{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,22]],"date-time":"2025-10-22T02:58:01Z","timestamp":1761101881540,"version":"3.37.0"},"reference-count":42,"publisher":"Oxford University Press (OUP)","issue":"14","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2009,7,15]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Motivation: The relationship between nucleosome positioning and gene regulation is fundamental yet complex. Previous studies on genomic nucleosome positions have revealed a correlation between nucleosome occupancy on promoters and gene expression levels. Many of these studies focused on individual nucleosomes, especially those proximal to transcription start sites. To study the collective effect of multiple nucleosomes on the gene expression, we developed a mathematical approach based on autocorrelation to relate genomic nucleosome organization to gene regulation.<\/jats:p><jats:p>Results: We found that nucleosome organization in gene promoters can be well described by autocorrelation transformation. Some promoters show obvious periods in their nucleosome organization, while others have no clear periodicity. The genes with periodic nucleosome organization in promoters tend to be lower expressed than the genes without periodic nucleosome organization. These suggest that regular organization of nucleosomes plays a critical role in gene regulation. To quantitatively associate nucleosome organization and gene expression, we predicted gene expression solely based on nucleosome status and found that nucleosome status accounts for \u223c25% of the observed gene expression variability. Furthermore, we explored the underlying forces that maintain the periodicity in nucleosome organization, namely intrinsic (i.e. DNA sequence) and extrinsic forces (i.e. chromatin remodeling factors). We found that the extrinsic factors play a critical role in maintaining the periodic nucleosome organization.<\/jats:p><jats:p>Contact: \u00a0jiang.qian@jhmi.edu<\/jats:p><jats:p>Supplementary information: \u00a0Supplementary data are available at Bioinformatics online.<\/jats:p>","DOI":"10.1093\/bioinformatics\/btp323","type":"journal-article","created":{"date-parts":[[2009,5,16]],"date-time":"2009-05-16T00:14:09Z","timestamp":1242432849000},"page":"1782-1788","source":"Crossref","is-referenced-by-count":13,"title":["Relating periodicity of nucleosome organization and gene regulation"],"prefix":"10.1093","volume":"25","author":[{"given":"Jun","family":"Wan","sequence":"first","affiliation":[{"name":"1 Wilmer Institute, 2 Celluar & Molecular Medicine Program, 3 Department of Molecular Biology and Genetics, 4 Department of Neuroscience and 5 McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jimmy","family":"Lin","sequence":"additional","affiliation":[{"name":"1 Wilmer Institute, 2 Celluar & Molecular Medicine Program, 3 Department of Molecular Biology and Genetics, 4 Department of Neuroscience and 5 McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Donald J.","family":"Zack","sequence":"additional","affiliation":[{"name":"1 Wilmer Institute, 2 Celluar & Molecular Medicine Program, 3 Department of Molecular Biology and Genetics, 4 Department of Neuroscience and 5 McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"},{"name":"1 Wilmer Institute, 2 Celluar & Molecular Medicine Program, 3 Department of Molecular Biology and Genetics, 4 Department of Neuroscience and 5 McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"},{"name":"1 Wilmer Institute, 2 Celluar & Molecular Medicine Program, 3 Department of Molecular Biology and Genetics, 4 Department of Neuroscience and 5 McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"},{"name":"1 Wilmer Institute, 2 Celluar & Molecular Medicine Program, 3 Department of Molecular Biology and Genetics, 4 Department of Neuroscience and 5 McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiang","family":"Qian","sequence":"additional","affiliation":[{"name":"1 Wilmer Institute, 2 Celluar & Molecular Medicine Program, 3 Department of Molecular Biology and Genetics, 4 Department of Neuroscience and 5 McKusick-Nathans Institute of Genetic Medicine, Johns Hopkins University School of Medicine, Baltimore, MD 21287, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2009,5,15]]},"reference":[{"key":"2023013112050648300_B1","doi-asserted-by":"crossref","first-page":"572","DOI":"10.1038\/nature05632","article-title":"Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome","volume":"446","author":"Albert","year":"2007","journal-title":"Nature"},{"key":"2023013112050648300_B2","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1016\/j.cell.2007.05.009","article-title":"High-resolution profiling of histone methylations in the human genome","volume":"129","author":"Barski","year":"2007","journal-title":"Cell"},{"key":"2023013112050648300_B3","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1016\/S0092-8674(04)00304-6","article-title":"Predicting gene expression from sequence","volume":"117","author":"Beer","year":"2004","journal-title":"Cell"},{"key":"2023013112050648300_B4","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1111\/j.2517-6161.1995.tb02031.x","article-title":"Controlling the false discovery rate: a practical and powerful approach to multiple testing","volume":"57","author":"Benjamini","year":"1995","journal-title":"J. R. Stat. Soc. Ser. B"},{"key":"2023013112050648300_B5","doi-asserted-by":"crossref","first-page":"8695","DOI":"10.1073\/pnas.082249499","article-title":"Methylation of histone H3 Lys 4 in coding regions of active genes","volume":"99","author":"Bernstein","year":"2002","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023013112050648300_B6","doi-asserted-by":"crossref","first-page":"R62","DOI":"10.1186\/gb-2004-5-9-r62","article-title":"Global nucleosome occupancy in yeast","volume":"5","author":"Bernstein","year":"2004","journal-title":"Genome Biol."},{"key":"2023013112050648300_B7","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1038\/84792","article-title":"Regulatory element detection using correlation with expression","volume":"27","author":"Bussemaker","year":"2001","journal-title":"Nat. Genet."},{"key":"2023013112050648300_B8","doi-asserted-by":"crossref","first-page":"3339","DOI":"10.1073\/pnas.0630591100","article-title":"Integrating regulatory motif discovery and genome-wide expression analysis","volume":"100","author":"Conlon","year":"2003","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023013112050648300_B9","doi-asserted-by":"crossref","first-page":"438","DOI":"10.1038\/ng.324","article-title":"Gene expression divergence in yeast is coupled to evolution of DNA-encoded nucleosome organization","volume":"41","author":"Field","year":"2009","journal-title":"Nat. Genet."},{"key":"2023013112050648300_B10","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1101\/gad.1139604","article-title":"Acf1 confers unique activities to ACF\/CHRAC and promotes the formation rather than disruption of chromatin in vivo","volume":"18","author":"Fyodorov","year":"2004","journal-title":"Genes Dev."},{"key":"2023013112050648300_B11","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1016\/j.cell.2007.01.030","article-title":"Chromatin challenges during DNA replication and repair","volume":"128","author":"Groth","year":"2007","journal-title":"Cell"},{"key":"2023013112050648300_B12","doi-asserted-by":"crossref","first-page":"1210","DOI":"10.1038\/ng1878","article-title":"Nucleosome positions predicted through comparative genomics","volume":"38","author":"Ioshikhes","year":"2006","journal-title":"Nat. Genet."},{"key":"2023013112050648300_B13","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1016\/S0092-8674(00)80321-9","article-title":"ACF, an ISWI-containing and ATP-utilizing chromatin assembly and remodeling factor","volume":"90","author":"Ito","year":"1997","journal-title":"Cell"},{"key":"2023013112050648300_B14","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1038\/nature07667","article-title":"The DNA-encoded nucleosome organization of a eukaryotic genome","volume":"458","author":"Kaplan","year":"2009","journal-title":"Nature"},{"key":"2023013112050648300_B15","doi-asserted-by":"crossref","first-page":"868","DOI":"10.1126\/science.184.4139.868","article-title":"Chromatin structure: a repeating unit of histones and DNA","volume":"184","author":"Kornberg","year":"1974","journal-title":"Science"},{"key":"2023013112050648300_B16","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1016\/S0092-8674(00)81958-3","article-title":"Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome","volume":"98","author":"Kornberg","year":"1999","journal-title":"Cell"},{"key":"2023013112050648300_B17","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1016\/j.cell.2004.05.023","article-title":"Mapping global histone acetylation patterns to gene expression","volume":"117","author":"Kurdistani","year":"2004","journal-title":"Cell"},{"key":"2023013112050648300_B18","doi-asserted-by":"crossref","first-page":"900","DOI":"10.1038\/ng1400","article-title":"Evidence for nucleosome depletion at active regulatory regions genome-wide","volume":"36","author":"Lee","year":"2004","journal-title":"Nat. Genet."},{"key":"2023013112050648300_B19","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1038\/ng2117","article-title":"A high-resolution atlas of nucleosome occupancy in yeast","volume":"39","author":"Lee","year":"2007","journal-title":"Nat. Genet."},{"key":"2023013112050648300_B20","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1186\/1471-2105-7-113","article-title":"An improved map of conserved regulatory sites for Saccharomyces cerevisiae","volume":"7","author":"MacIsaac","year":"2006","journal-title":"BMC Bioinformatics"},{"key":"2023013112050648300_B21","doi-asserted-by":"crossref","first-page":"1073","DOI":"10.1101\/gr.078261.108","article-title":"A barrier nucleosome model for statistical positioning of nucleosomes throughout the yeast genome","volume":"18","author":"Mavrich","year":"2008","journal-title":"Genome Res"},{"key":"2023013112050648300_B22","doi-asserted-by":"crossref","first-page":"831","DOI":"10.1016\/0092-8674(83)90025-9","article-title":"Higher order structure of chromatin: orientation of nucleosomes within the 30 nm chromatin solenoid is independent of species and spacer length","volume":"33","author":"McGhee","year":"1983","journal-title":"Cell"},{"key":"2023013112050648300_B23","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1101\/gad.1395506","article-title":"Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast","volume":"20","author":"Millar","year":"2006","journal-title":"Genes Dev."},{"key":"2023013112050648300_B24","doi-asserted-by":"crossref","first-page":"1828","DOI":"10.1093\/bioinformatics\/btm236","article-title":"ChromatinDB: a database of genome-wide histone modification patterns for Saccharomyces cerevisiae","volume":"23","author":"O'Connor","year":"2007","journal-title":"Bioinformatics"},{"key":"2023013112050648300_B25","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1038\/nbt1279","article-title":"High-throughput mapping of the chromatin structure of human promoters","volume":"25","author":"Ozsolak","year":"2007","journal-title":"Nat. Biotechnol."},{"key":"2023013112050648300_B26","doi-asserted-by":"crossref","first-page":"1170","DOI":"10.1101\/gr.6101007","article-title":"Nucleosome positioning signals in genomic DNA","volume":"17","author":"Peckham","year":"2007","journal-title":"Genome Res."},{"key":"2023013112050648300_B27","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1016\/0167-8655(94)90127-9","article-title":"Floating search methods in feature selection","volume":"15","author":"Pudil","year":"1994","journal-title":"Pattern Recognit. Lett"},{"key":"2023013112050648300_B28","doi-asserted-by":"crossref","first-page":"9447","DOI":"10.1128\/MCB.25.21.9447-9459.2005","article-title":"Dimethylation of histone H3 at lysine 36 demarcates regulatory and nonregulatory chromatin genome-wide","volume":"25","author":"Rao","year":"2005","journal-title":"Mol. Cell. Biol."},{"key":"2023013112050648300_B29","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1038\/nature01595","article-title":"The structure of DNA in the nucleosome core","volume":"423","author":"Richmond","year":"2003","journal-title":"Nature"},{"key":"2023013112050648300_B30","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1038\/nature04979","article-title":"A genomic code for nucleosome positioning","volume":"442","author":"Segal","year":"2006","journal-title":"Nature"},{"key":"2023013112050648300_B31","doi-asserted-by":"crossref","first-page":"561","DOI":"10.1146\/annurev.ps.46.020195.003021","article-title":"Multiple hypothesis testing","volume":"46","author":"Shaffer","year":"1995","journal-title":"Ann. Rev. Psychol."},{"key":"2023013112050648300_B32","doi-asserted-by":"crossref","first-page":"e65","DOI":"10.1371\/journal.pbio.0060065","article-title":"Dynamic remodeling of individual nucleosomes across a eukaryotic genome in response to transcriptional perturbation","volume":"6","author":"Shivaswamy","year":"2008","journal-title":"PLoS Biol."},{"key":"2023013112050648300_B33","doi-asserted-by":"crossref","first-page":"6275","DOI":"10.1073\/pnas.0508169103","article-title":"DNA motifs in human and mouse proximal promoters predict tissue-specific expression","volume":"103","author":"Smith","year":"2006","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"2023013112050648300_B34","doi-asserted-by":"crossref","first-page":"686","DOI":"10.1101\/gad.13.6.686","article-title":"Characterization of the imitation switch subfamily of ATP-dependent chromatin-remodeling factors in Saccharomyces cerevisiae","volume":"13","author":"Tsukiyama","year":"1999","journal-title":"Genes Dev."},{"key":"2023013112050648300_B35","doi-asserted-by":"crossref","first-page":"1031","DOI":"10.1038\/nature06391","article-title":"Chromatin remodelling at promoters suppresses antisense transcription","volume":"450","author":"Whitehouse","year":"2007","journal-title":"Nature"},{"key":"2023013112050648300_B36","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/0092-8674(85)90025-X","article-title":"Structure of the 300A chromatin filament: X-ray diffraction from oriented samples","volume":"43","author":"Widom","year":"1985","journal-title":"Cell"},{"key":"2023013112050648300_B37","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1016\/j.cell.2005.03.011","article-title":"Acetylation in histone H3 globular domain regulates gene expression in yeast","volume":"121","author":"Xu","year":"2005","journal-title":"Cell"},{"key":"2023013112050648300_B38","doi-asserted-by":"crossref","first-page":"1078","DOI":"10.1038\/nsmb1170","article-title":"The chromatin-remodeling enzyme ACF is an ATP-dependent DNA length sensor that regulates nucleosome spacing","volume":"13","author":"Yang","year":"2006","journal-title":"Nat. Struct. Mol. Biol."},{"key":"2023013112050648300_B39","doi-asserted-by":"crossref","first-page":"e13","DOI":"10.1371\/journal.pcbi.0040013","article-title":"Genomic sequence is highly predictive of local nucleosome depletion","volume":"4","author":"Yuan","year":"2008","journal-title":"PLoS Comput. Biol."},{"key":"2023013112050648300_B40","doi-asserted-by":"crossref","first-page":"626","DOI":"10.1126\/science.1112178","article-title":"Genome-scale identification of nucleosome positions in S. cerevisiae","volume":"309","author":"Yuan","year":"2005","journal-title":"Science"},{"key":"2023013112050648300_B41","doi-asserted-by":"crossref","first-page":"R70","DOI":"10.1186\/gb-2006-7-8-r70","article-title":"Statistical assessment of the global regulatory role of histone acetylation in Saccharomyces cerevisiae","volume":"7","author":"Yuan","year":"2006","journal-title":"Genome Biol."},{"key":"2023013112050648300_B42","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.cell.2005.08.036","article-title":"Genome-wide dynamics of Htz1, a histone H2A variant that poises repressed\/basal promoters for activation through histone loss","volume":"123","author":"Zhang","year":"2005","journal-title":"Cell"}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/25\/14\/1782\/48993647\/bioinformatics_25_14_1782.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/25\/14\/1782\/48993647\/bioinformatics_25_14_1782.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,2,9]],"date-time":"2025-02-09T13:12:22Z","timestamp":1739106742000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/25\/14\/1782\/225548"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,5,15]]},"references-count":42,"journal-issue":{"issue":"14","published-print":{"date-parts":[[2009,7,15]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/btp323","relation":{},"ISSN":["1367-4811","1367-4803"],"issn-type":[{"type":"electronic","value":"1367-4811"},{"type":"print","value":"1367-4803"}],"subject":[],"published-other":{"date-parts":[[2009,7,15]]},"published":{"date-parts":[[2009,5,15]]}}}