CoChat
Sign Up
Cited by 145Genomics and Chromatin DynamicsGenetic Associations and EpidemiologyChromatin Remodeling and Cancer

A promoter interaction map for cardiovascular disease genetics

Open access
Montefiori, Lindsey E, Sobreira, Debora R, Sakabe, Noboru J, Aneas, Ivy, Joslin, Amelia C, Hansen, Grace T, Bozek, Grazyna, Moskowitz, Ivan P +2 more·2018·eLife
DOI 10.7554/elife.35788PMC PMC6053306

Published version of a preprint

Open this paper in CoChat — free account

Abstract

Over 500 genetic loci have been associated with risk of cardiovascular diseases (CVDs); however, most loci are located in gene-distal non-coding regions and their target genes are not known. Here, we generated high-resolution promoter capture Hi-C (PCHi-C) maps in human induced pluripotent stem cells (iPSCs) and iPSC-derived cardiomyocytes (CMs) to provide a resource for identifying and prioritizing the functional targets of CVD associations. We validate these maps by demonstrating that promoters preferentially contact distal sequences enriched for tissue-specific transcription factor motifs and are enriched for chromatin marks that correlate with dynamic changes in gene expression. Using the CM PCHi-C map, we linked 1999 CVD-associated SNPs to 347 target genes. Remarkably, more than 90% of SNP-target gene interactions did not involve the nearest gene, while 40% of SNPs interacted with at least two genes, demonstrating the importance of considering long-range chromatin interactions when interpreting functional targets of disease loci.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.7554/elife.35788

Cites

24 of 24 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • 3C-derived methods have detected multitudes of enhancer-promoter loops in many human and mouse cell types.

    “These enrichment methods have detected multitudes of enhancer–promoter loops in many human and mouse cell types [243, 286–291].”

    From Transcriptional enhancers and their communication with gene promoters (2021) · cites this paper as [286]

    The Introduction says promoter-capture Hi-C has identified thousands of enhancer–promoter contacts in different cell types. The Results report hundreds of thousands of promoter interactions in two human cell types, iPSCs and cardiomyocytes. These passages support the claim for human cells, but do not establish its mouse-cell component. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 62

  1. Arking DE Pulit SL Crotti L van der Harst P Munroe PB Koopmann TT Sotoodehnia N Rossin EJ Morley M Wang X Johnson AD Lundby A Gudbjartsson DF Noseworthy PA Eijgelsheim M Bradford Y Tarasov KV Dörr M Müller-Nurasyid M Lahtinen AM Nolte IM Smith AV Bis JC Isaacs A Newhouse SJ Evans DS Post WS Waggott D Lyytikäinen LP Hicks AA Eisele L Ellinghaus D Hayward C Navarro P Ulivi S Tanaka T Tester DJ Chatel S Gustafsson S Kumari M Morris RW Naluai ÅT Padmanabhan S Kluttig A Strohmer B Panayiotou AG Torres M Knoflach M Hubacek JA Slowikowski K Raychaudhuri S Kumar RD Harris TB Launer LJ Shuldiner AR Alonso A Bader JS Ehret G Huang H Kao WH Strait JB Macfarlane PW Brown M Caulfield MJ Samani NJ Kronenberg F Willeit J Smith JG Greiser KH Meyer Zu Schwabedissen H Werdan K Carella M Zelante L Heckbert SR Psaty BM Rotter JI Kolcic I Polašek O Wright AF Griffin M Daly MJ Arnar DO Hólm H Thorsteinsdottir U Denny JC Roden DM Zuvich RL Emilsson V Plump AS Larson MG O'Donnell CJ Yin X Bobbo M D'Adamo AP Iorio A Sinagra G Carracedo A Cummings SR Nalls MA Jula A Kontula KK Marjamaa A Oikarinen L Perola M Porthan K Erbel R Hoffmann P Jöckel KH Kälsch H Nöthen MM den Hoed M Loos RJ Thelle DS Gieger C Meitinger T Perz S Peters A Prucha H Sinner MF Waldenberger M de Boer RA Franke L van der Vleuten PA Beckmann BM Martens E Bardai A Hofman N Wilde AA Behr ER Dalageorgou C Giudicessi JR Medeiros-Domingo A Barc J Kyndt F Probst V Ghidoni A Insolia R Hamilton RM Scherer SW Brandimarto J Margulies K Moravec CE del Greco M F Fuchsberger C O'Connell JR Lee WK Watt GC Campbell H Wild SH El Mokhtari NE Frey N Asselbergs FW Mateo Leach I Navis G van den Berg MP van Veldhuisen DJ Kellis M Krijthe BP Franco OH Hofman A Kors JA Uitterlinden AG Witteman JC Kedenko L Lamina C Oostra BA Abecasis GR Lakatta EG Mulas A Orrú M Schlessinger D Uda M Markus MR Völker U Snieder H Spector TD Ärnlöv J Lind L Sundström J Syvänen AC Kivimaki M Kähönen M Mononen N Raitakari OT Viikari JS Adamkova V Kiechl S Brion M Nicolaides AN Paulweber B Haerting J Dominiczak AF Nyberg F Whincup PH Hingorani AD Schott JJ Bezzina CR Ingelsson E Ferrucci L Gasparini P Wilson JF Rudan I Franke A Mühleisen TW Pramstaller PP Lehtimäki TJ Paterson AD Parsa A Liu Y van Duijn CM Siscovick DS Gudnason V Jamshidi Y Salomaa V Felix SB Sanna S Ritchie MD Stricker BH Stefansson K Boyer LA Cappola TP Olsen JV Lage K Schwartz PJ Kääb S Chakravarti A Ackerman MJ Pfeufer A de Bakker PI Newton-Cheh C CARe Consortium COGENT Consortium DCCT/EDIC eMERGE Consortium HRGEN Consortium 2014 Genetic association study of QT interval highlights role for calcium signaling pathways in myocardial repolarization Nature Genetics 46 826 836 10.1038/ng.3014 24952745 PMC4124521 · DOI
  2. Arnolds DE Liu F Fahrenbach JP Kim GH Schillinger KJ Smemo S McNally EM Nobrega MA Patel VV Moskowitz IP 2012 TBX5 drives Scn5a expression to regulate cardiac conduction system function Journal of Clinical Investigation 122 2509 2518 10.1172/JCI62617 22728936 PMC3386825 · DOI
  3. Ashburner M Ball CA Blake JA Botstein D Butler H Cherry JM Davis AP Dolinski K Dwight SS Eppig JT Harris MA Hill DP Issel-Tarver L Kasarskis A Lewis S Matese JC Richardson JE Ringwald M Rubin GM Sherlock G 2000 Gene ontology: tool for the unification of biology. the gene ontology consortium Nature Genetics 25 25 29 10.1038/75556 10802651 PMC3037419 · DOI · Paper page
  4. Banovich NE Li YI Raj A Ward MC Greenside P Calderon D Tung PY Burnett JE Myrthil M Thomas SM Burrows CK Romero IG Pavlovic BJ Kundaje A Pritchard JK Gilad Y 2018 Impact of regulatory variation across human iPSCs and differentiated cells Genome Research 28 122 131 10.1101/gr.224436.117 29208628 PMC5749177 · DOI
  5. Blake JA Eppig JT Kadin JA Richardson JE Smith CL Bult CJ the Mouse Genome Database Group 2017 Mouse Genome Database (MGD)-2017: community knowledge resource for the laboratory mouse Nucleic Acids Research 45 D723 D729 10.1093/nar/gkw1040 27899570 PMC5210536 · DOI
  6. Cai CL Zhou W Yang L Bu L Qyang Y Zhang X Li X Rosenfeld MG Chen J Evans S 2005 T-box genes coordinate regional rates of proliferation and regional specification during cardiogenesis Development 132 2475 2487 10.1242/dev.01832 15843407 PMC5576439 · DOI
  7. Calo E Wysocka J 2013 Modification of enhancer chromatin: what, how, and why? Molecular Cell 49 825 837 10.1016/j.molcel.2013.01.038 23473601 PMC3857148 · DOI · Paper page
  8. Carithers LJ Ardlie K Barcus M Branton PA Britton A Buia SA Compton CC DeLuca DS Peter-Demchok J Gelfand ET Guan P Korzeniewski GE Lockhart NC Rabiner CA Rao AK Robinson KL Roche NV Sawyer SJ Segrè AV Shive CE Smith AM Sobin LH Undale AH Valentino KM Vaught J Young TR Moore HM GTEx Consortium 2015 A novel approach to high-quality postmortem tissue procurement: The GTEx project Biopreservation and Biobanking 13 311 319 10.1089/bio.2015.0032 26484571 PMC4675181 · DOI · Paper page
  9. Claussnitzer M Dankel SN Kim KH Quon G Meuleman W Haugen C Glunk V Sousa IS Beaudry JL Puviindran V Abdennur NA Liu J Svensson PA Hsu YH Drucker DJ Mellgren G Hui CC Hauner H Kellis M 2015 FTO obesity variant circuitry and Adipocyte Browning in humans New England Journal of Medicine 373 895 907 10.1056/NEJMoa1502214 26287746 PMC4959911 · DOI · Paper page
  10. Cowper-Sal lari R Zhang X Wright JB Bailey SD Cole MD Eeckhoute J Moore JH Lupien M 2012 Breast cancer risk-associated SNPs modulate the affinity of chromatin for FOXA1 and alter gene expression Nature Genetics 44 1191 1198 10.1038/ng.2416 23001124 PMC3483423 · DOI
  11. Creyghton MP Cheng AW Welstead GG Kooistra T Carey BW Steine EJ Hanna J Lodato MA Frampton GM Sharp PA Boyer LA Young RA Jaenisch R 2010 Histone H3K27ac separates active from poised enhancers and predicts developmental state PNAS 107 21931 21936 10.1073/pnas.1016071107 21106759 PMC3003124 · DOI · Paper page
  12. Dao LTM Galindo-Albarrán AO Castro-Mondragon JA Andrieu-Soler C Medina-Rivera A Souaid C Charbonnier G Griffon A Vanhille L Stephen T Alomairi J Martin D Torres M Fernandez N Soler E van Helden J Puthier D Spicuglia S 2017 Genome-wide characterization of mammalian promoters with distal enhancer functions Nature Genetics 49 1073 1081 10.1038/ng.3884 28581502 · DOI · Paper page
  13. Dekker J Mirny L 2016 The 3D genome as moderator of chromosomal communication Cell 164 1110 1121 10.1016/j.cell.2016.02.007 26967279 PMC4788811 · DOI · Paper page
  14. Diao Y Fang R Li B Meng Z Yu J Qiu Y Lin KC Huang H Liu T Marina RJ Jung I Shen Y Guan KL Ren B 2017 A tiling-deletion-based genetic screen for cis-regulatory element identification in mammalian cells Nature Methods 14 629 635 10.1038/nmeth.4264 28417999 PMC5490986 · DOI · Paper page
  15. ENCODE Project Consortium 2012 An integrated encyclopedia of DNA elements in the human genome Nature 489 57 74 10.1038/nature11247 22955616 PMC3439153 · DOI · Paper page
  16. Erceg J Pakozdi T Marco-Ferreres R Ghavi-Helm Y Girardot C Bracken AP Furlong EE 2017 Dual functionality of cis-regulatory elements as developmental enhancers and Polycomb response elements Genes & Development 31 590 602 10.1101/gad.292870.116 28381411 PMC5393054 · DOI
  17. Gherghiceanu M Barad L Novak A Reiter I Itskovitz-Eldor J Binah O Popescu LM 2011 Cardiomyocytes derived from human embryonic and induced pluripotent stem cells: comparative ultrastructure Journal of Cellular and Molecular Medicine 15 2539 2551 10.1111/j.1582-4934.2011.01417.x 21883888 PMC3822963 · DOI
  18. Gilbert N Boyle S Fiegler H Woodfine K Carter NP Bickmore WA 2004 Chromatin architecture of the human genome: gene-rich domains are enriched in open chromatin fibers Cell 118 555 566 10.1016/j.cell.2004.08.011 15339661 · DOI
  19. Guo DC Papke CL Tran-Fadulu V Regalado ES Avidan N Johnson RJ Kim DH Pannu H Willing MC Sparks E Pyeritz RE Singh MN Dalman RL Grotta JC Marian AJ Boerwinkle EA Frazier LQ LeMaire SA Coselli JS Estrera AL Safi HJ Veeraraghavan S Muzny DM Wheeler DA Willerson JT Yu RK Shete SS Scherer SE Raman CS Buja LM Milewicz DM 2009 Mutations in smooth muscle alpha-actin (ACTA2) cause coronary artery disease, stroke, and Moyamoya disease, along with thoracic aortic disease The American Journal of Human Genetics 84 617 627 10.1016/j.ajhg.2009.04.007 19409525 PMC2680995 · DOI
  20. Heinz S Benner C Spann N Bertolino E Lin YC Laslo P Cheng JX Murre C Singh H Glass CK 2010 Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities Molecular Cell 38 576 589 10.1016/j.molcel.2010.05.004 20513432 PMC2898526 · DOI · Paper page
  21. Hnisz D Shrinivas K Young RA Chakraborty AK Sharp PA 2017 A phase separation model for transcriptional control Cell 169 13 23 10.1016/j.cell.2017.02.007 28340338 PMC5432200 · DOI · Paper page
  22. Jin F Li Y Dixon JR Selvaraj S Ye Z Lee AY Yen CA Schmitt AD Espinoza CA Ren B 2013 A high-resolution map of the three-dimensional chromatin interactome in human cells Nature 503 290 294 10.1038/nature12644 24141950 PMC3838900 · DOI · Paper page
  23. Karakikes I Ameen M Termglinchan V Wu JC 2015 Human induced pluripotent stem cell-derived cardiomyocytes: insights into molecular, cellular, and functional phenotypes Circulation Research 117 80 88 10.1161/CIRCRESAHA.117.305365 26089365 PMC4546707 · DOI · Paper page
  24. Karlić R Chung HR Lasserre J Vlahovicek K Vingron M 2010 Histone modification levels are predictive for gene expression PNAS 107 2926 2931 10.1073/pnas.0909344107 20133639 PMC2814872 · DOI
  25. Langmead B Salzberg SL 2012 Fast gapped-read alignment with Bowtie 2 Nature Methods 9 357 359 10.1038/nmeth.1923 22388286 PMC3322381 · DOI · Paper page
  26. Li H 2011 Tabix: fast retrieval of sequence features from generic TAB-delimited files Bioinformatics 27 718 719 10.1093/bioinformatics/btq671 21208982 PMC3042176 · DOI
  27. Lieberman-Aiden E van Berkum NL Williams L Imakaev M Ragoczy T Telling A Amit I Lajoie BR Sabo PJ Dorschner MO Sandstrom R Bernstein B Bender MA Groudine M Gnirke A Stamatoyannopoulos J Mirny LA Lander ES Dekker J 2009 Comprehensive mapping of long-range interactions reveals folding principles of the human genome Science 326 289 293 10.1126/science.1181369 19815776 PMC2858594 · DOI · Paper page
  28. Love MI Huber W Anders S 2014 Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2 Genome Biology 15 550 10.1186/s13059-014-0550-8 25516281 PMC4302049 · DOI · Paper page
  29. Mahmoud AI Kocabas F Muralidhar SA Kimura W Koura AS Thet S Porrello ER Sadek HA 2013 Meis1 regulates postnatal cardiomyocyte cell cycle arrest Nature 497 249 253 10.1038/nature12054 23594737 PMC4159712 · DOI
  30. Meder B Rühle F Weis T Homuth G Keller A Franke J Peil B Lorenzo Bermejo J Frese K Huge A Witten A Vogel B Haas J Völker U Ernst F Teumer A Ehlermann P Zugck C Friedrichs F Kroemer H Dörr M Hoffmann W Maisch B Pankuweit S Ruppert V Scheffold T Kühl U Schultheiss HP Kreutz R Ertl G Angermann C Charron P Villard E Gary F Isnard R Komajda M Lutz M Meitinger T Sinner MF Wichmann HE Krawczak M Ivandic B Weichenhan D Gelbrich G El-Mokhtari NE Schreiber S Felix SB Hasenfuß G Pfeufer A Hübner N Kääb S Arbustini E Rottbauer W Frey N Stoll M Katus HA 2014 A genome-wide association study identifies 6p21 as novel risk locus for dilated cardiomyopathy European Heart Journal 35 1069 1077 10.1093/eurheartj/eht251 23853074 · DOI
  31. Miele A Dekker J 2008 Long-range chromosomal interactions and gene regulation Molecular BioSystems 4 1046 10.1039/b803580f 18931780 PMC2653627 · DOI
  32. Mifsud B Tavares-Cadete F Young AN Sugar R Schoenfelder S Ferreira L Wingett SW Andrews S Grey W Ewels PA Herman B Happe S Higgs A LeProust E Follows GA Fraser P Luscombe NM Osborne CS 2015 Mapping long-range promoter contacts in human cells with high-resolution capture Hi-C Nature Genetics 47 598 606 10.1038/ng.3286 25938943 · DOI · Paper page
  33. Moshal K Roder K Werdich AA Dural NT Kim TY Cooper LL Yc L Choi B-R Terentyev D MacRae C Koren G 2017 LITAF, A novel regulator of cardiac excitation FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 31 686.3
  34. Musunuru K Strong A Frank-Kamenetsky M Lee NE Ahfeldt T Sachs KV Li X Li H Kuperwasser N Ruda VM Pirruccello JP Muchmore B Prokunina-Olsson L Hall JL Schadt EE Morales CR Lund-Katz S Phillips MC Wong J Cantley W Racie T Ejebe KG Orho-Melander M Melander O Koteliansky V Fitzgerald K Krauss RM Cowan CA Kathiresan S Rader DJ 2010 From noncoding variant to phenotype via SORT1 at the 1p13 cholesterol locus Nature 466 714 719 10.1038/nature09266 20686566 PMC3062476 · DOI · Paper page
  35. Patro R Duggal G Love MI Irizarry RA Kingsford C 2017 Salmon provides fast and bias-aware quantification of transcript expression Nature Methods 14 417 419 10.1038/nmeth.4197 28263959 PMC5600148 · DOI · Paper page
  36. Pennacchio LA Bickmore W Dean A Nobrega MA Bejerano G 2013 Enhancers: five essential questions Nature Reviews Genetics 14 288 295 10.1038/nrg3458 23503198 PMC4445073 · DOI
  37. Petersen CM Nielsen MS Nykjaer A Jacobsen L Tommerup N Rasmussen HH Roigaard H Gliemann J Madsen P Moestrup SK 1997 Molecular identification of a novel candidate sorting receptor purified from human brain by receptor-associated protein affinity chromatography Journal of Biological Chemistry 272 3599 3605 10.1074/jbc.272.6.3599 9013611 · DOI
  38. Phanstiel DH Van Bortle K Spacek D Hess GT Shamim MS Machol I Love MI Aiden EL Bassik MC Snyder MP 2017 Static and dynamic DNA loops form AP-1-Bound activation hubs during macrophage development Molecular Cell 67 1037 1048 10.1016/j.molcel.2017.08.006 28890333 PMC5610110 · DOI · Paper page
  39. Phillips JE Corces VG 2009 CTCF: master weaver of the genome Cell 137 1194 1211 10.1016/j.cell.2009.06.001 19563753 PMC3040116 · DOI
  40. Phillips-Cremins JE Sauria ME Sanyal A Gerasimova TI Lajoie BR Bell JS Ong CT Hookway TA Guo C Sun Y Bland MJ Wagstaff W Dalton S McDevitt TC Sen R Dekker J Taylor J Corces VG 2013 Architectural protein subclasses shape 3D organization of genomes during lineage commitment Cell 153 1281 1295 10.1016/j.cell.2013.04.053 23706625 PMC3712340 · DOI · Paper page
  41. Pikkarainen S Tokola H Kerkelä R Ruskoaho H 2004 GATA transcription factors in the developing and adult heart Cardiovascular Research 63 196 207 10.1016/j.cardiores.2004.03.025 15249177 · DOI
  42. Purcell S Neale B Todd-Brown K Thomas L Ferreira MA Bender D Maller J Sklar P de Bakker PI Daly MJ Sham PC 2007 PLINK: a tool set for whole-genome association and population-based linkage analyses The American Journal of Human Genetics 81 559 575 10.1086/519795 17701901 PMC1950838 · DOI · Paper page
  43. Quinlan AR Hall IM 2010 BEDTools: a flexible suite of utilities for comparing genomic features Bioinformatics 26 841 842 10.1093/bioinformatics/btq033 20110278 PMC2832824 · DOI · Paper page
  44. Rao SS Huntley MH Durand NC Stamenova EK Bochkov ID Robinson JT Sanborn AL Machol I Omer AD Lander ES Aiden EL 2014 A 3D map of the human genome at kilobase resolution reveals principles of chromatin looping Cell 159 1665 1680 10.1016/j.cell.2014.11.021 25497547 PMC5635824 · DOI · Paper page
  45. Sakabe NJ Aneas I Shen T Shokri L Park SY Bulyk ML Evans SM Nobrega MA 2012 Dual transcriptional activator and repressor roles of TBX20 regulate adult cardiac structure and function Human Molecular Genetics 21 2194 2204 10.1093/hmg/dds034 22328084 PMC3335310 · DOI
  46. Schoenfelder S Furlan-Magaril M Mifsud B Tavares-Cadete F Sugar R Javierre BM Nagano T Katsman Y Sakthidevi M Wingett SW Dimitrova E Dimond A Edelman LB Elderkin S Tabbada K Darbo E Andrews S Herman B Higgs A LeProust E Osborne CS Mitchell JA Luscombe NM Fraser P 2015 The pluripotent regulatory circuitry connecting promoters to their long-range interacting elements Genome Research 25 582 597 10.1101/gr.185272.114 25752748 PMC4381529 · DOI · Paper page
  47. Shen T Aneas I Sakabe N Dirschinger RJ Wang G Smemo S Westlund JM Cheng H Dalton N Gu Y Boogerd CJ Cai CL Peterson K Chen J Nobrega MA Evans SM 2011 Tbx20 regulates a genetic program essential to adult mouse cardiomyocyte function Journal of Clinical Investigation 121 4640 4654 10.1172/JCI59472 22080862 PMC3223071 · DOI
  48. Shin H Shi Y Dai C Tjong H Gong K Alber F Zhou XJ 2016 TopDom: an efficient and deterministic method for identifying topological domains in genomes Nucleic Acids Research 44 e70 10.1093/nar/gkv1505 26704975 PMC4838359 · DOI
  49. Smemo S Campos LC Moskowitz IP Krieger JE Pereira AC Nobrega MA 2012 Regulatory variation in a TBX5 enhancer leads to isolated congenital heart disease Human Molecular Genetics 21 3255 3263 10.1093/hmg/dds165 22543974 PMC3384386 · DOI
  50. Smemo S Tena JJ Kim KH Gamazon ER Sakabe NJ Gómez-Marín C Aneas I Credidio FL Sobreira DR Wasserman NF Lee JH Puviindran V Tam D Shen M Son JE Vakili NA Sung HK Naranjo S Acemel RD Manzanares M Nagy A Cox NJ Hui CC Gomez-Skarmeta JL Nóbrega MA 2014 Obesity-associated variants within FTO form long-range functional connections with IRX3 Nature 507 371 375 10.1038/nature13138 24646999 PMC4113484 · DOI · Paper page
  51. Smith NL Felix JF Morrison AC Demissie S Glazer NL Loehr LR Cupples LA Dehghan A Lumley T Rosamond WD Lieb W Rivadeneira F Bis JC Folsom AR Benjamin E Aulchenko YS Haritunians T Couper D Murabito J Wang YA Stricker BH Gottdiener JS Chang PP Wang TJ Rice KM Hofman A Heckbert SR Fox ER O'Donnell CJ Uitterlinden AG Rotter JI Willerson JT Levy D van Duijn CM Psaty BM Witteman JC Boerwinkle E Vasan RS 2010 Association of genome-wide variation with the risk of incident heart failure in adults of European and African ancestry: a prospective meta-analysis from the cohorts for heart and aging research in genomic epidemiology (CHARGE) consortium Circulation: Cardiovascular Genetics 3 256 266 10.1161/CIRCGENETICS.109.895763 20445134 PMC3025695 · DOI
  52. Soneson C Love MI Robinson MD 2015 Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences F1000Research 4 1521 10.12688/f1000research.7563.1 26925227 PMC4712774 · DOI · Paper page
  53. Speir ML Zweig AS Rosenbloom KR Raney BJ Paten B Nejad P Lee BT Learned K Karolchik D Hinrichs AS Heitner S Harte RA Haeussler M Guruvadoo L Fujita PA Eisenhart C Diekhans M Clawson H Casper J Barber GP Haussler D Kuhn RM Kent WJ 2016 The UCSC genome browser database: 2016 update Nucleic Acids Research 44 D717 D725 10.1093/nar/gkv1275 26590259 PMC4702902 · DOI
  54. Spitz F Furlong EE 2012 Transcription factors: from enhancer binding to developmental control Nature Reviews Genetics 13 613 626 10.1038/nrg3207 22868264 · DOI · Paper page
  55. Storey JD Tibshirani R 2003 Statistical significance for genomewide studies PNAS 100 9440 9445 10.1073/pnas.1530509100 12883005 PMC170937 · DOI · Paper page
  56. Symmons O Pan L Remeseiro S Aktas T Klein F Huber W Spitz F 2016 The shh topological domain facilitates the action of remote enhancers by reducing the effects of genomic distances Developmental Cell 39 529 543 10.1016/j.devcel.2016.10.015 27867070 PMC5142843 · DOI · Paper page
  57. Tsujimura T Klein FA Langenfeld K Glaser J Huber W Spitz F 2015 A discrete transition zone organizes the topological and regulatory autonomy of the adjacent tfap2c and bmp7 genes PLoS Genetics 11 e1004897 10.1371/journal.pgen.1004897 25569170 PMC4288730 · DOI
  58. Visel A Minovitsky S Dubchak I Pennacchio LA 2007 VISTA Enhancer Browser--a database of tissue-specific human enhancers Nucleic Acids Research 35 D88 D92 10.1093/nar/gkl822 17130149 PMC1716724 · DOI · Paper page
  59. Watt AJ Battle MA Li J Duncan SA 2004 GATA4 is essential for formation of the proepicardium and regulates cardiogenesis PNAS 101 12573 12578 10.1073/pnas.0400752101 15310850 PMC515098 · DOI
  60. Wingett S Ewels P Furlan-Magaril M Nagano T Schoenfelder S Fraser P Andrews S 2015 HiCUP: pipeline for mapping and processing Hi-C data F1000Research 4 1310 10.12688/f1000research.7334.1 26835000 PMC4706059 · DOI
  61. Wright JB Brown SJ Cole MD 2010 Upregulation of c-MYC in cis through a large chromatin loop linked to a cancer risk-associated single-nucleotide polymorphism in colorectal cancer cells Molecular and Cellular Biology 30 1411 1420 10.1128/MCB.01384-09 20065031 PMC2832500 · DOI
  62. Zhou X Li D Zhang B Lowdon RF Rockweiler NB Sears RL Madden PA Smirnov I Costello JF Wang T 2015 Epigenomic annotation of genetic variants using the roadmap epigenome browser Nature Biotechnology 33 345 346 10.1038/nbt.3158 25690851 PMC4467764 · DOI

Cited by

Sorted by citations

Authors
Montefiori, L. E., Sobreira, D. R., Sakabe, N. J., Aneas, I., Joslin, A. C., Hansen, G. T., Bozek, G., Moskowitz, I. P., McNally, E. M., & Nóbrega, M. A.
Affiliations
  • University of Chicago (US)
  • Department of Human Genetics, The University of Chicago, Chicago, United States
  • Northwestern University (US)
Corresponding author
Nóbrega, Marcelo A
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2018-07-10
Volume
7
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.35788
PMC
PMC6053306
OpenAlex
W2805705799
Cited by
145
References
24
Citations by year
2026: 10 · 2025: 12 · 2024: 9 · 2023: 12 · 2022: 17 · 2021: 39 · 2020: 27 · 2019: 18 · 2018: 1
FWCI
8.00
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Knowledge@UChicago (University of Chicago) (submittedVersion, cc-by-nc-nd)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • University of Chicago (cc-by)
Funders
  • National Institutes of Health (HL123857, HL119967, HL118758, HL128075, T32GMOO7197, HL137307-01)
  • American Heart Association (17PRE33410726)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords
cardiovascular genetics, promoter capture Hi-C, long-range chromatin interactions, non-coding variants, iPSC-derived cardiomyocytes, target gene identification, transcription factor binding motifs, chromatin marks, gene expression regulation, disease risk loci
MeSH terms
Cardiovascular Diseases, Gene Expression Regulation, Humans, Promoter Regions, Genetic, Genome, Human, Polymorphism, Single Nucleotide, Genomics, Myocytes, Cardiac, Regulatory Elements, Transcriptional, Gene Regulatory Networks, Genome-Wide Association Study, Genetic Loci, Induced Pluripotent Stem Cells

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review