Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage

Heart development is exquisitely sensitive to the precise temporal regulation of thousands of genes that govern developmental decisions during differentiation. However, we currently lack a detailed understanding of how chromatin and gene expression patterns are coordinated during developmental trans...

Celý popis

Uložené v:
Podrobná bibliografia
Vydané v:Cell Ročník 151; číslo 1; s. 206
Hlavní autori: Wamstad, Joseph A, Alexander, Jeffrey M, Truty, Rebecca M, Shrikumar, Avanti, Li, Fugen, Eilertson, Kirsten E, Ding, Huiming, Wylie, John N, Pico, Alexander R, Capra, John A, Erwin, Genevieve, Kattman, Steven J, Keller, Gordon M, Srivastava, Deepak, Levine, Stuart S, Pollard, Katherine S, Holloway, Alisha K, Boyer, Laurie A, Bruneau, Benoit G
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States 28.09.2012
Predmet:
ISSN:1097-4172, 1097-4172
On-line prístup:Zistit podrobnosti o prístupe
Tagy: Pridať tag
Žiadne tagy, Buďte prvý, kto otaguje tento záznam!
Abstract Heart development is exquisitely sensitive to the precise temporal regulation of thousands of genes that govern developmental decisions during differentiation. However, we currently lack a detailed understanding of how chromatin and gene expression patterns are coordinated during developmental transitions in the cardiac lineage. Here, we interrogated the transcriptome and several histone modifications across the genome during defined stages of cardiac differentiation. We find distinct chromatin patterns that are coordinated with stage-specific expression of functionally related genes, including many human disease-associated genes. Moreover, we discover a novel preactivation chromatin pattern at the promoters of genes associated with heart development and cardiac function. We further identify stage-specific distal enhancer elements and find enriched DNA binding motifs within these regions that predict sets of transcription factors that orchestrate cardiac differentiation. Together, these findings form a basis for understanding developmentally regulated chromatin transitions during lineage commitment and the molecular etiology of congenital heart disease.
AbstractList Heart development is exquisitely sensitive to the precise temporal regulation of thousands of genes that govern developmental decisions during differentiation. However, we currently lack a detailed understanding of how chromatin and gene expression patterns are coordinated during developmental transitions in the cardiac lineage. Here, we interrogated the transcriptome and several histone modifications across the genome during defined stages of cardiac differentiation. We find distinct chromatin patterns that are coordinated with stage-specific expression of functionally related genes, including many human disease-associated genes. Moreover, we discover a novel preactivation chromatin pattern at the promoters of genes associated with heart development and cardiac function. We further identify stage-specific distal enhancer elements and find enriched DNA binding motifs within these regions that predict sets of transcription factors that orchestrate cardiac differentiation. Together, these findings form a basis for understanding developmentally regulated chromatin transitions during lineage commitment and the molecular etiology of congenital heart disease.Heart development is exquisitely sensitive to the precise temporal regulation of thousands of genes that govern developmental decisions during differentiation. However, we currently lack a detailed understanding of how chromatin and gene expression patterns are coordinated during developmental transitions in the cardiac lineage. Here, we interrogated the transcriptome and several histone modifications across the genome during defined stages of cardiac differentiation. We find distinct chromatin patterns that are coordinated with stage-specific expression of functionally related genes, including many human disease-associated genes. Moreover, we discover a novel preactivation chromatin pattern at the promoters of genes associated with heart development and cardiac function. We further identify stage-specific distal enhancer elements and find enriched DNA binding motifs within these regions that predict sets of transcription factors that orchestrate cardiac differentiation. Together, these findings form a basis for understanding developmentally regulated chromatin transitions during lineage commitment and the molecular etiology of congenital heart disease.
Heart development is exquisitely sensitive to the precise temporal regulation of thousands of genes that govern developmental decisions during differentiation. However, we currently lack a detailed understanding of how chromatin and gene expression patterns are coordinated during developmental transitions in the cardiac lineage. Here, we interrogated the transcriptome and several histone modifications across the genome during defined stages of cardiac differentiation. We find distinct chromatin patterns that are coordinated with stage-specific expression of functionally related genes, including many human disease-associated genes. Moreover, we discover a novel preactivation chromatin pattern at the promoters of genes associated with heart development and cardiac function. We further identify stage-specific distal enhancer elements and find enriched DNA binding motifs within these regions that predict sets of transcription factors that orchestrate cardiac differentiation. Together, these findings form a basis for understanding developmentally regulated chromatin transitions during lineage commitment and the molecular etiology of congenital heart disease.
Author Wamstad, Joseph A
Alexander, Jeffrey M
Kattman, Steven J
Holloway, Alisha K
Shrikumar, Avanti
Keller, Gordon M
Levine, Stuart S
Boyer, Laurie A
Truty, Rebecca M
Eilertson, Kirsten E
Wylie, John N
Bruneau, Benoit G
Ding, Huiming
Capra, John A
Li, Fugen
Pico, Alexander R
Pollard, Katherine S
Erwin, Genevieve
Srivastava, Deepak
Author_xml – sequence: 1
  givenname: Joseph A
  surname: Wamstad
  fullname: Wamstad, Joseph A
  organization: Department of Biology, Massachusetts Institute of Technology, Cambridge, 02139, USA
– sequence: 2
  givenname: Jeffrey M
  surname: Alexander
  fullname: Alexander, Jeffrey M
– sequence: 3
  givenname: Rebecca M
  surname: Truty
  fullname: Truty, Rebecca M
– sequence: 4
  givenname: Avanti
  surname: Shrikumar
  fullname: Shrikumar, Avanti
– sequence: 5
  givenname: Fugen
  surname: Li
  fullname: Li, Fugen
– sequence: 6
  givenname: Kirsten E
  surname: Eilertson
  fullname: Eilertson, Kirsten E
– sequence: 7
  givenname: Huiming
  surname: Ding
  fullname: Ding, Huiming
– sequence: 8
  givenname: John N
  surname: Wylie
  fullname: Wylie, John N
– sequence: 9
  givenname: Alexander R
  surname: Pico
  fullname: Pico, Alexander R
– sequence: 10
  givenname: John A
  surname: Capra
  fullname: Capra, John A
– sequence: 11
  givenname: Genevieve
  surname: Erwin
  fullname: Erwin, Genevieve
– sequence: 12
  givenname: Steven J
  surname: Kattman
  fullname: Kattman, Steven J
– sequence: 13
  givenname: Gordon M
  surname: Keller
  fullname: Keller, Gordon M
– sequence: 14
  givenname: Deepak
  surname: Srivastava
  fullname: Srivastava, Deepak
– sequence: 15
  givenname: Stuart S
  surname: Levine
  fullname: Levine, Stuart S
– sequence: 16
  givenname: Katherine S
  surname: Pollard
  fullname: Pollard, Katherine S
– sequence: 17
  givenname: Alisha K
  surname: Holloway
  fullname: Holloway, Alisha K
– sequence: 18
  givenname: Laurie A
  surname: Boyer
  fullname: Boyer, Laurie A
– sequence: 19
  givenname: Benoit G
  surname: Bruneau
  fullname: Bruneau, Benoit G
BackLink https://www.ncbi.nlm.nih.gov/pubmed/22981692$$D View this record in MEDLINE/PubMed
BookMark eNpNUMtOwzAQtFARfcAPcEA-ckmwnbixj6g8pUpc4Bxt7U1xldgldpD696SiSFx2VprRaGbmZOKDR0KuOcs548u7XW6wbXPBuMhZlbNCnpEZZ7rKSl6Jyb9_SuYx7hhjSkp5QaZCaMWXWswIPBw8dM5Q8JaaEHrrPCS0FPduix7TSPW4HVpILngaGmrxG9uw79AnaGnqwUd35CJ1nqZPpAZGEzC0dR5hi5fkvIE24tUJF-Tj6fF99ZKt355fV_frzJSKpww1CissFrowY8qNHRtiYzkX0BQgtR6PtE1ZqVKKRnNbaG0ZyKYwUjBVigW5_fXd9-FrwJjqzsXjQOAxDLHmTHFVlWqpRunNSTpsOrT1vncd9If6bxbxA0lzaJk
CitedBy_id crossref_primary_10_1371_journal_pone_0200229
crossref_primary_10_1002_jcp_30140
crossref_primary_10_1172_JCI158593
crossref_primary_10_3390_medicines5020048
crossref_primary_10_1242_dev_109496
crossref_primary_10_7554_eLife_31706
crossref_primary_10_14348_molcells_2015_0053
crossref_primary_10_1161_CIRCRESAHA_113_300939
crossref_primary_10_1038_nsmb_2881
crossref_primary_10_1016_j_tig_2015_11_002
crossref_primary_10_1016_j_tcb_2013_10_008
crossref_primary_10_1016_j_tig_2019_11_004
crossref_primary_10_1161_CIRCRESAHA_116_302832
crossref_primary_10_1371_journal_pgen_1006985
crossref_primary_10_1002_advs_202303799
crossref_primary_10_1038_cr_2013_78
crossref_primary_10_3389_fcell_2022_929256
crossref_primary_10_1016_j_semcdb_2021_11_011
crossref_primary_10_1016_j_envpol_2021_117567
crossref_primary_10_1111_cpr_12371
crossref_primary_10_1007_s00439_024_02703_z
crossref_primary_10_1016_j_ceb_2016_02_014
crossref_primary_10_1186_s13148_019_0679_0
crossref_primary_10_1038_srep01740
crossref_primary_10_1161_CIRCRESAHA_116_310456
crossref_primary_10_1371_journal_pcbi_1003677
crossref_primary_10_1038_nsmb_2653
crossref_primary_10_1038_nature12054
crossref_primary_10_1038_nmeth_2886
crossref_primary_10_1073_pnas_1315155110
crossref_primary_10_1016_j_stem_2015_10_003
crossref_primary_10_1038_s41569_021_00597_2
crossref_primary_10_1016_j_yjmcc_2014_08_009
crossref_primary_10_1038_nrg3607
crossref_primary_10_1371_journal_pone_0141066
crossref_primary_10_1016_j_gde_2013_07_002
crossref_primary_10_1371_journal_pgen_1004668
crossref_primary_10_1038_ncomms5361
crossref_primary_10_3390_jcdd8040042
crossref_primary_10_1161_CIRCRESAHA_120_317254
crossref_primary_10_1016_j_coisb_2017_04_001
crossref_primary_10_1080_15592294_2018_1526029
crossref_primary_10_1242_dev_171983
crossref_primary_10_1016_j_bcp_2025_116964
crossref_primary_10_1007_s00018_022_04590_x
crossref_primary_10_3389_fbioe_2020_637538
crossref_primary_10_1038_ncomms11275
crossref_primary_10_3389_fgene_2014_00375
crossref_primary_10_3389_fendo_2019_00601
crossref_primary_10_1038_s41467_017_02762_z
crossref_primary_10_1039_C6IB00040A
crossref_primary_10_3892_mmr_2018_9681
crossref_primary_10_1113_JP276072
crossref_primary_10_1186_s13287_016_0446_5
crossref_primary_10_1161_CIRCRESAHA_117_308428
crossref_primary_10_1083_jcb_1992pi
crossref_primary_10_1096_fba_2024_00080
crossref_primary_10_3390_jcdd10040166
crossref_primary_10_1038_s41467_021_23816_3
crossref_primary_10_1186_s13072_016_0063_7
crossref_primary_10_1146_annurev_genet_120213_092518
crossref_primary_10_3390_ijms251910824
crossref_primary_10_1016_j_cell_2013_06_020
crossref_primary_10_1371_journal_pone_0214677
crossref_primary_10_1016_j_yjmcc_2015_09_013
crossref_primary_10_1242_dev_200375
crossref_primary_10_1007_s13238_022_00908_4
crossref_primary_10_1016_j_stem_2019_11_011
crossref_primary_10_1186_s12915_021_01207_w
crossref_primary_10_1016_j_fct_2023_113653
crossref_primary_10_1016_j_omtn_2020_07_011
crossref_primary_10_1093_eurheartj_ehu180
crossref_primary_10_1093_stmcls_sxab017
crossref_primary_10_1161_CIRCRESAHA_112_300625
crossref_primary_10_3390_genes12101564
crossref_primary_10_1038_srep37637
crossref_primary_10_1161_CIRCRESAHA_116_309040
crossref_primary_10_1242_dmm_029967
crossref_primary_10_1186_s12864_021_08224_7
crossref_primary_10_1101_gr_276542_121
crossref_primary_10_1016_j_yjmcc_2015_09_016
crossref_primary_10_1016_j_ydbio_2020_07_003
crossref_primary_10_1101_gr_209486_116
crossref_primary_10_1002_jmr_2602
crossref_primary_10_1083_jcb_201701154
crossref_primary_10_1161_CIRCRESAHA_118_314063
crossref_primary_10_3390_cells12040520
crossref_primary_10_1186_s12943_016_0560_0
crossref_primary_10_1371_journal_pone_0161096
crossref_primary_10_3390_ijms22147720
crossref_primary_10_1161_CIR_0000000000000606
crossref_primary_10_1128_MCB_01172_14
crossref_primary_10_1016_j_molcel_2021_03_038
crossref_primary_10_1089_scd_2013_0125
crossref_primary_10_1161_CIRCRESAHA_113_303060
crossref_primary_10_1093_nar_gkt1232
crossref_primary_10_1016_j_molcel_2019_04_014
crossref_primary_10_1161_CIRCRESAHA_116_309140
crossref_primary_10_1016_j_mod_2016_12_002
crossref_primary_10_1186_s13293_019_0259_1
crossref_primary_10_1016_j_stem_2018_07_001
crossref_primary_10_1002_jcb_24570
crossref_primary_10_1126_science_1242429
crossref_primary_10_1016_j_bbagen_2016_04_008
crossref_primary_10_1002_stem_2646
crossref_primary_10_1038_nature12903
crossref_primary_10_1101_gad_225144_113
crossref_primary_10_1093_cvr_cvu122
crossref_primary_10_1093_nar_gkaa248
crossref_primary_10_1038_emboj_2013_134
crossref_primary_10_1016_j_bbagrm_2017_07_009
crossref_primary_10_1371_journal_pone_0194895
crossref_primary_10_1016_j_semcdb_2021_05_019
crossref_primary_10_1002_pmic_201400131
crossref_primary_10_1016_j_gde_2013_05_004
crossref_primary_10_1093_hmg_ddw216
crossref_primary_10_1038_s41588_018_0263_0
crossref_primary_10_1016_j_diff_2019_05_001
crossref_primary_10_1093_cvr_cvt166
crossref_primary_10_1002_dvdy_24441
crossref_primary_10_1016_j_molcel_2023_07_003
crossref_primary_10_3390_jcdd1010003
crossref_primary_10_1111_pbi_13836
crossref_primary_10_1038_s41598_019_42953_w
crossref_primary_10_1186_s12864_019_5637_x
crossref_primary_10_2217_epi_14_60
crossref_primary_10_1016_j_stem_2016_02_003
crossref_primary_10_1161_CIRCRESAHA_116_309877
crossref_primary_10_1016_j_stem_2016_02_001
crossref_primary_10_4161_21541272_2014_944014
crossref_primary_10_1038_s41556_022_00947_3
crossref_primary_10_1038_cr_2012_172
crossref_primary_10_1101_gad_207415_112
crossref_primary_10_1016_j_cell_2013_04_037
crossref_primary_10_1016_j_cell_2013_11_033
crossref_primary_10_1038_nrg3682
crossref_primary_10_1016_j_yjmcc_2013_05_008
crossref_primary_10_1016_j_molcel_2013_02_018
crossref_primary_10_1016_j_yjmcc_2018_02_003
crossref_primary_10_1016_j_yjmcc_2019_04_012
crossref_primary_10_1016_j_ebiom_2017_09_015
crossref_primary_10_1038_s41593_022_01123_4
crossref_primary_10_1002_dvg_22833
crossref_primary_10_1093_jmcb_mjae044
crossref_primary_10_1016_j_stem_2015_08_009
crossref_primary_10_1371_journal_pgen_1003725
crossref_primary_10_1016_j_rsci_2023_12_002
crossref_primary_10_1038_cr_2012_163
crossref_primary_10_1007_s00395_013_0361_1
crossref_primary_10_1002_prca_201400031
crossref_primary_10_1038_s41467_021_23660_5
crossref_primary_10_1097_MOT_0000000000000363
crossref_primary_10_1007_s11515_014_1340_0
crossref_primary_10_1016_j_lfs_2017_04_013
crossref_primary_10_1016_j_tcb_2016_11_010
crossref_primary_10_1161_CIRCRESAHA_115_307093
crossref_primary_10_1038_nprot_2016_153
crossref_primary_10_1016_j_exphem_2017_01_003
crossref_primary_10_3109_07853890_2014_959557
crossref_primary_10_1016_j_ydbio_2016_08_022
crossref_primary_10_1371_journal_pone_0138478
crossref_primary_10_5966_sctm_2014_0290
crossref_primary_10_3390_cells11030460
crossref_primary_10_1038_jhg_2015_84
crossref_primary_10_1002_jcb_25156
crossref_primary_10_1161_CIRCRESAHA_120_316704
crossref_primary_10_3390_cells10123297
crossref_primary_10_1038_s41467_024_45669_2
crossref_primary_10_2217_epi_13_67
crossref_primary_10_3389_fmolb_2021_685938
crossref_primary_10_1242_dev_185314
crossref_primary_10_1038_s41467_023_40606_1
crossref_primary_10_1016_j_ymthe_2021_10_015
crossref_primary_10_1038_srep24724
crossref_primary_10_1093_cvr_cvad059
crossref_primary_10_1002_ctd2_70087
crossref_primary_10_1016_j_yjmcc_2021_07_002
crossref_primary_10_1186_s12872_018_0939_5
crossref_primary_10_1038_s41467_021_21910_0
crossref_primary_10_1074_jbc_M115_672931
crossref_primary_10_1186_s13148_024_01709_8
crossref_primary_10_3390_cells11233915
crossref_primary_10_1016_j_stem_2013_06_006
crossref_primary_10_1038_s41422_019_0168_1
crossref_primary_10_1161_CIRCRESAHA_113_301134
crossref_primary_10_1038_s41467_017_00319_8
crossref_primary_10_1016_j_cell_2017_09_018
crossref_primary_10_15252_embj_201490542
crossref_primary_10_4161_epi_26405
crossref_primary_10_1007_s11033_018_4247_z
crossref_primary_10_3390_jcdd10070305
crossref_primary_10_1007_s11886_020_01280_7
crossref_primary_10_1016_j_devcel_2016_10_001
crossref_primary_10_1038_s42003_025_08160_2
crossref_primary_10_1002_jcb_26102
crossref_primary_10_1161_CIRCRESAHA_117_304156
crossref_primary_10_1093_bib_bby110
crossref_primary_10_7554_eLife_99026
crossref_primary_10_7554_eLife_55124
crossref_primary_10_1242_dev_185652
crossref_primary_10_1016_j_yjmcc_2014_05_002
crossref_primary_10_1016_j_molcel_2013_01_038
crossref_primary_10_1016_j_stem_2015_09_010
crossref_primary_10_1161_CIRCRESAHA_115_301517
crossref_primary_10_1016_j_jmb_2020_07_004
crossref_primary_10_7554_eLife_49921
crossref_primary_10_1371_journal_pcbi_1009368
crossref_primary_10_1038_s44318_025_00385_5
crossref_primary_10_7554_eLife_99026_3
crossref_primary_10_1101_gr_237073_118
crossref_primary_10_1038_s41551_022_00865_7
crossref_primary_10_7554_eLife_03848
crossref_primary_10_1186_1471_2164_14_914
crossref_primary_10_3389_fgene_2022_1011228
crossref_primary_10_1002_stem_1713
crossref_primary_10_1002_stem_1954
crossref_primary_10_1161_CIRCGENETICS_111_000043
crossref_primary_10_3389_fcell_2021_747842
crossref_primary_10_1016_j_stem_2012_10_009
crossref_primary_10_1371_journal_pone_0180096
crossref_primary_10_1016_j_cell_2013_01_003
crossref_primary_10_1016_j_tcm_2015_02_010
crossref_primary_10_1016_j_cardfail_2019_09_005
crossref_primary_10_3389_fcell_2021_680713
crossref_primary_10_1038_ng_3142
crossref_primary_10_1242_dev_138487
crossref_primary_10_1152_physrev_00001_2014
crossref_primary_10_1093_cvr_cvac040
crossref_primary_10_1126_scitranslmed_abe5407
crossref_primary_10_5966_sctm_2015_0136
crossref_primary_10_1007_s12519_016_0020_3
crossref_primary_10_1186_s13059_018_1485_2
crossref_primary_10_5713_ab_23_0402
crossref_primary_10_7554_eLife_65381
crossref_primary_10_1038_emboj_2013_71
crossref_primary_10_1038_s41594_021_00589_3
crossref_primary_10_1186_s12864_018_4886_4
crossref_primary_10_7554_eLife_83606
crossref_primary_10_1161_CIRCRESAHA_115_306337
crossref_primary_10_1101_gr_210930_116
crossref_primary_10_7554_eLife_31362
crossref_primary_10_1038_srep25194
crossref_primary_10_1242_dmm_046789
crossref_primary_10_1016_j_jbc_2025_108423
crossref_primary_10_1016_j_stem_2017_02_004
crossref_primary_10_1016_j_cellin_2022_100058
crossref_primary_10_3390_genes12071020
crossref_primary_10_1038_s41467_022_35063_1
crossref_primary_10_3389_fgene_2021_642975
crossref_primary_10_1155_2017_3464953
crossref_primary_10_1517_14728222_2014_1001740
crossref_primary_10_1096_fj_14_264093
crossref_primary_10_3389_fphys_2016_00418
crossref_primary_10_1016_j_stem_2018_04_013
crossref_primary_10_1161_CIRCRESAHA_113_302202
crossref_primary_10_1016_j_semcdb_2021_06_002
crossref_primary_10_1016_j_scr_2014_06_003
crossref_primary_10_1186_s12859_017_1828_0
crossref_primary_10_1002_stem_2196
crossref_primary_10_1016_j_omtn_2021_05_019
crossref_primary_10_3390_cells12182324
crossref_primary_10_1161_CIRCRESAHA_118_311597
crossref_primary_10_1113_jphysiol_2014_274712
crossref_primary_10_1371_journal_pone_0140831
crossref_primary_10_1038_ncomms9146
crossref_primary_10_1242_dev_178632
crossref_primary_10_3390_ijms22083914
crossref_primary_10_1016_j_tice_2024_102361
crossref_primary_10_1093_nar_gkw301
crossref_primary_10_15252_msb_20177754
crossref_primary_10_14814_phy2_13522
crossref_primary_10_1161_CIRCGENETICS_115_001264
crossref_primary_10_1242_dev_094789
crossref_primary_10_3389_fcell_2019_00358
crossref_primary_10_1002_dvdy_24366
crossref_primary_10_1186_s12859_015_0460_0
crossref_primary_10_1242_dmm_035972
crossref_primary_10_1016_j_tcm_2015_01_014
crossref_primary_10_1093_g3journal_jkaf012
crossref_primary_10_1038_s41467_020_15552_x
crossref_primary_10_1038_s41586_021_04336_y
crossref_primary_10_3390_jcdd5030037
crossref_primary_10_1016_j_ydbio_2017_03_030
crossref_primary_10_7554_eLife_07103
crossref_primary_10_1186_s12915_019_0709_6
crossref_primary_10_1093_toxsci_kfaa153
crossref_primary_10_1161_CIRCRESAHA_116_304269
crossref_primary_10_1016_j_omtn_2019_07_015
crossref_primary_10_1172_JCI88353
crossref_primary_10_1038_s41467_017_00667_5
crossref_primary_10_1016_j_cell_2013_09_011
crossref_primary_10_1161_CIRCRESAHA_116_308741
crossref_primary_10_1245_s10434_015_5024_z
crossref_primary_10_1038_cdd_2014_199
crossref_primary_10_3390_biomedicines13082044
crossref_primary_10_1155_2015_839590
crossref_primary_10_1038_ncomms9243
crossref_primary_10_1016_j_stem_2014_05_005
crossref_primary_10_1038_s44161_022_00124_7
crossref_primary_10_7554_eLife_22617
crossref_primary_10_15252_embj_201591206
crossref_primary_10_1016_j_ceb_2013_01_004
crossref_primary_10_1371_journal_pone_0173977
crossref_primary_10_26508_lsa_201800085
crossref_primary_10_1016_j_pharmthera_2024_108638
crossref_primary_10_7554_eLife_31683
crossref_primary_10_1038_s41598_017_13442_9
crossref_primary_10_15252_embj_201592655
crossref_primary_10_1371_journal_pcbi_1007337
crossref_primary_10_1016_j_cr_2018_11_002
crossref_primary_10_1016_j_molcel_2016_08_010
crossref_primary_10_1038_s41598_017_01628_0
crossref_primary_10_1038_s41467_017_01804_w
crossref_primary_10_3390_life13020569
crossref_primary_10_1038_nrcardio_2015_55
crossref_primary_10_1016_j_cell_2017_11_018
crossref_primary_10_1038_srep09758
crossref_primary_10_1161_CIRCGENETICS_113_000259
crossref_primary_10_1038_s44161_022_00129_2
crossref_primary_10_1186_s12864_015_1264_3
crossref_primary_10_1016_j_febslet_2015_04_055
crossref_primary_10_1038_s41467_018_07451_z
crossref_primary_10_1016_j_cell_2016_01_004
crossref_primary_10_1038_srep08790
crossref_primary_10_1186_scrt308
crossref_primary_10_1038_s42003_024_06017_8
crossref_primary_10_1016_j_stem_2018_02_005
crossref_primary_10_1242_dev_098327
crossref_primary_10_1101_gad_352306_124
crossref_primary_10_1371_journal_pone_0083364
crossref_primary_10_1242_dev_204384
crossref_primary_10_1007_s11886_017_0826_1
crossref_primary_10_1016_j_cell_2013_07_020
crossref_primary_10_1016_j_yjmcc_2019_01_019
crossref_primary_10_1016_j_cell_2022_11_026
crossref_primary_10_1016_j_yjmcc_2015_04_006
crossref_primary_10_1002_wsbm_1467
crossref_primary_10_1074_jbc_M116_719633
crossref_primary_10_1002_stem_3021
crossref_primary_10_1111_bjh_19721
crossref_primary_10_1007_s10741_019_09792_3
crossref_primary_10_1186_s13287_017_0638_7
crossref_primary_10_1016_j_stem_2015_12_001
crossref_primary_10_1016_j_cmet_2016_06_014
crossref_primary_10_1172_JCI153635
crossref_primary_10_3390_ijms141019987
crossref_primary_10_1016_j_devcel_2014_04_001
crossref_primary_10_3892_mmr_2014_2287
crossref_primary_10_1186_s13059_025_03658_8
crossref_primary_10_1002_stem_3027
crossref_primary_10_1007_s00441_014_2011_9
crossref_primary_10_1038_s41598_019_40867_1
crossref_primary_10_7717_peerj_2339
crossref_primary_10_7554_eLife_29330
crossref_primary_10_3390_ijms22168599
crossref_primary_10_1073_pnas_1608256113
crossref_primary_10_1038_celldisc_2016_36
crossref_primary_10_1371_journal_pgen_1003288
crossref_primary_10_1242_dev_132688
crossref_primary_10_1038_ncomms11688
crossref_primary_10_1016_j_molcel_2013_10_009
crossref_primary_10_1016_j_semcdb_2015_12_021
crossref_primary_10_1111_febs_15895
crossref_primary_10_1038_ncomms12418
crossref_primary_10_1016_j_bone_2014_12_063
crossref_primary_10_1101_gr_272468_120
crossref_primary_10_1002_dvdy_45
crossref_primary_10_1186_gb_2014_15_2_r32
crossref_primary_10_1161_CIRCGENETICS_113_000045
crossref_primary_10_1016_j_drudis_2013_10_019
crossref_primary_10_3390_jdb3040093
crossref_primary_10_1073_pnas_1808341116
crossref_primary_10_1002_stem_2111
crossref_primary_10_1242_dev_154146
crossref_primary_10_3389_fcvm_2018_00007
crossref_primary_10_1002_wsbm_1274
crossref_primary_10_1101_gad_240101_114
crossref_primary_10_1016_j_bbadis_2023_166689
crossref_primary_10_1007_s00335_021_09937_6
crossref_primary_10_1007_s11033_024_09657_5
crossref_primary_10_1016_j_stem_2019_03_022
crossref_primary_10_1093_nar_gkx234
crossref_primary_10_1093_nar_gkx232
crossref_primary_10_15252_emmm_201606558
crossref_primary_10_1016_j_devcel_2016_01_024
crossref_primary_10_1038_nature12141
crossref_primary_10_1038_srep41840
crossref_primary_10_1371_journal_pone_0102716
crossref_primary_10_1038_s41467_024_48362_6
crossref_primary_10_1016_j_bbamcr_2015_11_026
crossref_primary_10_1161_CIRCHEARTFAILURE_120_006926
crossref_primary_10_1007_s00018_016_2322_y
crossref_primary_10_1016_j_semcdb_2019_04_009
crossref_primary_10_1161_CIRCRESAHA_117_311367
crossref_primary_10_1098_rsob_160183
crossref_primary_10_1161_CIRCRESAHA_123_322676
crossref_primary_10_1038_ncomms6288
crossref_primary_10_1016_j_semcdb_2019_10_003
crossref_primary_10_1016_j_apsb_2019_09_003
crossref_primary_10_1161_CIRCHEARTFAILURE_114_001193
crossref_primary_10_1038_s41576_019_0184_5
crossref_primary_10_1038_s41556_021_00668_z
crossref_primary_10_1016_j_nbd_2016_11_007
crossref_primary_10_1016_j_yjmcc_2016_10_013
crossref_primary_10_1161_CIRCULATIONAHA_123_066804
crossref_primary_10_1161_CIRCULATIONAHA_117_029430
crossref_primary_10_3390_epigenomes5040021
crossref_primary_10_1186_s13059_021_02485_x
crossref_primary_10_1016_j_jmb_2019_02_012
crossref_primary_10_1002_2211_5463_13252
crossref_primary_10_1016_j_omtn_2023_07_033
crossref_primary_10_1038_ng_3970
crossref_primary_10_1002_wsbm_1268
crossref_primary_10_1016_j_ebiom_2016_01_021
crossref_primary_10_1002_dvdy_24075
crossref_primary_10_1007_s11010_020_03709_7
crossref_primary_10_1093_stmcls_sxac077
crossref_primary_10_3390_cells9030554
crossref_primary_10_7554_eLife_41769
crossref_primary_10_1016_j_cell_2015_02_035
crossref_primary_10_1111_febs_15468
crossref_primary_10_1007_s12015_015_9596_6
crossref_primary_10_1016_j_scr_2016_02_037
crossref_primary_10_1007_s12015_021_10314_8
crossref_primary_10_1371_journal_pone_0110498
crossref_primary_10_1038_ncomms7473
crossref_primary_10_3390_ph17030337
crossref_primary_10_1093_nar_gkae085
crossref_primary_10_1007_s00204_018_2166_3
crossref_primary_10_1002_wsbm_1287
crossref_primary_10_3390_biom10091204
crossref_primary_10_1016_j_gde_2015_02_008
crossref_primary_10_3390_children12050611
crossref_primary_10_3390_genes9060289
crossref_primary_10_1242_dev_174086
ContentType Journal Article
Copyright Copyright © 2012 Elsevier Inc. All rights reserved.
Copyright_xml – notice: Copyright © 2012 Elsevier Inc. All rights reserved.
DBID CGR
CUY
CVF
ECM
EIF
NPM
7X8
DOI 10.1016/j.cell.2012.07.035
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
MEDLINE - Academic
DatabaseTitleList MEDLINE - Academic
MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: 7X8
  name: MEDLINE - Academic
  url: https://search.proquest.com/medline
  sourceTypes: Aggregation Database
DeliveryMethod no_fulltext_linktorsrc
Discipline Biology
EISSN 1097-4172
ExternalDocumentID 22981692
Genre Research Support, Non-U.S. Gov't
Journal Article
Research Support, N.I.H., Extramural
GrantInformation_xml – fundername: NHLBI NIH HHS
  grantid: F32-HL104913
– fundername: NHLBI NIH HHS
  grantid: U01 HL098179
– fundername: NIGMS NIH HHS
  grantid: T32 GM067547
– fundername: NHLBI NIH HHS
  grantid: U01HL098179
– fundername: NHLBI NIH HHS
  grantid: F32 HL104913
GroupedDBID ---
--K
-DZ
-ET
-~X
0R~
0WA
1RT
1~5
29B
2FS
2WC
3EH
4.4
457
4G.
53G
5GY
5RE
5VS
62-
6J9
7-5
85S
9M8
AACTN
AAEDT
AAEDW
AAFWJ
AAHBH
AAIKJ
AAKRW
AAKUH
AALRI
AAMRU
AAQFI
AAVLU
AAXUO
AAYJJ
ABCQX
ABJNI
ABMAC
ABOCM
ABTAH
ACGFO
ACGFS
ACNCT
ADBBV
ADEZE
ADVLN
AEFWE
AENEX
AEXQZ
AFTJW
AGHFR
AGHSJ
AGKMS
AHHHB
AIDAL
AITUG
AKAPO
AKRWK
ALMA_UNASSIGNED_HOLDINGS
AMRAJ
ASPBG
AVWKF
AZFZN
BAWUL
CGR
CS3
CUY
CVF
DIK
DU5
E3Z
EBS
ECM
EIF
EJD
F5P
FCP
FDB
FIRID
HH5
HZ~
IH2
IHE
IXB
J1W
JIG
K-O
KOO
KQ8
L7B
LX5
M3Z
M41
N9A
NPM
O-L
O9-
OK1
P2P
RIG
RNS
ROL
RPZ
SCP
SDG
SDP
SES
SSZ
TAE
TN5
TR2
TWZ
UKR
UPT
WH7
YYQ
YZZ
ZCA
ZY4
7X8
AAYWO
ABDGV
ACVFH
ADCNI
ADXHL
AEUPX
AFPUW
AIGII
AKBMS
AKYEP
APXCP
EFKBS
ID FETCH-LOGICAL-c481t-e9e2d2de393c855bd016efd112af3a5993a55df478452f91d399d0a5f3c520842
IEDL.DBID 7X8
ISICitedReferencesCount 493
ISICitedReferencesURI http://www.webofscience.com/api/gateway?GWVersion=2&SrcApp=Summon&SrcAuth=ProQuest&DestLinkType=CitingArticles&DestApp=WOS_CPL&KeyUT=000309544200021&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
ISSN 1097-4172
IngestDate Thu Oct 02 07:03:26 EDT 2025
Thu Apr 03 07:03:36 EDT 2025
IsPeerReviewed true
IsScholarly true
Issue 1
Language English
License Copyright © 2012 Elsevier Inc. All rights reserved.
LinkModel DirectLink
MergedId FETCHMERGED-LOGICAL-c481t-e9e2d2de393c855bd016efd112af3a5993a55df478452f91d399d0a5f3c520842
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
PMID 22981692
PQID 1081874868
PQPubID 23479
ParticipantIDs proquest_miscellaneous_1081874868
pubmed_primary_22981692
PublicationCentury 2000
PublicationDate 2012-09-28
PublicationDateYYYYMMDD 2012-09-28
PublicationDate_xml – month: 09
  year: 2012
  text: 2012-09-28
  day: 28
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Cell
PublicationTitleAlternate Cell
PublicationYear 2012
References 23493303 - Circ Res. 2013 Mar 15;112(6):881-3
23122282 - Cell Stem Cell. 2012 Nov 2;11(5):581-2
References_xml – reference: 23122282 - Cell Stem Cell. 2012 Nov 2;11(5):581-2
– reference: 23493303 - Circ Res. 2013 Mar 15;112(6):881-3
SSID ssj0008555
Score 2.584648
Snippet Heart development is exquisitely sensitive to the precise temporal regulation of thousands of genes that govern developmental decisions during differentiation....
SourceID proquest
pubmed
SourceType Aggregation Database
Index Database
StartPage 206
SubjectTerms Animals
Cell Differentiation
Chromatin - metabolism
Embryonic Stem Cells - metabolism
Enhancer Elements, Genetic
Epigenesis, Genetic
Gene Regulatory Networks
Heart - embryology
Humans
Mice
Myocardium - cytology
Transcription Factors - metabolism
Transcriptome
Title Dynamic and coordinated epigenetic regulation of developmental transitions in the cardiac lineage
URI https://www.ncbi.nlm.nih.gov/pubmed/22981692
https://www.proquest.com/docview/1081874868
Volume 151
WOSCitedRecordID wos000309544200021&url=https%3A%2F%2Fcvtisr.summon.serialssolutions.com%2F%23%21%2Fsearch%3Fho%3Df%26include.ft.matches%3Dt%26l%3Dnull%26q%3D
hasFullText
inHoldings 1
isFullTextHit
isPrint
link http://cvtisr.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1LS8NAEF7UKnjx_X6wgtdAs49k9ySiFg9aelDoLewTeklqWwX_vTPZlF48CF5y2xDm-WV2Zj5Cbm2hQ-gblSmG1arCmkwb5bIgrNPOecfLdlD4pRwO1XisR13Bbd61VS5jYhuofeOwRg7erZA-ThXqbvqRIWsU3q52FBrrpMcByqBjluPVtnAlW9ZTvGTNBGTqbmgm9XdhYRxbu1i7vLOje_sVYrapZrD734_cIzsdyKT3ySr2yVqoD8hWop38PiTmMdHQU1N76hr4_ZzUADk9DVPczYljjXSWOOpBa7SJ1K9ai-C9C8xvqdWLTmoKEJK61tAcRdAKEeqIvA-e3h6es45qIXNC5Yss6MA884Fr7kBq1oOMQvQAxkzkRgKIMVL6KEolJIs694BrfN_IyJ1kfSXYMdmomzqcEsoLafsWDnJrhAy5tQ6Uz4sYohXCszNys5RdBaaMajB1aD7n1Up6Z-QkKaCapp0bFWNa5YVm5384fUG2Ua_Y1cHUJelFcORwRTbd12Iyn123NgLP4ej1B2EOyPY
linkProvider ProQuest
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Dynamic+and+coordinated+epigenetic+regulation+of+developmental+transitions+in+the+cardiac+lineage&rft.jtitle=Cell&rft.au=Wamstad%2C+Joseph+A&rft.au=Alexander%2C+Jeffrey+M&rft.au=Truty%2C+Rebecca+M&rft.au=Shrikumar%2C+Avanti&rft.date=2012-09-28&rft.issn=1097-4172&rft.eissn=1097-4172&rft.volume=151&rft.issue=1&rft.spage=206&rft_id=info:doi/10.1016%2Fj.cell.2012.07.035&rft.externalDBID=NO_FULL_TEXT
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1097-4172&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1097-4172&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1097-4172&client=summon