{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,21]],"date-time":"2026-02-21T07:29:34Z","timestamp":1771658974466,"version":"3.50.1"},"reference-count":29,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2023,1,11]],"date-time":"2023-01-11T00:00:00Z","timestamp":1673395200000},"content-version":"vor","delay-in-days":10,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100006364","name":"Institut National du Cancer","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100006364","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,1,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:sec>\n                  <jats:title>Motivation<\/jats:title>\n                  <jats:p>Nowadays, epigenetic gene regulations are studied in each part of the biology, from embryonic development to diseases such as cancers and neurodegenerative disorders. Currently, to quantify and compare CpG methylation levels of a specific region of interest, the most accessible technique is the bisulfite sequencing PCR (BSP). However, no existing user-friendly tool is able to analyze data from all approaches of BSP. Therefore, the most convenient way to process results from the direct sequencing of PCR products (direct-BSP) is to manually analyze the chromatogram traces, which is a repetitive and prone to error task.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Results<\/jats:title>\n                  <jats:p>Here, we implement a new R-based tool, called ABSP for analysis of bisulfite sequencing PCR, providing a complete analytic process of both direct-BSP and cloning-BSP data. It uses the raw sequencing trace files (.ab1) as input to compute and compare CpG methylation percentages. It is fully automated and includes a user-friendly interface as a built-in R shiny app, quality control steps and generates publication-ready graphics.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Availability and implementation<\/jats:title>\n                  <jats:p>The ABSP tool and associated data are available on GitHub at https:\/\/github.com\/ABSP-methylation-tool\/ABSP.<\/jats:p>\n               <\/jats:sec>\n               <jats:sec>\n                  <jats:title>Supplementary information<\/jats:title>\n                  <jats:p>Supplementary data are available at Bioinformatics online.<\/jats:p>\n               <\/jats:sec>","DOI":"10.1093\/bioinformatics\/btad008","type":"journal-article","created":{"date-parts":[[2023,1,11]],"date-time":"2023-01-11T17:40:25Z","timestamp":1673458825000},"source":"Crossref","is-referenced-by-count":6,"title":["ABSP: an automated R tool to efficiently analyze region-specific CpG methylation from bisulfite sequencing PCR"],"prefix":"10.1093","volume":"39","author":[{"given":"Marie","family":"Denoulet","sequence":"first","affiliation":[{"name":"CNRS, Inserm, CHU Lille, UMR9020-U1277 - CANTHER\u2014Cancer Heterogeneity Plasticity and Resistance to Therapies, University of Lille , Lille F-59000, France"},{"name":"Institut pour la Recherche sur le Cancer de Lille (IRCL) , Lille F-59000, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mathilde","family":"Brul\u00e9","sequence":"additional","affiliation":[{"name":"CNRS, Inserm, CHU Lille, UMR9020-U1277 - CANTHER\u2014Cancer Heterogeneity Plasticity and Resistance to Therapies, University of Lille , Lille F-59000, France"},{"name":"Institut pour la Recherche sur le Cancer de Lille (IRCL) , Lille F-59000, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Fran\u00e7ois","family":"Anquez","sequence":"additional","affiliation":[{"name":"CNRS, UMR 8523 - PhLAM\u2014Physique des Lasers Atomes et Mol\u00e9cules, University of Lille , Lille F-59000, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Audrey","family":"Vincent","sequence":"additional","affiliation":[{"name":"CNRS, Inserm, CHU Lille, UMR9020-U1277 - CANTHER\u2014Cancer Heterogeneity Plasticity and Resistance to Therapies, University of Lille , Lille F-59000, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julie","family":"Schnipper","sequence":"additional","affiliation":[{"name":"Laboratory of Cellular and Molecular Physiology, UR UPJV 4667, University of Picardie Jules Verne , Amiens 80000, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Eric","family":"Adriaenssens","sequence":"additional","affiliation":[{"name":"CNRS, Inserm, CHU Lille, UMR9020-U1277 - CANTHER\u2014Cancer Heterogeneity Plasticity and Resistance to Therapies, University of Lille , Lille F-59000, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Robert-Alain","family":"Toillon","sequence":"additional","affiliation":[{"name":"CNRS, Inserm, CHU Lille, UMR9020-U1277 - CANTHER\u2014Cancer Heterogeneity Plasticity and Resistance to Therapies, University of Lille , Lille F-59000, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xuefen","family":"Le Bourhis","sequence":"additional","affiliation":[{"name":"CNRS, Inserm, CHU Lille, UMR9020-U1277 - CANTHER\u2014Cancer Heterogeneity Plasticity and Resistance to Therapies, University of Lille , Lille F-59000, France"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5182-2069","authenticated-orcid":false,"given":"Chann","family":"Lagadec","sequence":"additional","affiliation":[{"name":"CNRS, Inserm, CHU Lille, UMR9020-U1277 - CANTHER\u2014Cancer Heterogeneity Plasticity and Resistance to Therapies, University of Lille , Lille F-59000, France"},{"name":"Institut pour la Recherche sur le Cancer de Lille (IRCL) , Lille F-59000, France"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2023,1,11]]},"reference":[{"key":"2023011809302736100_btad008-B1","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1007\/s11033-017-4110-7","article-title":"Region of interest methylation analysis: a comparison of MSP with MS-HRM and direct BSP","volume":"44","author":"Akika","year":"2017","journal-title":"Mol. Biol. Rep"},{"key":"2023011809302736100_btad008-B2","doi-asserted-by":"crossref","first-page":"4067","DOI":"10.1093\/bioinformatics\/bti652","article-title":"BiQ analyzer: visualization and quality control for DNA methylation data from bisulfite sequencing","volume":"21","author":"Bock","year":"2005","journal-title":"Bioinformatics"},{"key":"2023011809302736100_btad008-B3","doi-asserted-by":"crossref","first-page":"evab028","DOI":"10.1093\/gbe\/evab028","article-title":"sangeranalyseR: simple and interactive processing of sanger sequencing data in R","volume":"13","author":"Chao","year":"2021","journal-title":"Genome Biol. Evol"},{"key":"2023011809302736100_btad008-B4","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1007\/978-1-4939-6685-1_15","article-title":"Tools and strategies for analysis of genome-wide and gene-specific DNA methylation patterns","volume":"1537","author":"Chatterjee","year":"2017","journal-title":"Methods Mol. Biol"},{"key":"2023011809302736100_btad008-B5","doi-asserted-by":"crossref","first-page":"488","DOI":"10.1186\/s12885-022-09477-5","article-title":"DNA methylation of miR-138 regulates cell proliferation and EMT in cervical cancer by targeting EZH2","volume":"22","author":"Chen","year":"2022","journal-title":"BMC Cancer"},{"key":"2023011809302736100_btad008-B6","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.ab.2008.02.026","article-title":"Single-molecule polymerase chain reaction reduces bias: application to DNA methylation analysis by bisulfite sequencing","volume":"377","author":"Chhibber","year":"2008","journal-title":"Anal. Biochem"},{"key":"2023011809302736100_btad008-B7","doi-asserted-by":"crossref","first-page":"2990","DOI":"10.1093\/nar\/22.15.2990","article-title":"High sensitivity mapping of methylated cytosines","volume":"22","author":"Clark","year":"1994","journal-title":"Nucleic Acids Res"},{"key":"2023011809302736100_btad008-B8","doi-asserted-by":"crossref","first-page":"113062","DOI":"10.1016\/j.yexcr.2022.113062","article-title":"CYP1A1 contiguous hypermethylation within a putative CpG block is associated with breast cancer progression: feasibility to define boundary motives","volume":"413","author":"Dehdari","year":"2022","journal-title":"Exp. Cell Res"},{"key":"2023011809302736100_btad008-B9","doi-asserted-by":"crossref","first-page":"1827","DOI":"10.1073\/pnas.89.5.1827","article-title":"A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands","volume":"89","author":"Frommer","year":"1992","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"2023011809302736100_btad008-B10","doi-asserted-by":"crossref","first-page":"590","DOI":"10.1038\/s41580-019-0159-6","article-title":"The diverse roles of DNA methylation in mammalian development and disease","volume":"20","author":"Greenberg","year":"2019","journal-title":"Nat. Rev. Mol. Cell Biol"},{"key":"2023011809302736100_btad008-B11","doi-asserted-by":"crossref","first-page":"1053","DOI":"10.1093\/nar\/28.5.1053","article-title":"MethTools\u2014a toolbox to visualize and analyze DNA methylation data","volume":"28","author":"Grunau","year":"2000","journal-title":"Nucleic Acids Res"},{"key":"2023011809302736100_btad008-B12","doi-asserted-by":"crossref","first-page":"2858","DOI":"10.1021\/bi00816a016","article-title":"Reaction of sodium bisulfite with uracil, cytosine, and their derivatives","volume":"9","author":"Hayatsu","year":"1970","journal-title":"Biochemistry"},{"key":"2023011809302736100_btad008-B13","doi-asserted-by":"crossref","first-page":"282","DOI":"10.1038\/labinvest.2009.132","article-title":"Rapid quantification of DNA methylation by measuring relative peak heights in direct bisulfite-PCR sequencing traces","volume":"90","author":"Jiang","year":"2010","journal-title":"Lab. Invest"},{"key":"2023011809302736100_btad008-B14","doi-asserted-by":"crossref","first-page":"484","DOI":"10.1038\/nrg3230","article-title":"Functions of DNA methylation: islands, start sites, gene bodies and beyond","volume":"13","author":"Jones","year":"2012","journal-title":"Nat. Rev. Genet"},{"key":"2023011809302736100_btad008-B15","doi-asserted-by":"crossref","first-page":"W170","DOI":"10.1093\/nar\/gkn294","article-title":"QUMA: quantification tool for methylation analysis","volume":"36","author":"Kumaki","year":"2008","journal-title":"Nucleic Acids Res"},{"key":"2023011809302736100_btad008-B16","doi-asserted-by":"crossref","first-page":"3005","DOI":"10.1093\/bioinformatics\/bth346","article-title":"Quantitative DNA methylation analysis based on four-dye trace data from direct sequencing of PCR amplificates","volume":"20","author":"Lewin","year":"2004","journal-title":"Bioinformatics"},{"key":"2023011809302736100_btad008-B17","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1007\/978-1-61779-316-5_2","article-title":"DNA methylation detection: bisulfite genomic sequencing analysis","volume":"791","author":"Li","year":"2011","journal-title":"Methods Mol. Biol"},{"key":"2023011809302736100_btad008-B18","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1186\/1751-0473-9-11","article-title":"Methylation plotter: a web tool for dynamic visualization of DNA methylation data","volume":"9","author":"Mallona","year":"2014","journal-title":"Source Code Biol. Med"},{"key":"2023011809302736100_btad008-B19","doi-asserted-by":"crossref","first-page":"4247","DOI":"10.3390\/ijms22084247","article-title":"DNA methylation in solid tumors: functions and methods of detection","volume":"22","author":"Martisova","year":"2021","journal-title":"Int. J. Mol. Sci. USA"},{"key":"2023011809302736100_btad008-B20","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/s11060-006-9309-8","article-title":"Frequent but borderline methylation of p16INK4a and TIMP3 in medulloblastoma and sPNET revealed by quantitative analyses","volume":"83","author":"M\u00fchlisch","year":"2007","journal-title":"J. Neurooncol"},{"key":"2023011809302736100_btad008-B21","doi-asserted-by":"crossref","first-page":"561","DOI":"10.2217\/epi.10.32","article-title":"The implications of heterogeneous DNA methylation for the accurate quantification of methylation","volume":"2","author":"Mikeska","year":"2010","journal-title":"Epigenomics"},{"key":"2023011809302736100_btad008-B22","doi-asserted-by":"crossref","first-page":"571","DOI":"10.3389\/fpsyt.2020.00571","article-title":"DNA methylation of the t-PA gene differs between various immune cell subtypes isolated from depressed patients receiving electroconvulsive therapy","volume":"11","author":"Moschny","year":"2020","journal-title":"Front. Psychiatry"},{"key":"2023011809302736100_btad008-B23","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.ymeth.2020.06.021","article-title":"Methods for analysis of specific DNA methylation status","volume":"187","author":"Pajares","year":"2021","journal-title":"Methods"},{"key":"2023011809302736100_btad008-B24","doi-asserted-by":"crossref","first-page":"7.24.1","DOI":"10.1002\/0471142301.ns0724s60","article-title":"Direct bisulfite sequencing for examination of DNA methylation with gene and nucleotide resolution from brain tissues","volume":"60","author":"Parrish","year":"2012","journal-title":"Curr. Protoc. Neurosci"},{"key":"2023011809302736100_btad008-B25","doi-asserted-by":"crossref","first-page":"126","DOI":"10.2144\/96211rr04","article-title":"Cytosine methylation: quantitation by automated genomic sequencing and GENESCAN analysis","volume":"21","author":"Paul","year":"1996","journal-title":"Biotechniques"},{"key":"2023011809302736100_btad008-B26","doi-asserted-by":"crossref","first-page":"331","DOI":"10.1016\/j.bbrc.2003.08.008","article-title":"Quantification of single nucleotide polymorphisms by automated DNA sequencing","volume":"309","author":"Qiu","year":"2003","journal-title":"Biochem. Biophys. Res. Commun"},{"key":"2023011809302736100_btad008-B27","doi-asserted-by":"crossref","first-page":"230","DOI":"10.1186\/1471-2105-11-230","article-title":"BISMA - fast and accurate bisulfite sequencing data analysis of individual clones from unique and repetitive sequences","volume":"11","author":"Rohde","year":"2010","journal-title":"BMC Bioinformatics"},{"key":"2023011809302736100_btad008-B28","doi-asserted-by":"crossref","first-page":"191","DOI":"10.1093\/ijnp\/pyaa081","article-title":"Serotonin transporter gene promoter hypomethylation as a predictor of antidepressant treatment response in major depression: a replication study","volume":"24","author":"Schiele","year":"2021","journal-title":"Int. J. Neuropsychopharmacol"},{"key":"2023011809302736100_btad008-B29","doi-asserted-by":"crossref","first-page":"3818","DOI":"10.1021\/ac980067t","article-title":"Combating PCR bias in Bisulfite-Based cytosine methylation analysis. betaine-modified cytosine deamination PCR","volume":"70","author":"Voss","year":"1998","journal-title":"Anal. Chem"}],"container-title":["Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/bioinformatics\/advance-article-pdf\/doi\/10.1093\/bioinformatics\/btad008\/48614764\/btad008.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/39\/1\/btad008\/48755307\/btad008.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article-pdf\/39\/1\/btad008\/48755307\/btad008.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,18]],"date-time":"2023-01-18T09:33:30Z","timestamp":1674034410000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/bioinformatics\/article\/doi\/10.1093\/bioinformatics\/btad008\/6984714"}},"subtitle":[],"editor":[{"given":"Janet","family":"Kelso","sequence":"additional","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2023,1,1]]},"references-count":29,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2023,1,1]]}},"URL":"https:\/\/doi.org\/10.1093\/bioinformatics\/btad008","relation":{},"ISSN":["1367-4811"],"issn-type":[{"value":"1367-4811","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,1,1]]},"published":{"date-parts":[[2023,1,1]]},"article-number":"btad008"}}