{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,5]],"date-time":"2025-11-05T14:13:51Z","timestamp":1762352031911},"reference-count":30,"publisher":"Springer Science and Business Media LLC","issue":"1","content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Bioinformatics"],"published-print":{"date-parts":[[2009,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:sec>\n            <jats:title>Background<\/jats:title>\n            <jats:p>Time series gene expression data analysis is used widely to study the dynamics of various cell processes. Most of the time series data available today consist of few time points only, thus making the application of standard clustering techniques difficult.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Results<\/jats:title>\n            <jats:p>We developed two new algorithms that are capable of extracting biological patterns from short time point series gene expression data. The two algorithms, <jats:italic>ASTRO<\/jats:italic> and <jats:italic>MiMeSR<\/jats:italic>, are inspired by the <jats:italic>rank order preserving<\/jats:italic> framework and the <jats:italic>minimum mean squared residue<\/jats:italic> approach, respectively. However, <jats:italic>ASTRO<\/jats:italic> and <jats:italic>MiMeSR<\/jats:italic> differ from previous approaches in that they take advantage of the relatively few number of time points in order to reduce the problem from NP-hard to linear. Tested on well-defined short time expression data, we found that our approaches are robust to noise, as well as to random patterns, and that they can correctly detect the temporal expression profile of relevant functional categories. Evaluation of our methods was performed using Gene Ontology (GO) annotations and chromatin immunoprecipitation (ChIP-chip) data.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Conclusion<\/jats:title>\n            <jats:p>Our approaches generally outperform both standard clustering algorithms and algorithms designed specifically for clustering of short time series gene expression data. Both algorithms are available at <jats:ext-link xmlns:xlink=\"http:\/\/www.w3.org\/1999\/xlink\" xlink:href=\"http:\/\/www.benoslab.pitt.edu\/astro\/\" ext-link-type=\"uri\">http:\/\/www.benoslab.pitt.edu\/astro\/<\/jats:ext-link>.<\/jats:p>\n          <\/jats:sec>","DOI":"10.1186\/1471-2105-10-255","type":"journal-article","created":{"date-parts":[[2009,8,20]],"date-time":"2009-08-20T18:13:37Z","timestamp":1250792017000},"update-policy":"http:\/\/dx.doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":16,"title":["Extracting biologically significant patterns from short time series gene expression data"],"prefix":"10.1186","volume":"10","author":[{"given":"Alain B","family":"Tchagang","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Kevin V","family":"Bui","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Thomas","family":"McGinnis","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Panayiotis V","family":"Benos","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2009,8,20]]},"reference":[{"issue":"12","key":"2985_CR1","doi-asserted-by":"publisher","first-page":"3273","DOI":"10.1091\/mbc.9.12.3273","volume":"9","author":"PT Spellman","year":"1998","unstructured":"Spellman PT, Sherlock G, Zhang MQ, Iyer VR, Anders K, Eisen MB, Brown PO, Botstein D, Futcher B: Comprehensive identification of cell cycle-regulated genes of the yeast Saccharomyces cerevisiae by microarray hybridization. Mol Biol Cell 1998, 9(12):3273\u20133297.","journal-title":"Mol Biol Cell"},{"issue":"5590","key":"2985_CR2","doi-asserted-by":"publisher","first-page":"2270","DOI":"10.1126\/science.1072152","volume":"297","author":"MN Arbeitman","year":"2002","unstructured":"Arbeitman MN, Furlong EE, Imam F, Johnson E, Null BH, Baker BS, Krasnow MA, Scott MP, Davis RW, White KP: Gene expression during the life cycle of Drosophila melanogaster. Science 2002, 297(5590):2270\u20132275. 10.1126\/science.1072152","journal-title":"Science"},{"issue":"12","key":"2985_CR3","doi-asserted-by":"publisher","first-page":"4241","DOI":"10.1091\/mbc.11.12.4241","volume":"11","author":"AP Gasch","year":"2000","unstructured":"Gasch AP, Spellman PT, Kao CM, Carmel-Harel O, Eisen MB, Storz G, Botstein D, Brown PO: Genomic expression programs in the response of yeast cells to environmental changes. Mol Biol Cell 2000, 11(12):4241\u20134257.","journal-title":"Mol Biol Cell"},{"issue":"23","key":"2985_CR4","doi-asserted-by":"publisher","first-page":"15136","DOI":"10.1073\/pnas.182558799","volume":"99","author":"K Guillemin","year":"2002","unstructured":"Guillemin K, Salama NR, Tompkins LS, Falkow S: Cag pathogenicity island-specific responses of gastric epithelial cells to Helicobacter pylori infection. Proc Natl Acad Sci USA 2002, 99(23):15136\u201315141. 10.1073\/pnas.182558799","journal-title":"Proc Natl Acad Sci USA"},{"issue":"25","key":"2985_CR5","doi-asserted-by":"publisher","first-page":"14863","DOI":"10.1073\/pnas.95.25.14863","volume":"95","author":"MB Eisen","year":"1998","unstructured":"Eisen MB, Spellman PT, Brown PO, Botstein D: Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci USA 1998, 95(25):14863\u201314868. 10.1073\/pnas.95.25.14863","journal-title":"Proc Natl Acad Sci USA"},{"issue":"3","key":"2985_CR6","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1038\/10343","volume":"22","author":"S Tavazoie","year":"1999","unstructured":"Tavazoie S, Hughes JD, Campbell MJ, Cho RJ, Church GM: Systematic determination of genetic network architecture. Nat Genet 1999, 22(3):281\u2013285. 10.1038\/10343","journal-title":"Nat Genet"},{"issue":"3\u20134","key":"2985_CR7","doi-asserted-by":"publisher","first-page":"601","DOI":"10.1089\/106652700750050961","volume":"7","author":"N Friedman","year":"2000","unstructured":"Friedman N, Linial M, Nachman I, Pe'er D: Using Bayesian networks to analyze expression data. J Comput Biol 2000, 7(3\u20134):601\u2013620. 10.1089\/106652700750050961","journal-title":"J Comput Biol"},{"issue":"6","key":"2985_CR8","doi-asserted-by":"publisher","first-page":"2907","DOI":"10.1073\/pnas.96.6.2907","volume":"96","author":"P Tamayo","year":"1999","unstructured":"Tamayo P, Slonim D, Mesirov J, Zhu Q, Kitareewan S, Dmitrovsky E, Lander ES, Golub TR: Interpreting patterns of gene expression with self-organizing maps: methods and application to hematopoietic differentiation. Proc Natl Acad Sci USA 1999, 96(6):2907\u20132912. 10.1073\/pnas.96.6.2907","journal-title":"Proc Natl Acad Sci USA"},{"issue":"3\u20134","key":"2985_CR9","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1089\/10665270360688057","volume":"10","author":"Z Bar-Joseph","year":"2003","unstructured":"Bar-Joseph Z, Gerber GK, Gifford DK, Jaakkola TS, Simon I: Continuous representations of time-series gene expression data. J Comput Biol 2003, 10(3\u20134):341\u2013356. 10.1089\/10665270360688057","journal-title":"J Comput Biol"},{"issue":"Suppl 1","key":"2985_CR10","doi-asserted-by":"publisher","first-page":"i255","DOI":"10.1093\/bioinformatics\/btg1036","volume":"19","author":"A Schliep","year":"2003","unstructured":"Schliep A, Schonhuth A, Steinhoff C: Using hidden Markov models to analyze gene expression time course data. Bioinformatics 2003, 19(Suppl 1):i255\u2013263. 10.1093\/bioinformatics\/btg1036","journal-title":"Bioinformatics"},{"issue":"14","key":"2985_CR11","doi-asserted-by":"publisher","first-page":"9121","DOI":"10.1073\/pnas.132656399","volume":"99","author":"MF Ramoni","year":"2002","unstructured":"Ramoni MF, Sebastiani P, Kohane IS: Cluster analysis of gene expression dynamics. Proc Natl Acad Sci USA 2002, 99(14):9121\u20139126. 10.1073\/pnas.132656399","journal-title":"Proc Natl Acad Sci USA"},{"issue":"11","key":"2985_CR12","doi-asserted-by":"publisher","first-page":"1477","DOI":"10.1093\/bioinformatics\/18.11.1477","volume":"18","author":"MJ De Hoon","year":"2002","unstructured":"De Hoon MJ, Imoto S, Miyano S: Statistical analysis of a small set of time-ordered gene expression data using linear splines. Bioinformatics 2002, 18(11):1477\u20131485. 10.1093\/bioinformatics\/18.11.1477","journal-title":"Bioinformatics"},{"issue":"7","key":"2985_CR13","doi-asserted-by":"publisher","first-page":"834","DOI":"10.1093\/bioinformatics\/btg093","volume":"19","author":"SD Peddada","year":"2003","unstructured":"Peddada SD, Lobenhofer EK, Li L, Afshari CA, Weinberg CR, Umbach DM: Gene selection and clustering for time-course and dose-response microarray experiments using order-restricted inference. Bioinformatics 2003, 19(7):834\u2013841. 10.1093\/bioinformatics\/btg093","journal-title":"Bioinformatics"},{"key":"2985_CR14","first-page":"83","volume":"38","author":"R Sharan","year":"2002","unstructured":"Sharan R, Elkon R, Shamir R: Cluster analysis and its applications to gene expression data. Ernst Schering Res Found Workshop 2002, (38):83\u2013108.","journal-title":"Ernst Schering Res Found Workshop"},{"issue":"Suppl 1","key":"2985_CR15","doi-asserted-by":"publisher","first-page":"i159","DOI":"10.1093\/bioinformatics\/bti1022","volume":"21","author":"J Ernst","year":"2005","unstructured":"Ernst J, Nau GJ, Bar-Joseph Z: Clustering short time series gene expression data. Bioinformatics 2005, 21(Suppl 1):i159\u2013168. 10.1093\/bioinformatics\/bti1022","journal-title":"Bioinformatics"},{"issue":"2","key":"2985_CR16","doi-asserted-by":"publisher","first-page":"447","DOI":"10.1093\/nar\/gkh205","volume":"32","author":"X Lu","year":"2004","unstructured":"Lu X, Zhang W, Qin ZS, Kwast KE, Liu JS: Statistical resynchronization and Bayesian detection of periodically expressed genes. Nucleic Acids Res 2004, 32(2):447\u2013455. 10.1093\/nar\/gkh205","journal-title":"Nucleic Acids Res"},{"issue":"1","key":"2985_CR17","first-page":"35","volume":"2","author":"CS Moller-Levet","year":"2003","unstructured":"Moller-Levet CS, Cho KH, Wolkenhauer O: Microarray data clustering based on temporal variation: FCV with TSD preclustering. Appl Bioinformatics 2003, 2(1):35\u201345.","journal-title":"Appl Bioinformatics"},{"issue":"10","key":"2985_CR18","doi-asserted-by":"publisher","first-page":"5631","DOI":"10.1073\/pnas.101013198","volume":"98","author":"LP Zhao","year":"2001","unstructured":"Zhao LP, Prentice R, Breeden L: Statistical modeling of large microarray data sets to identify stimulus-response profiles. Proc Natl Acad Sci USA 2001, 98(10):5631\u20135636. 10.1073\/pnas.101013198","journal-title":"Proc Natl Acad Sci USA"},{"issue":"3\u20134","key":"2985_CR19","doi-asserted-by":"publisher","first-page":"373","DOI":"10.1089\/10665270360688075","volume":"10","author":"A Ben-Dor","year":"2003","unstructured":"Ben-Dor A, Chor B, Karp R, Yakhini Z: Discovering local structure in gene expression data: the order-preserving submatrix problem. J Comput Biol 2003, 10(3\u20134):373\u2013384. 10.1089\/10665270360688075","journal-title":"J Comput Biol"},{"key":"2985_CR20","first-page":"93","volume":"8","author":"Y Cheng","year":"2000","unstructured":"Cheng Y, Church GM: Biclustering of expression data. Proc Int Conf Intell Syst Mol Biol 2000, 8: 93\u2013103.","journal-title":"Proc Int Conf Intell Syst Mol Biol"},{"issue":"1","key":"2985_CR21","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1109\/TCBB.2004.2","volume":"1","author":"SC Madeira","year":"2004","unstructured":"Madeira SC, Oliveira AL: Biclustering Algorithms for Biological Data Analysis: A Survey. IEEE\/ACM Transactions on Computational Biology and Bioinformatics 2004, 1(1):24\u201345. 10.1109\/TCBB.2004.2","journal-title":"IEEE\/ACM Transactions on Computational Biology and Bioinformatics"},{"issue":"9","key":"2985_CR22","doi-asserted-by":"publisher","first-page":"763","DOI":"10.1093\/bioinformatics\/17.9.763","volume":"17","author":"KY Yeung","year":"2001","unstructured":"Yeung KY, Ruzzo WL: Principal component analysis for clustering gene expression data. Bioinformatics 2001, 17(9):763\u2013774. 10.1093\/bioinformatics\/17.9.763","journal-title":"Bioinformatics"},{"key":"2985_CR23","doi-asserted-by":"crossref","unstructured":"Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R, Eilbeck K, Lewis S, Marshall B, Mungall C, et al.: The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 2004, (32 Database):D258\u2013261.","DOI":"10.1093\/nar\/gkh036"},{"issue":"7004","key":"2985_CR24","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1038\/nature02800","volume":"431","author":"CT Harbison","year":"2004","unstructured":"Harbison CT, Gordon DB, Lee TI, Rinaldi NJ, Macisaac KD, Danford TW, Hannett NM, Tagne JB, Reynolds DB, Yoo J, et al.: Transcriptional regulatory code of a eukaryotic genome. Nature 2004, 431(7004):99\u2013104. 10.1038\/nature02800","journal-title":"Nature"},{"key":"2985_CR25","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1186\/1471-2105-7-191","volume":"7","author":"J Ernst","year":"2006","unstructured":"Ernst J, Bar-Joseph Z: STEM: a tool for the analysis of short time series gene expression data. BMC Bioinformatics 2006, 7: 191. 10.1186\/1471-2105-7-191","journal-title":"BMC Bioinformatics"},{"key":"2985_CR26","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1038\/msb4100115","volume":"3","author":"J Ernst","year":"2007","unstructured":"Ernst J, Vainas O, Harbison CT, Simon I, Bar-Joseph Z: Reconstructing dynamic regulatory maps. Mol Syst Biol 2007, 3: 74. 10.1038\/msb4100115","journal-title":"Mol Syst Biol"},{"issue":"20","key":"2985_CR27","doi-asserted-by":"publisher","first-page":"2491","DOI":"10.1101\/gad.1228804","volume":"18","author":"P Jorgensen","year":"2004","unstructured":"Jorgensen P, Rupes I, Sharom JR, Schneper L, Broach JR, Tyers M: A dynamic transcriptional network communicates growth potential to ribosome synthesis and critical cell size. Genes Dev 2004, 18(20):2491\u20132505. 10.1101\/gad.1228804","journal-title":"Genes Dev"},{"issue":"7","key":"2985_CR28","doi-asserted-by":"publisher","first-page":"3640","DOI":"10.1128\/MCB.17.7.3640","volume":"17","author":"PL Blaiseau","year":"1997","unstructured":"Blaiseau PL, Isnard AD, Surdin-Kerjan Y, Thomas D: Met31p and Met32p, two related zinc finger proteins, are involved in transcriptional regulation of yeast sulfur amino acid metabolism. Mol Cell Biol 1997, 17(7):3640\u20133648.","journal-title":"Mol Cell Biol"},{"key":"2985_CR29","first-page":"111","volume":"12","author":"S Dudoit","year":"2002","unstructured":"Dudoit S, Yee Hwa Yang YH, Callow MJ, Speed TP: Statistical methods for identifying differentially expressed genes in replicated cDNA microarray experiments. Statistica sinica 2002, 12: 111\u2013139.","journal-title":"Statistica sinica"},{"key":"2985_CR30","volume-title":"IEEE International Workshop On Genomic Signal Processing and Statistics: 2005","author":"A Hassibi","year":"2005","unstructured":"Hassibi A, Vikalo H: A probabilistic model for inherent noise and systematic errors of microarrays. In IEEE International Workshop On Genomic Signal Processing and Statistics: 2005. New Port, Rhode Island, USA; 2005."}],"container-title":["BMC Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/1471-2105-10-255.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,8,31]],"date-time":"2021-08-31T21:40:35Z","timestamp":1630446035000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcbioinformatics.biomedcentral.com\/articles\/10.1186\/1471-2105-10-255"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,8,20]]},"references-count":30,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2009,12]]}},"alternative-id":["2985"],"URL":"https:\/\/doi.org\/10.1186\/1471-2105-10-255","relation":{},"ISSN":["1471-2105"],"issn-type":[{"value":"1471-2105","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,8,20]]},"assertion":[{"value":"27 January 2009","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 August 2009","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 August 2009","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"255"}}