatory, while the non-CRMCs are not. Our predicted CRMs are under stronger evolutionary constraints than three state-of-the-art predictions (GeneHancer, EnhancerAtlas and ENCODE phase 3) and substantially outperform them for recalling VISTA enhancers and non-coding ClinVar variants. We estimated that the human genome might encode about 1.47M CRMs and 68M TFBSs, comprising about 55% and 22% of the genome, respectively; for both of which, we predicted 80%. Therefore, the cis -regulatory genome appears to be more prevalent than originally thought.
Abstract cis-regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying phenotypes of humans. It is essential to categorize all CRMs and constituent TFBSs in the genome. In contrast to most existing methods that predict CRMs in specific cell types using epigenetic marks, we predict a largely cell type agonistic but more comprehensive map of CRMs and constituent TFBSs in the gnome by integrating all available TF ChIP-seq datasets. Our method is able to partition 77.47% of genome regions covered by available 6092 datasets into a CRM candidate (CRMC) set (56.84%) and a non-CRMC set (43.16%). Intriguingly, the predicted CRMCs are under strong evolutionary constraints, while the non-CRMCs are largely selectively neutral, strongly suggesting that the CRMCs are likely cis-regulatory, while the non-CRMCs are not. Our predicted CRMs are under stronger evolutionary constraints than three state-of-the-art predictions (GeneHancer, EnhancerAtlas and ENCODE phase 3) and substantially outperform them for recalling VISTA enhancers and non-coding ClinVar variants. We estimated that the human genome might encode about 1.47M CRMs and 68M TFBSs, comprising about 55% and 22% of the genome, respectively; for both of which, we predicted 80%. Therefore, the cis-regulatory genome appears to be more prevalent than originally thought.
cis-regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying phenotypes of humans. It is essential to categorize all CRMs and constituent TFBSs in the genome. In contrast to most existing methods that predict CRMs in specific cell types using epigenetic marks, we predict a largely cell type agonistic but more comprehensive map of CRMs and constituent TFBSs in the gnome by integrating all available TF ChIP-seq datasets. Our method is able to partition 77.47% of genome regions covered by available 6092 datasets into a CRM candidate (CRMC) set (56.84%) and a non-CRMC set (43.16%). Intriguingly, the predicted CRMCs are under strong evolutionary constraints, while the non-CRMCs are largely selectively neutral, strongly suggesting that the CRMCs are likely cis-regulatory, while the non-CRMCs are not. Our predicted CRMs are under stronger evolutionary constraints than three state-of-the-art predictions (GeneHancer, EnhancerAtlas and ENCODE phase 3) and substantially outperform them for recalling VISTA enhancers and non-coding ClinVar variants. We estimated that the human genome might encode about 1.47M CRMs and 68M TFBSs, comprising about 55% and 22% of the genome, respectively; for both of which, we predicted 80%. Therefore, the cis-regulatory genome appears to be more prevalent than originally thought.
cis-regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying phenotypes of humans. It is essential to categorize all CRMs and constituent TFBSs in the genome. In contrast to most existing methods that predict CRMs in specific cell types using epigenetic marks, we predict a largely cell type agonistic but more comprehensive map of CRMs and constituent TFBSs in the gnome by integrating all available TF ChIP-seq datasets. Our method is able to partition 77.47% of genome regions covered by available 6092 datasets into a CRM candidate (CRMC) set (56.84%) and a non-CRMC set (43.16%). Intriguingly, the predicted CRMCs are under strong evolutionary constraints, while the non-CRMCs are largely selectively neutral, strongly suggesting that the CRMCs are likely cis-regulatory, while the non-CRMCs are not. Our predicted CRMs are under stronger evolutionary constraints than three state-of-the-art predictions (GeneHancer, EnhancerAtlas and ENCODE phase 3) and substantially outperform them for recalling VISTA enhancers and non-coding ClinVar variants. We estimated that the human genome might encode about 1.47M CRMs and 68M TFBSs, comprising about 55% and 22% of the genome, respectively; for both of which, we predicted 80%. Therefore, the cis-regulatory genome appears to be more prevalent than originally thought.
cis-regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying phenotypes of humans. It is essential to categorize all CRMs and constituent TFBSs in the genome. In contrast to most existing methods that predict CRMs in specific cell types using epigenetic marks, we predict a largely cell type agonistic but more comprehensive map of CRMs and constituent TFBSs in the gnome by integrating all available TF ChIP-seq datasets. Our method is able to partition 77.47% of genome regions covered by available 6092 datasets into a CRM candidate (CRMC) set (56.84%) and a non-CRMC set (43.16%). Intriguingly, the predicted CRMCs are under strong evolutionary constraints, while the non-CRMCs are largely selectively neutral, strongly suggesting that the CRMCs are likely cis-regulatory, while the non-CRMCs are not. Our predicted CRMs are under stronger evolutionary constraints than three state-of-the-art predictions (GeneHancer, EnhancerAtlas and ENCODE phase 3) and substantially outperform them for recalling VISTA enhancers and non-coding ClinVar variants. We estimated that the human genome might encode about 1.47M CRMs and 68M TFBSs, comprising about 55% and 22% of the genome, respectively; for both of which, we predicted 80%. Therefore, the cis-regulatory genome appears to be more prevalent than originally thought.cis-regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying phenotypes of humans. It is essential to categorize all CRMs and constituent TFBSs in the genome. In contrast to most existing methods that predict CRMs in specific cell types using epigenetic marks, we predict a largely cell type agonistic but more comprehensive map of CRMs and constituent TFBSs in the gnome by integrating all available TF ChIP-seq datasets. Our method is able to partition 77.47% of genome regions covered by available 6092 datasets into a CRM candidate (CRMC) set (56.84%) and a non-CRMC set (43.16%). Intriguingly, the predicted CRMCs are under strong evolutionary constraints, while the non-CRMCs are largely selectively neutral, strongly suggesting that the CRMCs are likely cis-regulatory, while the non-CRMCs are not. Our predicted CRMs are under stronger evolutionary constraints than three state-of-the-art predictions (GeneHancer, EnhancerAtlas and ENCODE phase 3) and substantially outperform them for recalling VISTA enhancers and non-coding ClinVar variants. We estimated that the human genome might encode about 1.47M CRMs and 68M TFBSs, comprising about 55% and 22% of the genome, respectively; for both of which, we predicted 80%. Therefore, the cis-regulatory genome appears to be more prevalent than originally thought.
Author Su, Zhengchang
Ni, Pengyu
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  email: zcsu@uncc.edu
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Cites_doi 10.1093/nar/gkj115
10.1186/gb-2007-8-2-r24
10.1093/bioinformatics/btw495
10.1371/journal.pgen.1004857
10.1038/nmeth.3065
10.1093/nar/gkt829
10.1016/j.febslet.2015.11.027
10.1016/j.cell.2007.05.009
10.1007/978-1-61779-361-5_15
10.1038/nmeth0410-250
10.1038/nature11247
10.1371/journal.pgen.1004525
10.1093/nar/gkl822
10.1126/science.1098119
10.1126/science.1262110
10.1101/gr.139881.112
10.1101/gr.249326.119
10.1101/gad.310367.117
10.1093/nar/gks1092
10.1016/j.tig.2012.09.007
10.1093/nar/gkx920
10.1101/gr.173518.114
10.1016/j.celrep.2018.03.129
10.1093/nar/gkt1302
10.1016/j.cell.2015.01.006
10.1038/ejhg.2013.96
10.1089/10665270360688219
10.1093/nar/gkw983
10.1038/nrg3458
10.1038/msb.2010.35
10.1093/nar/gks433
10.1038/nmeth.1906
10.1126/science.1242429
10.1126/science.1090005
10.1093/nar/gky338
10.1038/nmeth.2688
10.1038/nsmb.2784
10.3389/fgene.2017.00063
10.1038/ng.2007.55
10.1126/science.1141319
10.1016/j.gde.2016.10.007
10.1038/nature12787
10.1186/s13059-019-1750-z
10.1126/science.1242510
10.1182/blood-2002-04-1104
10.1093/bioinformatics/btz290
10.1093/nar/gkv1002
10.1093/gbe/evt028
10.1371/journal.pgen.1008827
10.1093/nar/29.1.281
10.1158/2159-8290.CD-16-0745
10.1073/pnas.1318948111
10.2217/epi-2017-0157
10.1016/j.gde.2014.08.011
10.1186/s13072-015-0009-5
10.1093/nar/gkw1133
10.1093/nar/gks1284
10.1186/s13059-017-1379-8
10.1101/gr.116814.110
10.1016/j.tig.2014.12.003
10.1038/nrg3891
10.1016/j.molcel.2010.05.004
10.1016/j.cell.2012.01.030
10.1080/21541264.2017.1317694
10.1126/science.1242463
10.1145/2700404
10.1038/onc.2015.352
10.1186/s13059-020-01996-3
10.1093/nar/gky1120
10.1038/nrg.2015.17
10.1016/j.molcel.2014.02.033
10.1038/s41586-020-2449-8
10.1093/bib/bbv101
10.1093/database/bay141
10.1186/1752-0509-7-S2-S14
10.1093/nar/gkt1249
10.1016/j.cell.2014.08.009
10.1016/j.ydbio.2011.03.007
10.1016/j.cell.2013.07.020
10.1186/gb-2009-10-3-r29
10.1093/bioinformatics/btr261
10.1074/jbc.C000773200
10.1038/s41586-020-2493-4
10.1038/nrg2538
10.1016/j.cell.2012.12.009
10.1186/1471-2164-15-1047
10.1002/jcb.20352
10.1093/nar/gkz483
10.1073/pnas.1016071107
10.1371/journal.pcbi.1002968
10.1093/database/bax028
10.1038/nature11232
10.1093/nar/gks1233
10.1038/nature13602
10.1002/pro.3978
10.1534/g3.113.008680
10.1093/nar/gkx1106
10.1093/gbe/evx121
10.1186/s13059-015-0621-5
10.1073/pnas.0903103106
10.1016/j.cell.2018.09.045
10.1073/pnas.1808833115
10.1038/nbt.2422
10.1093/nar/gkx1153
10.1098/rstb.2013.0017
10.1186/1471-2105-9-547
10.1093/database/bav085
10.1016/j.cell.2006.12.048
10.1038/s41576-019-0209-0
10.1101/gr.1562804
10.1038/nmeth.1937
10.1038/nature13182
10.1093/gbe/evaa040
10.1093/nar/gks237
10.1093/nar/gkx1092
10.1371/journal.pbio.0030007
10.1093/bioinformatics/btq248
10.1093/nar/gku1058
10.1038/nature14248
10.1093/bioinformatics/btr189
10.1016/j.cell.2013.09.053
10.1186/1471-2164-14-S5-S2
10.1093/nar/gkr341
10.1093/nar/gkv1176
10.1111/pcmr.12149
10.1126/science.1222794
10.1101/gr.3642605
10.1101/gr.097857.109
10.1038/s41467-018-07746-1
10.1186/gb-2012-13-9-r48
10.1126/science.1142430
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References Pollard (2021070810414566000_B108) 2010; 20
Zhou (2021070810414566000_B17) 2016; 6
Young (2021070810414566000_B116) 2017; 18
Yanez-Cuna (2021070810414566000_B77) 2013; 29
Khan (2021070810414566000_B120) 2015; 44
Galeota-Sprung (2021070810414566000_B134) 2020; 12
Johnson (2021070810414566000_B25) 2007; 316
Liu (2021070810414566000_B32) 2001; 2001
Chereji (2021070810414566000_B117) 2019; 29
Devailly (2021070810414566000_B103) 2015; 589
Kleftogiannis (2021070810414566000_B53) 2015; 43
Kulakovskiy (2021070810414566000_B93) 2018; 46
Davidson (2021070810414566000_B1) 2006
Hartmann (2021070810414566000_B35) 2013; 23
Whitaker (2021070810414566000_B18) 2015; 12
Heinz (2021070810414566000_B36) 2010; 38
Junion (2021070810414566000_B39) 2012; 148
Aday (2021070810414566000_B65) 2011; 357
Rands (2021070810414566000_B137) 2014; 10
Sánchez-Tilló (2021070810414566000_B100) 2015; 34
Ambrosini (2021070810414566000_B97) 2020; 21
Wilderman (2021070810414566000_B123) 2018; 23
Kellis (2021070810414566000_B127) 2014; 111
Cheneby (2021070810414566000_B62) 2018; 46
Arnosti (2021070810414566000_B76) 2005; 94
Visel (2021070810414566000_B110) 2008; 40
MacArthur (2021070810414566000_B118) 2017; 45
Ashoor (2021070810414566000_B56) 2015; 2015
Stergachis (2021070810414566000_B104) 2013; 154
Pai (2021070810414566000_B21) 2015; 11
Buenrostro (2021070810414566000_B64) 2013; 10
Vockley (2021070810414566000_B78) 2017; 43
Wang (2021070810414566000_B19) 2019; 47
van Dongen (2021070810414566000_B89) 2012; 804
Consortium (2021070810414566000_B28) 2015; 348
Kleftogiannis (2021070810414566000_B30) 2016; 17
Hindorff (2021070810414566000_B6) 2009; 106
Ongen (2021070810414566000_B15) 2014; 512
Gupta (2021070810414566000_B95) 2007; 8
Bailey (2021070810414566000_B31) 1994; 2
Whitington (2021070810414566000_B40) 2011; 39
Graur (2021070810414566000_B138) 2017; 9
Lambert (2021070810414566000_B96) 2018; 175
Dreos (2021070810414566000_B121) 2013; 41
Rubinstein (2021070810414566000_B4) 2013; 368
Visel (2021070810414566000_B79) 2007; 35
Woolfe (2021070810414566000_B114) 2005; 3
Gao (2021070810414566000_B61) 2020; 48
Zhang (2021070810414566000_B60) 2018; 46
Yip (2021070810414566000_B45) 2012; 13
Kundaje (2021070810414566000_B27) 2015; 518
Niu (2021070810414566000_B75) 2014; 15
Snetkova (2021070810414566000_B91) 2018; 10
Chen (2021070810414566000_B58) 2020; 48
Kang (2021070810414566000_B59) 2019; 2019
Vaquerizas (2021070810414566000_B131) 2009; 10
Arbel (2021070810414566000_B71) 2019; 116
Hoffman (2021070810414566000_B124) 2012; 9
Fishilevich (2021070810414566000_B57) 2017; 2017
Landrum (2021070810414566000_B80) 2018; 46
King (2021070810414566000_B3) 1975; 188
Ernst (2021070810414566000_B49) 2012; 9
Buniello (2021070810414566000_B83) 2019; 47
Wang (2021070810414566000_B129) 2018; 9
Kheradpour (2021070810414566000_B46) 2014; 42
Pennacchio (2021070810414566000_B126) 2013; 14
Rajagopal (2021070810414566000_B52) 2013; 9
Firpi (2021070810414566000_B51) 2010; 26
Kwasnieski (2021070810414566000_B68) 2014; 24
Ponting (2021070810414566000_B135) 2011; 21
Smith (2021070810414566000_B12) 2014; 21
Li (2021070810414566000_B73) 2019; 35
Siepel (2021070810414566000_B5) 2014; 29
Catarino (2021070810414566000_B70) 2018; 32
Maurano (2021070810414566000_B8) 2012; 337
Li (2021070810414566000_B92) 2002; 100
Snyder (2021070810414566000_B128) 2020; 583
Machanick (2021070810414566000_B34) 2011; 27
Marinov (2021070810414566000_B102) 2014; 4
Cooper (2021070810414566000_B109) 2010; 7
Niu (2021070810414566000_B48) 2014; 15
Herz (2021070810414566000_B14) 2014; 53
Vlieghe (2021070810414566000_B44) 2006; 34
Soundarajan (2021070810414566000_B86) 2015; 9
Khurana (2021070810414566000_B16) 2016; 17
Zerbino (2021070810414566000_B55) 2015; 16
Mathelier (2021070810414566000_B13) 2015; 31
Bejerano (2021070810414566000_B111) 2004; 304
Graur (2021070810414566000_B133) 2013; 5
Hoffman (2021070810414566000_B50) 2013; 41
Won (2021070810414566000_B54) 2008; 9
Villar (2021070810414566000_B115) 2015; 160
Gao (2021070810414566000_B125) 2016; 32
Barski (2021070810414566000_B24) 2007; 129
Goi (2021070810414566000_B72) 2013; 14
Sinha (2021070810414566000_B37) 2003; 10
Sun (2021070810414566000_B41) 2012; 40
Kim (2021070810414566000_B67) 2007; 128
Gasperini (2021070810414566000_B23) 2020; 21
Oughtred (2021070810414566000_B84) 2021; 30
Hnisz (2021070810414566000_B106) 2013; 155
Huber (2021070810414566000_B139) 2020; 16
Li (2021070810414566000_B113) 2019; 20
Wilczynski (2021070810414566000_B2) 2010; 6
Mei (2021070810414566000_B29) 2017; 45
Fulton (2021070810414566000_B130) 2009; 10
Ward (2021070810414566000_B20) 2012; 30
Kilpinen (2021070810414566000_B10) 2013; 342
Koyabu (2021070810414566000_B99) 2001; 276
Wingender (2021070810414566000_B43) 2001; 29
Dimitrieva (2021070810414566000_B122) 2013; 41
Weirauch (2021070810414566000_B87) 2014; 158
Creyghton (2021070810414566000_B66) 2010; 107
Li (2021070810414566000_B105) 2017; 8
Vockley (2021070810414566000_B90) 2017; 8
Kasowski (2021070810414566000_B9) 2013; 342
Moore (2021070810414566000_B26) 2020; 583
Zhang (2021070810414566000_B88) 2013; 7
Bernstein (2021070810414566000_B119) 2012; 489
Thurman (2021070810414566000_B63) 2012; 489
Bailey (2021070810414566000_B33) 2011; 27
Allen (2021070810414566000_B74) 2004; 14
King (2021070810414566000_B136) 2005; 15
Niu (2021070810414566000_B47) 2018; 46
Andersson (2021070810414566000_B81) 2014; 507
Albert (2021070810414566000_B22) 2015; 16
McVicker (2021070810414566000_B11) 2013; 342
Jiang (2021070810414566000_B42) 2014; 42
Cooper (2021070810414566000_B107) 2010; 7
Katzman (2021070810414566000_B112) 2007; 317
Jassal (2021070810414566000_B85) 2020; 48
Perrot (2021070810414566000_B98) 2013; 26
Bailey (2021070810414566000_B38) 2012; 40
Mendoza-Parra (2021070810414566000_B101) 2013; 41
Mathelier (2021070810414566000_B94) 2016; 44
Ramos (2021070810414566000_B7) 2014; 22
Dogan (2021070810414566000_B69) 2015; 8
Forrest (2021070810414566000_B82) 2014; 507
Jolma (2021070810414566000_B132) 2013; 152
References_xml – volume: 34
  start-page: D95
  year: 2006
  ident: 2021070810414566000_B44
  article-title: A new generation of JASPAR, the open-access repository for transcription factor binding site profiles
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkj115
– volume: 8
  start-page: R24
  year: 2007
  ident: 2021070810414566000_B95
  article-title: Quantifying similarity between motifs
  publication-title: Genome Biol.
  doi: 10.1186/gb-2007-8-2-r24
– volume: 32
  start-page: 3543
  year: 2016
  ident: 2021070810414566000_B125
  article-title: EnhancerAtlas: a resource for enhancer annotation and analysis in 105 human cell/tissue types
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btw495
– volume: 11
  start-page: e1004857
  year: 2015
  ident: 2021070810414566000_B21
  article-title: The genetic and mechanistic basis for variation in gene regulation
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1004857
– volume: 12
  start-page: 265
  year: 2015
  ident: 2021070810414566000_B18
  article-title: Predicting the human epigenome from DNA motifs
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.3065
– volume: 41
  start-page: e196
  year: 2013
  ident: 2021070810414566000_B101
  article-title: A quality control system for profiles obtained by ChIP sequencing
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkt829
– volume: 589
  start-page: 3866
  year: 2015
  ident: 2021070810414566000_B103
  article-title: Variable reproducibility in genome-scale public data: a case study using ENCODE ChIP sequencing resource
  publication-title: FEBS Lett.
  doi: 10.1016/j.febslet.2015.11.027
– volume: 129
  start-page: 823
  year: 2007
  ident: 2021070810414566000_B24
  article-title: High-resolution profiling of histone methylations in the human genome
  publication-title: Cell
  doi: 10.1016/j.cell.2007.05.009
– volume: 804
  start-page: 281
  year: 2012
  ident: 2021070810414566000_B89
  article-title: Using MCL to extract clusters from networks
  publication-title: Methods Mol. Biol.
  doi: 10.1007/978-1-61779-361-5_15
– volume: 7
  start-page: 250
  year: 2010
  ident: 2021070810414566000_B109
  article-title: Single-nucleotide evolutionary constraint scores highlight disease-causing mutations
  publication-title: Nat. Methods
  doi: 10.1038/nmeth0410-250
– volume: 489
  start-page: 57
  year: 2012
  ident: 2021070810414566000_B119
  article-title: An integrated encyclopedia of DNA elements in the human genome
  publication-title: Nature
  doi: 10.1038/nature11247
– volume: 10
  start-page: e1004525
  year: 2014
  ident: 2021070810414566000_B137
  article-title: 8.2% of the Human genome is constrained: variation in rates of turnover across functional element classes in the human lineage
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1004525
– volume: 35
  start-page: D88
  year: 2007
  ident: 2021070810414566000_B79
  article-title: VISTA Enhancer Browser – a database of tissue-specific human enhancers
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkl822
– volume: 304
  start-page: 1321
  year: 2004
  ident: 2021070810414566000_B111
  article-title: Ultraconserved elements in the human genome
  publication-title: Science
  doi: 10.1126/science.1098119
– volume: 348
  start-page: 648
  year: 2015
  ident: 2021070810414566000_B28
  article-title: Human genomics. The Genotype-Tissue Expression (GTEx) pilot analysis: multitissue gene regulation in humans
  publication-title: Science
  doi: 10.1126/science.1262110
– volume: 23
  start-page: 181
  year: 2013
  ident: 2021070810414566000_B35
  article-title: P-value-based regulatory motif discovery using positional weight matrices
  publication-title: Genome Res.
  doi: 10.1101/gr.139881.112
– volume: 29
  start-page: 1985
  year: 2019
  ident: 2021070810414566000_B117
  article-title: Accessibility of promoter DNA is not the primary determinant of chromatin-mediated gene regulation
  publication-title: Genome Res.
  doi: 10.1101/gr.249326.119
– volume: 32
  start-page: 202
  year: 2018
  ident: 2021070810414566000_B70
  article-title: Assessing sufficiency and necessity of enhancer activities for gene expression and the mechanisms of transcription activation
  publication-title: Genes Dev.
  doi: 10.1101/gad.310367.117
– volume: 41
  start-page: D101
  year: 2013
  ident: 2021070810414566000_B122
  article-title: UCNEbase–a database of ultraconserved non-coding elements and genomic regulatory blocks
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gks1092
– volume: 29
  start-page: 11
  year: 2013
  ident: 2021070810414566000_B77
  article-title: Deciphering the transcriptional cis-regulatory code
  publication-title: Trends Genet.
  doi: 10.1016/j.tig.2012.09.007
– volume: 46
  start-page: D78
  year: 2018
  ident: 2021070810414566000_B60
  article-title: DiseaseEnhancer: a resource of human disease-associated enhancer catalog
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkx920
– volume: 24
  start-page: 1595
  year: 2014
  ident: 2021070810414566000_B68
  article-title: High-throughput functional testing of ENCODE segmentation predictions
  publication-title: Genome Res.
  doi: 10.1101/gr.173518.114
– volume: 23
  start-page: 1581
  year: 2018
  ident: 2021070810414566000_B123
  article-title: High-resolution epigenomic atlas of human embryonic craniofacial development
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2018.03.129
– volume: 42
  start-page: 2833
  year: 2014
  ident: 2021070810414566000_B42
  article-title: CCAT: Combinatorial Code Analysis Tool for transcriptional regulation
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkt1302
– volume: 160
  start-page: 554
  year: 2015
  ident: 2021070810414566000_B115
  article-title: Enhancer evolution across 20 mammalian species
  publication-title: Cell
  doi: 10.1016/j.cell.2015.01.006
– volume: 22
  start-page: 144
  year: 2014
  ident: 2021070810414566000_B7
  article-title: Phenotype-Genotype Integrator (PheGenI): synthesizing genome-wide association study (GWAS) data with existing genomic resources
  publication-title: Eur. J. Hum. Genet.
  doi: 10.1038/ejhg.2013.96
– volume: 10
  start-page: 599
  year: 2003
  ident: 2021070810414566000_B37
  article-title: Discriminative motifs
  publication-title: J. Comput. Biol.
  doi: 10.1089/10665270360688219
– volume: 45
  start-page: D658
  year: 2017
  ident: 2021070810414566000_B29
  article-title: Cistrome Data Browser: a data portal for ChIP-Seq and chromatin accessibility data in human and mouse
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkw983
– volume: 14
  start-page: 288
  year: 2013
  ident: 2021070810414566000_B126
  article-title: Enhancers: five essential questions
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg3458
– volume: 6
  start-page: 383
  year: 2010
  ident: 2021070810414566000_B2
  article-title: Dynamic CRM occupancy reflects a temporal map of developmental progression
  publication-title: Mol. Syst. Biol.
  doi: 10.1038/msb.2010.35
– volume: 40
  start-page: e128
  year: 2012
  ident: 2021070810414566000_B38
  article-title: Inferring direct DNA binding from ChIP-seq
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gks433
– volume: 9
  start-page: 215
  year: 2012
  ident: 2021070810414566000_B49
  article-title: ChromHMM: automating chromatin-state discovery and characterization
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.1906
– volume: 342
  start-page: 747
  year: 2013
  ident: 2021070810414566000_B11
  article-title: Identification of genetic variants that affect histone modifications in human cells
  publication-title: Science
  doi: 10.1126/science.1242429
– volume: 188
  start-page: 107
  year: 1975
  ident: 2021070810414566000_B3
  article-title: Evolution at two levels in humans and chimpanzees
  publication-title: Science
  doi: 10.1126/science.1090005
– volume: 46
  start-page: 5395
  year: 2018
  ident: 2021070810414566000_B47
  article-title: Towards a map of cis-regulatory sequences in the human genome
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gky338
– volume: 10
  start-page: 1213
  year: 2013
  ident: 2021070810414566000_B64
  article-title: Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.2688
– volume: 21
  start-page: 210
  year: 2014
  ident: 2021070810414566000_B12
  article-title: Enhancer biology and enhanceropathies
  publication-title: Nat. Struct. Mol. Biol.
  doi: 10.1038/nsmb.2784
– volume: 8
  start-page: 63
  year: 2017
  ident: 2021070810414566000_B105
  article-title: An enhancer's length and composition are shaped by Its regulatory task
  publication-title: Front Genet
  doi: 10.3389/fgene.2017.00063
– volume: 40
  start-page: 158
  year: 2008
  ident: 2021070810414566000_B110
  article-title: Ultraconservation identifies a small subset of extremely constrained developmental enhancers
  publication-title: Nat. Genet.
  doi: 10.1038/ng.2007.55
– volume: 316
  start-page: 1497
  year: 2007
  ident: 2021070810414566000_B25
  article-title: Genome-wide mapping of in vivo protein-DNA interactions
  publication-title: Science
  doi: 10.1126/science.1141319
– volume: 43
  start-page: 38
  year: 2017
  ident: 2021070810414566000_B78
  article-title: Decoding the role of regulatory element polymorphisms in complex disease
  publication-title: Curr. Opin. Genet. Dev.
  doi: 10.1016/j.gde.2016.10.007
– volume: 507
  start-page: 455
  year: 2014
  ident: 2021070810414566000_B81
  article-title: An atlas of active enhancers across human cell types and tissues
  publication-title: Nature
  doi: 10.1038/nature12787
– volume: 20
  start-page: 140
  year: 2019
  ident: 2021070810414566000_B113
  article-title: Stable enhancers are active in development, and fragile enhancers are associated with evolutionary adaptation
  publication-title: Genome Biol.
  doi: 10.1186/s13059-019-1750-z
– volume: 342
  start-page: 750
  year: 2013
  ident: 2021070810414566000_B9
  article-title: Extensive variation in chromatin states across humans
  publication-title: Science
  doi: 10.1126/science.1242510
– volume: 100
  start-page: 3077
  year: 2002
  ident: 2021070810414566000_B92
  article-title: Locus control regions
  publication-title: Blood
  doi: 10.1182/blood-2002-04-1104
– volume: 35
  start-page: 4632
  year: 2019
  ident: 2021070810414566000_B73
  article-title: ProSampler: an ultra-fast and accurate motif finder in large ChIP-seq datasets for combinatory motif discovery
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btz290
– volume: 44
  start-page: D164
  year: 2015
  ident: 2021070810414566000_B120
  article-title: dbSUPER: a database of super-enhancers in mouse and human genome
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkv1002
– volume: 5
  start-page: 578
  year: 2013
  ident: 2021070810414566000_B133
  article-title: On the immortality of television sets: “function” in the human genome according to the evolution-free gospel of ENCODE
  publication-title: Genome Biol. Evol.
  doi: 10.1093/gbe/evt028
– volume: 16
  start-page: e1008827
  year: 2020
  ident: 2021070810414566000_B139
  article-title: Population genetic models of GERP scores suggest pervasive turnover of constrained sites across mammalian evolution
  publication-title: PLoS Genet.
  doi: 10.1371/journal.pgen.1008827
– volume: 29
  start-page: 281
  year: 2001
  ident: 2021070810414566000_B43
  article-title: The TRANSFAC system on gene expression regulation
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/29.1.281
– volume: 6
  start-page: 1215
  year: 2016
  ident: 2021070810414566000_B17
  article-title: Emergence of the noncoding cancer genome: a target of genetic and epigenetic alterations
  publication-title: Cancer Discov.
  doi: 10.1158/2159-8290.CD-16-0745
– volume: 111
  start-page: 6131
  year: 2014
  ident: 2021070810414566000_B127
  article-title: Defining functional DNA elements in the human genome
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1318948111
– volume: 48
  start-page: D498
  year: 2020
  ident: 2021070810414566000_B85
  article-title: The reactome pathway knowledgebase
  publication-title: Nucleic Acids Res.
– volume: 10
  start-page: 483
  year: 2018
  ident: 2021070810414566000_B91
  article-title: Enhancer talk
  publication-title: Epigenomics
  doi: 10.2217/epi-2017-0157
– volume: 29
  start-page: 81
  year: 2014
  ident: 2021070810414566000_B5
  article-title: Cis-regulatory elements and human evolution
  publication-title: Curr. Opin. Genet. Dev.
  doi: 10.1016/j.gde.2014.08.011
– volume: 8
  start-page: 16
  year: 2015
  ident: 2021070810414566000_B69
  article-title: Occupancy by key transcription factors is a more accurate predictor of enhancer activity than histone modifications or chromatin accessibility
  publication-title: Epigenet. Chromatin
  doi: 10.1186/s13072-015-0009-5
– volume: 45
  start-page: D896
  year: 2017
  ident: 2021070810414566000_B118
  article-title: The new NHGRI-EBI Catalog of published genome-wide association studies (GWAS Catalog)
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkw1133
– volume: 41
  start-page: 827
  year: 2013
  ident: 2021070810414566000_B50
  article-title: Integrative annotation of chromatin elements from ENCODE data
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gks1284
– volume: 18
  start-page: 242
  year: 2017
  ident: 2021070810414566000_B116
  article-title: Bidirectional transcription initiation marks accessible chromatin and is not specific to enhancers
  publication-title: Genome Biol.
  doi: 10.1186/s13059-017-1379-8
– volume: 21
  start-page: 1769
  year: 2011
  ident: 2021070810414566000_B135
  article-title: What fraction of the human genome is functional
  publication-title: Genome Res.
  doi: 10.1101/gr.116814.110
– volume: 31
  start-page: 67
  year: 2015
  ident: 2021070810414566000_B13
  article-title: Identification of altered cis-regulatory elements in human disease
  publication-title: Trends Genet.
  doi: 10.1016/j.tig.2014.12.003
– volume: 16
  start-page: 197
  year: 2015
  ident: 2021070810414566000_B22
  article-title: The role of regulatory variation in complex traits and disease
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg3891
– volume: 38
  start-page: 576
  year: 2010
  ident: 2021070810414566000_B36
  article-title: Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2010.05.004
– volume: 148
  start-page: 473
  year: 2012
  ident: 2021070810414566000_B39
  article-title: A transcription factor collective defines cardiac cell fate and reflects lineage history
  publication-title: Cell
  doi: 10.1016/j.cell.2012.01.030
– volume: 8
  start-page: 261
  year: 2017
  ident: 2021070810414566000_B90
  article-title: A long-range flexible billboard model of gene activation
  publication-title: Transcription
  doi: 10.1080/21541264.2017.1317694
– volume: 342
  start-page: 744
  year: 2013
  ident: 2021070810414566000_B10
  article-title: Coordinated effects of sequence variation on DNA binding, chromatin structure, and transcription
  publication-title: Science
  doi: 10.1126/science.1242463
– volume: 9
  start-page: 21
  year: 2015
  ident: 2021070810414566000_B86
  article-title: Use of Local Group Information to Identify Communities in Networks
  publication-title: ACM Trans. Knowl. Discov. Data
  doi: 10.1145/2700404
– volume: 34
  start-page: 5760
  year: 2015
  ident: 2021070810414566000_B100
  article-title: ZEB1 and TCF4 reciprocally modulate their transcriptional activities to regulate Wnt target gene expression
  publication-title: Oncogene
  doi: 10.1038/onc.2015.352
– volume: 21
  start-page: 114
  year: 2020
  ident: 2021070810414566000_B97
  article-title: Insights gained from a comprehensive all-against-all transcription factor binding motif benchmarking study
  publication-title: Genome Biol.
  doi: 10.1186/s13059-020-01996-3
– volume: 47
  start-page: D1005
  year: 2019
  ident: 2021070810414566000_B83
  article-title: The NHGRI-EBI GWAS Catalog of published genome-wide association studies, targeted arrays and summary statistics 2019
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gky1120
– volume: 17
  start-page: 93
  year: 2016
  ident: 2021070810414566000_B16
  article-title: Role of non-coding sequence variants in cancer
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg.2015.17
– volume: 53
  start-page: 859
  year: 2014
  ident: 2021070810414566000_B14
  article-title: Enhancer malfunction in cancer
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2014.02.033
– volume: 583
  start-page: 693
  year: 2020
  ident: 2021070810414566000_B128
  article-title: Perspectives on ENCODE
  publication-title: Nature
  doi: 10.1038/s41586-020-2449-8
– volume: 17
  start-page: 967
  year: 2016
  ident: 2021070810414566000_B30
  article-title: Progress and challenges in bioinformatics approaches for enhancer identification
  publication-title: Brief. Bioinform.
  doi: 10.1093/bib/bbv101
– volume: 2019
  start-page: bay141
  year: 2019
  ident: 2021070810414566000_B59
  article-title: EnhancerDB: a resource of transcriptional regulation in the context of enhancers
  publication-title: Database (Oxford)
  doi: 10.1093/database/bay141
– volume: 7
  start-page: S14
  year: 2013
  ident: 2021070810414566000_B88
  article-title: SPIC: A novel information contents based similarity metric for comparing transcription factor binding site motifs
  publication-title: BMC Syst. Biol.
  doi: 10.1186/1752-0509-7-S2-S14
– volume: 42
  start-page: 2976
  year: 2014
  ident: 2021070810414566000_B46
  article-title: Systematic discovery and characterization of regulatory motifs in ENCODE TF binding experiments
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkt1249
– volume: 158
  start-page: 1431
  year: 2014
  ident: 2021070810414566000_B87
  article-title: Determination and inference of eukaryotic transcription factor sequence specificity
  publication-title: Cell
  doi: 10.1016/j.cell.2014.08.009
– volume: 357
  start-page: 450
  year: 2011
  ident: 2021070810414566000_B65
  article-title: Identification of cis regulatory features in the embryonic zebrafish genome through large-scale profiling of H3K4me1 and H3K4me3 binding sites
  publication-title: Dev. Biol.
  doi: 10.1016/j.ydbio.2011.03.007
– volume: 154
  start-page: 888
  year: 2013
  ident: 2021070810414566000_B104
  article-title: Developmental fate and cellular maturity encoded in human regulatory DNA landscapes
  publication-title: Cell
  doi: 10.1016/j.cell.2013.07.020
– volume: 10
  start-page: R29
  year: 2009
  ident: 2021070810414566000_B130
  article-title: TFCat: the curated catalog of mouse and human transcription factors
  publication-title: Genome Biol.
  doi: 10.1186/gb-2009-10-3-r29
– volume: 27
  start-page: 1653
  year: 2011
  ident: 2021070810414566000_B33
  article-title: DREME: motif discovery in transcription factor ChIP-seq data
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btr261
– volume: 2001
  start-page: 127
  year: 2001
  ident: 2021070810414566000_B32
  article-title: BioProspector: discovering conserved DNA motifs in upstream regulatory regions of co-expressed genes
  publication-title: Pac. Symp. Biocomput.
– volume: 276
  start-page: 6889
  year: 2001
  ident: 2021070810414566000_B99
  article-title: Physical and functional interactions between Zic and Gli proteins
  publication-title: J. Biol. Chem.
  doi: 10.1074/jbc.C000773200
– volume: 583
  start-page: 699
  year: 2020
  ident: 2021070810414566000_B26
  article-title: Expanded encyclopaedias of DNA elements in the human and mouse genomes
  publication-title: Nature
  doi: 10.1038/s41586-020-2493-4
– volume: 10
  start-page: 252
  year: 2009
  ident: 2021070810414566000_B131
  article-title: A census of human transcription factors: function, expression and evolution
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/nrg2538
– volume: 48
  start-page: D58
  year: 2020
  ident: 2021070810414566000_B61
  article-title: EnhancerAtlas 2.0: an updated resource with enhancer annotation in 586 tissue/cell types across nine species
  publication-title: Nucleic Acids Res.
– volume: 152
  start-page: 327
  year: 2013
  ident: 2021070810414566000_B132
  article-title: DNA-binding specificities of human transcription factors
  publication-title: Cell
  doi: 10.1016/j.cell.2012.12.009
– volume: 2
  start-page: 28
  year: 1994
  ident: 2021070810414566000_B31
  article-title: Fitting a mixture model by expectation maximization to discover motifs in biopolymers
  publication-title: Proc. Int. Conf. Intell. Syst. Mol. Biol.
– volume: 15
  start-page: 1047
  year: 2014
  ident: 2021070810414566000_B75
  article-title: De novo prediction of cis-regulatory elements and modules through integrative analysis of a large number of ChIP datasets
  publication-title: BMC Genomics
  doi: 10.1186/1471-2164-15-1047
– volume: 94
  start-page: 890
  year: 2005
  ident: 2021070810414566000_B76
  article-title: Transcriptional enhancers: Intelligent enhanceosomes or flexible billboards
  publication-title: J. Cell. Biochem.
  doi: 10.1002/jcb.20352
– volume: 47
  start-page: 6753
  year: 2019
  ident: 2021070810414566000_B19
  article-title: Identification of DNA motifs that regulate DNA methylation
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkz483
– volume: 107
  start-page: 21931
  year: 2010
  ident: 2021070810414566000_B66
  article-title: Histone H3K27ac separates active from poised enhancers and predicts developmental state
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1016071107
– volume: 9
  start-page: e1002968
  year: 2013
  ident: 2021070810414566000_B52
  article-title: RFECS: a random-forest based algorithm for enhancer identification from chromatin state
  publication-title: PLoS Comput. Biol.
  doi: 10.1371/journal.pcbi.1002968
– volume: 2017
  start-page: bax028
  year: 2017
  ident: 2021070810414566000_B57
  article-title: GeneHancer: genome-wide integration of enhancers and target genes in GeneCards
  publication-title: Database (Oxford)
  doi: 10.1093/database/bax028
– volume: 489
  start-page: 75
  year: 2012
  ident: 2021070810414566000_B63
  article-title: The accessible chromatin landscape of the human genome
  publication-title: Nature
  doi: 10.1038/nature11232
– volume: 41
  start-page: D157
  year: 2013
  ident: 2021070810414566000_B121
  article-title: EPD and EPDnew, high-quality promoter resources in the next-generation sequencing era
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gks1233
– volume: 512
  start-page: 87
  year: 2014
  ident: 2021070810414566000_B15
  article-title: Putative cis-regulatory drivers in colorectal cancer
  publication-title: Nature
  doi: 10.1038/nature13602
– volume: 30
  start-page: 187
  year: 2021
  ident: 2021070810414566000_B84
  article-title: The BioGRID database: a comprehensive biomedical resource of curated protein, genetic, and chemical interactions
  publication-title: Protein Sci.
  doi: 10.1002/pro.3978
– volume: 4
  start-page: 209
  year: 2014
  ident: 2021070810414566000_B102
  article-title: Large-scale quality analysis of published ChIP-seq data
  publication-title: G3 (Bethesda)
  doi: 10.1534/g3.113.008680
– volume: 46
  start-page: D252
  year: 2018
  ident: 2021070810414566000_B93
  article-title: HOCOMOCO: towards a complete collection of transcription factor binding models for human and mouse via large-scale ChIP-Seq analysis
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkx1106
– volume: 9
  start-page: 1880
  year: 2017
  ident: 2021070810414566000_B138
  article-title: An upper limit on the functional fraction of the human genome
  publication-title: Genome Biol Evol
  doi: 10.1093/gbe/evx121
– volume: 15
  start-page: 1047
  year: 2014
  ident: 2021070810414566000_B48
  article-title: De novo prediction of cis-regulatory elements and modules through integrative analysis of a large number of ChIP datasets
  publication-title: BMC Genomics
  doi: 10.1186/1471-2164-15-1047
– volume: 16
  start-page: 56
  year: 2015
  ident: 2021070810414566000_B55
  article-title: The ensembl regulatory build
  publication-title: Genome Biol.
  doi: 10.1186/s13059-015-0621-5
– volume: 106
  start-page: 9362
  year: 2009
  ident: 2021070810414566000_B6
  article-title: Potential etiologic and functional implications of genome-wide association loci for human diseases and traits
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.0903103106
– volume: 175
  start-page: 598
  year: 2018
  ident: 2021070810414566000_B96
  article-title: The human transcription factors
  publication-title: Cell
  doi: 10.1016/j.cell.2018.09.045
– volume: 116
  start-page: 900
  year: 2019
  ident: 2021070810414566000_B71
  article-title: Exploiting regulatory heterogeneity to systematically identify enhancers with high accuracy
  publication-title: Proc. Natl. Acad. Sci. U.S.A.
  doi: 10.1073/pnas.1808833115
– volume: 30
  start-page: 1095
  year: 2012
  ident: 2021070810414566000_B20
  article-title: Interpreting noncoding genetic variation in complex traits and human disease
  publication-title: Nat. Biotechnol.
  doi: 10.1038/nbt.2422
– volume: 46
  start-page: D1062
  year: 2018
  ident: 2021070810414566000_B80
  article-title: ClinVar: improving access to variant interpretations and supporting evidence
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkx1153
– volume: 368
  start-page: 20130017
  year: 2013
  ident: 2021070810414566000_B4
  article-title: Evolution of transcriptional enhancers and animal diversity
  publication-title: Philos. Trans. R. Soc. Lond. B Biol. Sci.
  doi: 10.1098/rstb.2013.0017
– volume: 9
  start-page: 547
  year: 2008
  ident: 2021070810414566000_B54
  article-title: Prediction of regulatory elements in mammalian genomes using chromatin signatures
  publication-title: BMC Bioinformatics
  doi: 10.1186/1471-2105-9-547
– volume: 2015
  start-page: bav085
  year: 2015
  ident: 2021070810414566000_B56
  article-title: DENdb: database of integrated human enhancers
  publication-title: Database
  doi: 10.1093/database/bav085
– volume: 128
  start-page: 1231
  year: 2007
  ident: 2021070810414566000_B67
  article-title: Analysis of the vertebrate insulator protein CTCF-binding sites in the human genome
  publication-title: Cell
  doi: 10.1016/j.cell.2006.12.048
– volume: 21
  start-page: 292
  year: 2020
  ident: 2021070810414566000_B23
  article-title: Towards a comprehensive catalogue of validated and target-linked human enhancers
  publication-title: Nat. Rev. Genet.
  doi: 10.1038/s41576-019-0209-0
– volume: 14
  start-page: 142
  year: 2004
  ident: 2021070810414566000_B74
  article-title: Computational gene prediction using multiple sources of evidence
  publication-title: Genome Res.
  doi: 10.1101/gr.1562804
– volume: 9
  start-page: 473
  year: 2012
  ident: 2021070810414566000_B124
  article-title: Unsupervised pattern discovery in human chromatin structure through genomic segmentation
  publication-title: Nat. Methods
  doi: 10.1038/nmeth.1937
– volume: 507
  start-page: 462
  year: 2014
  ident: 2021070810414566000_B82
  article-title: A promoter-level mammalian expression atlas
  publication-title: Nature
  doi: 10.1038/nature13182
– volume: 12
  start-page: 273
  year: 2020
  ident: 2021070810414566000_B134
  article-title: Mutational load and the functional fraction of the human genome
  publication-title: Genome Biol Evol
  doi: 10.1093/gbe/evaa040
– volume: 40
  start-page: e90
  year: 2012
  ident: 2021070810414566000_B41
  article-title: Unveiling combinatorial regulation through the combination of ChIP information and in silico cis-regulatory module detection
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gks237
– volume: 46
  start-page: D267
  year: 2018
  ident: 2021070810414566000_B62
  article-title: ReMap 2018: an updated atlas of regulatory regions from an integrative analysis of DNA-binding ChIP-seq experiments
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkx1092
– volume: 3
  start-page: e7
  year: 2005
  ident: 2021070810414566000_B114
  article-title: Highly conserved non-coding sequences are associated with vertebrate development
  publication-title: PLoS Biol.
  doi: 10.1371/journal.pbio.0030007
– volume-title: The Regulatory Genome: Gene Regulatory Networks In Development And Evolution
  year: 2006
  ident: 2021070810414566000_B1
– volume: 26
  start-page: 1579
  year: 2010
  ident: 2021070810414566000_B51
  article-title: Discover regulatory DNA elements using chromatin signatures and artificial neural network
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btq248
– volume: 43
  start-page: e6
  year: 2015
  ident: 2021070810414566000_B53
  article-title: DEEP: a general computational framework for predicting enhancers
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gku1058
– volume: 518
  start-page: 317
  year: 2015
  ident: 2021070810414566000_B27
  article-title: Integrative analysis of 111 reference human epigenomes
  publication-title: Nature
  doi: 10.1038/nature14248
– volume: 27
  start-page: 1696
  year: 2011
  ident: 2021070810414566000_B34
  article-title: MEME-ChIP: motif analysis of large DNA datasets
  publication-title: Bioinformatics
  doi: 10.1093/bioinformatics/btr189
– volume: 155
  start-page: 934
  year: 2013
  ident: 2021070810414566000_B106
  article-title: Super-enhancers in the control of cell identity and disease
  publication-title: Cell
  doi: 10.1016/j.cell.2013.09.053
– volume: 48
  start-page: D198
  year: 2020
  ident: 2021070810414566000_B58
  article-title: SEA version 3.0: a comprehensive extension and update of the Super-Enhancer archive
  publication-title: Nucleic Acids Res.
– volume: 14
  start-page: S2
  year: 2013
  ident: 2021070810414566000_B72
  article-title: Cell-type and transcription factor specific enrichment of transcriptional cofactor motifs in ENCODE ChIP-seq data
  publication-title: BMC Genomics
  doi: 10.1186/1471-2164-14-S5-S2
– volume: 39
  start-page: e98
  year: 2011
  ident: 2021070810414566000_B40
  article-title: Inferring transcription factor complexes from ChIP-seq data
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkr341
– volume: 44
  start-page: D110
  year: 2016
  ident: 2021070810414566000_B94
  article-title: JASPAR 2016: a major expansion and update of the open-access database of transcription factor binding profiles
  publication-title: Nucleic Acids Res.
  doi: 10.1093/nar/gkv1176
– volume: 26
  start-page: 861
  year: 2013
  ident: 2021070810414566000_B98
  article-title: GLI2 cooperates with ZEB1 for transcriptional repression of CDH1 expression in human melanoma cells
  publication-title: Pigment Cell Melanoma Res.
  doi: 10.1111/pcmr.12149
– volume: 337
  start-page: 1190
  year: 2012
  ident: 2021070810414566000_B8
  article-title: Systematic localization of common disease-associated variation in regulatory DNA
  publication-title: Science
  doi: 10.1126/science.1222794
– volume: 15
  start-page: 1051
  year: 2005
  ident: 2021070810414566000_B136
  article-title: Evaluation of regulatory potential and conservation scores for detecting cis-regulatory modules in aligned mammalian genome sequences
  publication-title: Genome Res.
  doi: 10.1101/gr.3642605
– volume: 20
  start-page: 110
  year: 2010
  ident: 2021070810414566000_B108
  article-title: Detection of nonneutral substitution rates on mammalian phylogenies
  publication-title: Genome Res.
  doi: 10.1101/gr.097857.109
– volume: 7
  start-page: 250
  year: 2010
  ident: 2021070810414566000_B107
  article-title: Single-nucleotide evolutionary constraint scores highlight disease-causing mutations
  publication-title: Nat. Methods
  doi: 10.1038/nmeth0410-250
– volume: 9
  start-page: 5380
  year: 2018
  ident: 2021070810414566000_B129
  article-title: High-resolution genome-wide functional dissection of transcriptional regulatory regions and nucleotides in human
  publication-title: Nat. Commun.
  doi: 10.1038/s41467-018-07746-1
– volume: 13
  start-page: R48
  year: 2012
  ident: 2021070810414566000_B45
  article-title: Classification of human genomic regions based on experimentally determined binding sites of more than 100 transcription-related factors
  publication-title: Genome Biol.
  doi: 10.1186/gb-2012-13-9-r48
– volume: 317
  start-page: 915
  year: 2007
  ident: 2021070810414566000_B112
  article-title: Human genome ultraconserved elements are ultraselected
  publication-title: Science
  doi: 10.1126/science.1142430
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Snippet Abstract cis-regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying...
cis-regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying...
cis-regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying...
cis -regulatory modules(CRMs) formed by clusters of transcription factor (TF) binding sites (TFBSs) are as important as coding sequences in specifying...
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SubjectTerms Enhancers
Epigenetics
Genomes
Phenotypes
Title Accurate prediction of cis-regulatory modules reveals a prevalent regulatory genome of humans
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https://www.proquest.com/docview/2544461306
https://pubmed.ncbi.nlm.nih.gov/PMC8210889
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