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To rank TFs, WhichTF applies an ontology-guided functional approach to compute novel enrichment by integrating accessibility measurements, high-confidence pre-computed conservation-aware TF binding sites, and putative gene-regulatory models. Comparison with prior sheer abundance-based methods reveals the unique ability of WhichTF to identify context-specific TFs with functional relevance, including NF-\u03baB family members in lymphocytes and GATA factors in cardiac cells. To distinguish the transcriptional regulatory landscape in closely related samples, we apply differential analysis and demonstrate its utility in lymphocyte, mesoderm developmental, and disease cells. We find suggestive, under-characterized TFs, such as RUNX3 in mesoderm development and GLI1 in systemic lupus erythematosus. We also find TFs known for stress response, suggesting routine experimental caveats that warrant careful consideration. WhichTF yields biological insight into known and novel molecular mechanisms of TF-mediated transcriptional regulation in diverse contexts, including human and mouse cell types, cell fate trajectories, and disease-associated cells.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1010378","type":"journal-article","created":{"date-parts":[[2022,8,30]],"date-time":"2022-08-30T18:33:45Z","timestamp":1661884425000},"page":"e1010378","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":154,"title":["WhichTF is functionally important in your open chromatin data?"],"prefix":"10.1371","volume":"18","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9759-157X","authenticated-orcid":true,"given":"Yosuke","family":"Tanigawa","sequence":"first","affiliation":[]},{"given":"Ethan 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Neurosci"},{"key":"pcbi.1010378.ref033","first-page":"2579","article-title":"Visualizing data using t-SNE","volume":"9","author":"L Van der Maaten","year":"2008","journal-title":"J Mach Learn Res"},{"key":"pcbi.1010378.ref034","doi-asserted-by":"crossref","first-page":"7374","DOI":"10.4049\/jimmunol.1001413","article-title":"Regulation of follicular B cell differentiation by the related E26 transformation-specific transcription factors PU.1, Spi-B, and Spi-C","volume":"185","author":"RP DeKoter","year":"2010","journal-title":"J Immunol"},{"key":"pcbi.1010378.ref035","doi-asserted-by":"crossref","first-page":"2801","DOI":"10.1182\/blood-2011-02-335539","article-title":"Deletion of genes encoding PU.1 and Spi-B in B cells impairs differentiation and induces pre-B cell acute lymphoblastic leukemia","volume":"118","author":"KM Sokalski","year":"2011","journal-title":"Blood"},{"key":"pcbi.1010378.ref036","doi-asserted-by":"crossref","first-page":"1426","DOI":"10.1038\/s41467-017-01605-1","article-title":"Environmental sensing by mature B cells is controlled by the transcription factors PU.1 and SpiB","volume":"8","author":"SN Willis","year":"2017","journal-title":"Nat Commun"},{"key":"pcbi.1010378.ref037","doi-asserted-by":"crossref","first-page":"7731","DOI":"10.1073\/pnas.1232420100","article-title":"Runx3 and Runx1 are required for CD8 T cell development during thymopoiesis","volume":"100","author":"E Woolf","year":"2003","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pcbi.1010378.ref038","doi-asserted-by":"crossref","first-page":"1494","DOI":"10.1038\/s41588-019-0505-9","article-title":"Landscape of stimulation-responsive chromatin across diverse human immune cells","volume":"51","author":"D Calderon","year":"2019","journal-title":"Nat 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Papaioannou","year":"2014","journal-title":"Development"},{"key":"pcbi.1010378.ref042","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1016\/j.stemcr.2013.08.002","article-title":"TBX3 Directs Cell-Fate Decision toward Mesendoderm","volume":"1","author":"CE Weidgang","year":"2013","journal-title":"Stem Cell Reports"},{"key":"pcbi.1010378.ref043","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.04379","article-title":"Hox genes control vertebrate body elongation by collinear Wnt repression","volume":"4","author":"N Denans","year":"2015","journal-title":"Elife"},{"key":"pcbi.1010378.ref044","doi-asserted-by":"crossref","first-page":"3728","DOI":"10.1091\/mbc.E15-02-0112","article-title":"Meis3 is required for neural crest invasion of the gut during zebrafish enteric nervous system development","volume":"26","author":"RA Uribe","year":"2015","journal-title":"Mol Biol 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Heritability","volume":"14","author":"JS Lawrence","year":"1987","journal-title":"J Rheumatol"},{"key":"pcbi.1010378.ref054","doi-asserted-by":"crossref","first-page":"1518","DOI":"10.1001\/jamainternmed.2015.3528","article-title":"Familial Aggregation of Systemic Lupus Erythematosus and Coaggregation of Autoimmune Diseases in Affected Families","volume":"175","author":"C-F Kuo","year":"2015","journal-title":"JAMA Intern Med"},{"key":"pcbi.1010378.ref055","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1038\/s41467-021-21049-y","article-title":"Identification of 38 novel loci for systemic lupus erythematosus and genetic heterogeneity between ancestral groups","volume":"12","author":"Y-F Wang","year":"2021","journal-title":"Nat Commun"},{"key":"pcbi.1010378.ref056","doi-asserted-by":"crossref","first-page":"632","DOI":"10.1136\/annrheumdis-2020-219209","article-title":"Meta-analysis of 208370 East Asians identifies 113 susceptibility loci for systemic lupus erythematosus","volume":"80","author":"X Yin","year":"2021","journal-title":"Ann Rheum Dis"},{"key":"pcbi.1010378.ref057","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1038\/s41588-018-0102-3","article-title":"Transcription factors operate across disease loci, with EBNA2 implicated in autoimmunity","volume":"50","author":"JB Harley","year":"2018","journal-title":"Nat Genet"},{"key":"pcbi.1010378.ref058","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1615\/CritRevImmunol.2017020284","article-title":"The Role of the Transcription Factor Ets1 in Lupus and Other Autoimmune Diseases","volume":"36","author":"LA Garrett-Sinha","year":"2016","journal-title":"Crit Rev Immunol"},{"key":"pcbi.1010378.ref059","doi-asserted-by":"crossref","first-page":"1392","DOI":"10.1172\/JCI91250","article-title":"B cells expressing the transcription factor T-bet drive lupus-like autoimmunity","volume":"127","author":"K Rubtsova","year":"2017","journal-title":"J Clin Invest"},{"key":"pcbi.1010378.ref060","first-page":"780436","article-title":"Interferon regulatory factor 5 in the pathogenesis of systemic lupus erythematosus","volume":"2012","author":"CM Cham","year":"2012","journal-title":"Clin Dev Immunol"},{"key":"pcbi.1010378.ref061","doi-asserted-by":"crossref","first-page":"1855","DOI":"10.1038\/s41467-022-29514-y","article-title":"Lupus enhancer risk variant causes dysregulation of IRF8 through cooperative lncRNA and DNA methylation machinery","volume":"13","author":"T Zhou","year":"2022","journal-title":"Nat Commun"},{"key":"pcbi.1010378.ref062","doi-asserted-by":"crossref","first-page":"27030","DOI":"10.1038\/srep27030","article-title":"ATAC-seq on biobanked specimens defines a unique chromatin accessibility structure in na\u00efve SLE B cells","volume":"6","author":"CD Scharer","year":"2016","journal-title":"Sci Rep"},{"key":"pcbi.1010378.ref063","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1016\/j.bbagrm.2016.08.011","article-title":"NF-Y and SP transcription factors\u2014New insights in a long-standing liaison","volume":"1860","author":"G. Suske","year":"2017","journal-title":"Biochim Biophys Acta Gene Regul Mech"},{"key":"pcbi.1010378.ref064","doi-asserted-by":"crossref","first-page":"172","DOI":"10.1111\/j.1600-065X.2012.01112.x","article-title":"Roles of BCL6 in normal and transformed germinal center B cells","volume":"247","author":"K Basso","year":"2012","journal-title":"Immunol Rev"},{"key":"pcbi.1010378.ref065","doi-asserted-by":"crossref","first-page":"5361","DOI":"10.4049\/jimmunol.173.9.5361","article-title":"Regulation of B cell differentiation and plasma cell generation by IL-21, a novel inducer of Blimp-1 and Bcl-6","volume":"173","author":"K Ozaki","year":"2004","journal-title":"J Immunol"},{"key":"pcbi.1010378.ref066","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1038\/s41392-021-00725-x","article-title":"AIM2 deficiency in B cells ameliorates systemic lupus erythematosus by regulating Blimp-1-Bcl-6 axis-mediated B-cell differentiation","volume":"6","author":"M Yang","year":"2021","journal-title":"Signal Transduct Target Ther"},{"key":"pcbi.1010378.ref067","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1007\/s10753-015-0273-3","article-title":"The Effect of SHH-Gli Signaling Pathway on the Synovial Fibroblast Proliferation in Rheumatoid Arthritis","volume":"39","author":"S Qin","year":"2016","journal-title":"Inflammation"},{"key":"pcbi.1010378.ref068","doi-asserted-by":"crossref","first-page":"1624","DOI":"10.2337\/dci19-0001","article-title":"The TCF7L2 Locus: A Genetic Window Into the Pathogenesis of Type 1 and Type 2 Diabetes","volume":"42","author":"SFA Grant","year":"2019","journal-title":"Diabetes Care"},{"key":"pcbi.1010378.ref069","doi-asserted-by":"crossref","first-page":"e12716","DOI":"10.1371\/journal.pone.0012716","article-title":"Fine-mapping resolves Eae23 into two QTLs and implicates ZEB1 as a candidate gene regulating experimental neuroinflammation in rat","volume":"5","author":"P Stridh","year":"2010","journal-title":"PLoS One"},{"key":"pcbi.1010378.ref070","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1038\/nmeth.4437","article-title":"Single-cell sequencing reveals dissociation-induced gene expression in tissue subpopulations","volume":"14","author":"SC van den Brink","year":"2017","journal-title":"Nat Methods"},{"key":"pcbi.1010378.ref071","doi-asserted-by":"crossref","first-page":"2130","DOI":"10.1093\/ndt\/16.11.2130","article-title":"GATA3 and kidney development: why case reports are still important","volume":"16","author":"H Van Esch","year":"2001","journal-title":"Nephrol Dial Transplant"},{"key":"pcbi.1010378.ref072","doi-asserted-by":"crossref","first-page":"61","DOI":"10.4161\/org.6.2.11928","article-title":"WT1 and kidney progenitor cells","volume":"6","author":"JA 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Cell"},{"key":"pcbi.1010378.ref082","doi-asserted-by":"crossref","first-page":"D754","DOI":"10.1093\/nar\/gkx1098","article-title":"Ensembl 2018","volume":"46","author":"DR Zerbino","year":"2018","journal-title":"Nucleic Acids Res"},{"key":"pcbi.1010378.ref083","doi-asserted-by":"crossref","first-page":"330","DOI":"10.1038\/nmeth.4632","article-title":"A toolbox of immunoprecipitation-grade monoclonal antibodies to human transcription factors","volume":"15","author":"A Venkataraman","year":"2018","journal-title":"Nat Methods"},{"key":"pcbi.1010378.ref084","first-page":"163","article-title":"GATA factor switching during erythroid differentiation","volume":"17","author":"H Kaneko","year":"2010","journal-title":"Curr Opin Hematol"},{"key":"pcbi.1010378.ref085","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1038\/nature10730","article-title":"Differential oestrogen receptor binding is associated with clinical outcome in breast cancer","volume":"481","author":"CS Ross-Innes","year":"2012","journal-title":"Nature"},{"key":"pcbi.1010378.ref086","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1038\/s41586-021-03446-x","article-title":"Genome-wide enhancer maps link risk variants to disease genes","volume":"593","author":"J Nasser","year":"2021","journal-title":"Nature"},{"key":"pcbi.1010378.ref087","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1038\/s41586-021-04103-z","article-title":"Exome sequencing and analysis of 454,787 UK Biobank participants","volume":"599","author":"JD Backman","year":"2021","journal-title":"Nature"},{"key":"pcbi.1010378.ref088","doi-asserted-by":"crossref","first-page":"300","DOI":"10.1038\/s41586-020-03145-z","article-title":"Regulatory genomic circuitry of human disease loci by integrative epigenomics","volume":"590","author":"CA Boix","year":"2021","journal-title":"Nature"},{"key":"pcbi.1010378.ref089","doi-asserted-by":"crossref","first-page":"e27041","DOI":"10.7554\/eLife.27041","article-title":"Science Forum: The Human Cell Atlas","volume":"6","author":"A Regev","year":"2017","journal-title":"eLife Sciences"},{"key":"pcbi.1010378.ref090","unstructured":"Tanigawa Y, Dyer E, Bejerano G. Reference data for WhichTF software. 2022."},{"key":"pcbi.1010378.ref091","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1038\/75556","article-title":"Gene ontology: tool for the unification of biology. The Gene Ontology Consortium","volume":"25","author":"M Ashburner","year":"2000","journal-title":"Nat Genet"},{"key":"pcbi.1010378.ref092","doi-asserted-by":"crossref","first-page":"D331","DOI":"10.1093\/nar\/gkw1108","article-title":"Expansion of the Gene Ontology knowledgebase and resources","volume":"45","author":"The Gene Ontology Consortium","year":"2017","journal-title":"Nucleic Acids Res"},{"key":"pcbi.1010378.ref093","doi-asserted-by":"crossref","first-page":"D1018","DOI":"10.1093\/nar\/gky1105","article-title":"Expansion of the Human Phenotype Ontology (HPO) knowledge base and resources","volume":"47","author":"S K\u00f6hler","year":"2019","journal-title":"Nucleic Acids Res"},{"key":"pcbi.1010378.ref094","doi-asserted-by":"crossref","first-page":"9299","DOI":"10.1093\/nar\/gky741","article-title":"Independent erosion of conserved transcription factor binding sites points to shared hindlimb, vision and external testes loss in different mammals","volume":"46","author":"MJ Berger","year":"2018","journal-title":"Nucleic Acids Res"},{"key":"pcbi.1010378.ref095","doi-asserted-by":"crossref","first-page":"e1004711","DOI":"10.1371\/journal.pcbi.1004711","article-title":"Erosion of Conserved Binding Sites in Personal Genomes Points to Medical Histories","volume":"12","author":"H Guturu","year":"2016","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1010378.ref096","doi-asserted-by":"crossref","first-page":"996","DOI":"10.1101\/gr.229102","article-title":"The human genome browser at UCSC","volume":"12","author":"WJ Kent","year":"2002","journal-title":"Genome Res"},{"key":"pcbi.1010378.ref097","first-page":"42","volume":"36","author":"O Tange","year":"2011","journal-title":"GNU Parallel\u2014The Command-Line Power Tool. ;login: The USENIX Magazine"},{"key":"pcbi.1010378.ref098","unstructured":"Thomas H. Cormen, Charles E. Leiserson, Ronald L. Rivest and Clifford Stein. Introduction to Algorithms, Third Edition. The MIT Press; 2009."},{"key":"pcbi.1010378.ref099","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1038\/nature11247","article-title":"An integrated encyclopedia of DNA elements in the human genome","volume":"489","author":"ENCODE Project Consortium","year":"2012","journal-title":"Nature"},{"key":"pcbi.1010378.ref100","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1038\/nature14248","article-title":"Integrative analysis of 111 reference human epigenomes","volume":"518","author":"Roadmap Epigenomics Consortium","year":"2015","journal-title":"Nature"},{"key":"pcbi.1010378.ref101","unstructured":"Wolfram Research, Inc. Champaign, IL. Wolfram Mathematica. 2020. https:\/\/www.wolfram.com\/mathematica"},{"key":"pcbi.1010378.ref102","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1093\/bioinformatics\/btq033","article-title":"BEDTools: a flexible suite of utilities for comparing genomic features","volume":"26","author":"AR Quinlan","year":"2010","journal-title":"Bioinformatics"},{"key":"pcbi.1010378.ref103","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1038\/nmeth.1923","article-title":"Fast gapped-read alignment with Bowtie 2","volume":"9","author":"B Langmead","year":"2012","journal-title":"Nat Methods"},{"key":"pcbi.1010378.ref104","doi-asserted-by":"crossref","first-page":"2078","DOI":"10.1093\/bioinformatics\/btp352","article-title":"The Sequence Alignment\/Map format and SAMtools","volume":"25","author":"H Li","year":"2009","journal-title":"Bioinformatics"},{"key":"pcbi.1010378.ref105","doi-asserted-by":"crossref","first-page":"R137","DOI":"10.1186\/gb-2008-9-9-r137","article-title":"Model-based analysis of ChIP-Seq (MACS)","volume":"9","author":"Y Zhang","year":"2008","journal-title":"Genome Biol"},{"key":"pcbi.1010378.ref106","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1038\/nature24267","article-title":"The impact of rare variation on gene expression across tissues","volume":"550","author":"X Li","year":"2017","journal-title":"Nature"}],"container-title":["PLOS Computational Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010378","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,8,30]],"date-time":"2022-08-30T18:35:53Z","timestamp":1661884553000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pcbi.1010378"}},"subtitle":[],"editor":[{"given":"Ferhat","family":"Ay","sequence":"first","affiliation":[]}],"short-title":[],"issued":{"date-parts":[[2022,8,30]]},"references-count":106,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2022,8,30]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pcbi.1010378","relation":{},"ISSN":["1553-7358"],"issn-type":[{"value":"1553-7358","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,30]]}}}