{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T08:27:34Z","timestamp":1772180854867,"version":"3.50.1"},"reference-count":35,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2019,4,8]],"date-time":"2019-04-08T00:00:00Z","timestamp":1554681600000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Hong Kong Research Grants Council","award":["C1007-15G"],"award-info":[{"award-number":["C1007-15G"]}]},{"DOI":"10.13039\/100007567","name":"City University of Hong Kong","doi-asserted-by":"publisher","award":["9610034"],"award-info":[{"award-number":["9610034"]}],"id":[{"id":"10.13039\/100007567","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Bioinformatics"],"published-print":{"date-parts":[[2019,12]]},"DOI":"10.1186\/s12859-019-2720-x","type":"journal-article","created":{"date-parts":[[2019,4,8]],"date-time":"2019-04-08T14:03:47Z","timestamp":1554732227000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":20,"title":["3DMMS: robust 3D Membrane Morphological Segmentation of C. elegans embryo"],"prefix":"10.1186","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-7323-8875","authenticated-orcid":false,"given":"Jianfeng","family":"Cao","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ming-Kin","family":"Wong","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhongying","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hong","family":"Yan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2019,4,8]]},"reference":[{"issue":"5","key":"2720_CR1","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1109\/MSP.2012.2204190","volume":"29","author":"E Meijering","year":"2012","unstructured":"Meijering E. Cell segmentation: 50 years down the road. IEEE Signal Proc Mag. 2012; 29(5):140\u20135.","journal-title":"IEEE Signal Proc Mag"},{"issue":"11","key":"2720_CR2","first-page":"1","volume":"98","author":"L Cheng","year":"2018","unstructured":"Cheng L, Romobucheli D, Wang X, Janowczyk A, Ganesan S, Gilmore H, Rimm D, Madabhushi A. Nuclear shape and orientation features from h&e images predict survival in early-stage estrogen receptor-positive breast cancers. Lab Investi. 2018; 98(11):1.","journal-title":"Lab Investi"},{"issue":"6","key":"2720_CR3","first-page":"296","volume":"34","author":"C Lu","year":"2012","unstructured":"Lu C, Mahmood M, Jha N, Mandal M. A robust automatic nuclei segmentation technique for quantitative histopathological image analysis. Anal Quant Cytol Histol. 2012; 34(6):296.","journal-title":"Anal Quant Cytol Histol"},{"key":"2720_CR4","doi-asserted-by":"publisher","unstructured":"Oscanoa J, Doimi F, Dyer R, Araujo J, Pinto J, Castaneda B. Automated segmentation and classification of cell nuclei in immunohistochemical breast cancer images with estrogen receptor marker. In: 2016 38th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC): 2016. p. 2399\u2013402. ISSN 1558-4615 \n                    https:\/\/doi.org\/10.1109\/EMBC.2016.7591213\n                    \n                  .","DOI":"10.1109\/EMBC.2016.7591213"},{"key":"2720_CR5","doi-asserted-by":"publisher","first-page":"276","DOI":"10.12688\/f1000research.10680.1","volume":"6","author":"V Tang","year":"2017","unstructured":"Tang V. Cell-cell adhesion interface: rise of the lateral membrane. F1000research. 2017; 6:276.","journal-title":"F1000research"},{"issue":"4","key":"2720_CR6","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1006\/cbir.2002.0857","volume":"26","author":"WH Goldmann","year":"2002","unstructured":"Goldmann WH. Mechanical aspects of cell shape regulation and signaling. Cell Biol Int. 2002; 26(4):313\u20137.","journal-title":"Cell Biol Int"},{"issue":"1","key":"2720_CR7","doi-asserted-by":"publisher","first-page":"84","DOI":"10.1016\/j.yexcr.2004.08.017","volume":"301","author":"M Ding","year":"2004","unstructured":"Ding M, Woo WM, Chisholm AD. The cytoskeleton and epidermal morphogenesis in c. elegans. Exp Cell Res. 2004; 301(1):84\u201390.","journal-title":"Exp Cell Res"},{"issue":"32","key":"2720_CR8","doi-asserted-by":"publisher","first-page":"4620","DOI":"10.1073\/pnas.1512156113","volume":"113","author":"DZ Bar","year":"2016","unstructured":"Bar DZ, Charar C, Dorfman J, Yadid T, Tafforeau L, Lafontaine DL, Gruenbaum Y. Cell size and fat content of dietary-restricted caenorhabditis elegans are regulated by atx-2, an mtor repressor. Proc Natl Acad Sci U S A. 2016; 113(32):4620.","journal-title":"Proc Natl Acad Sci U S A"},{"key":"2720_CR9","doi-asserted-by":"publisher","unstructured":"Shan EAR, Cheung L, Epstein D, Pelengaris S, Rajpoot NM. Mimo-net: A multi-input multi-output convolutional neural network for cell segmentation in fluorescence microscopy images. In: 2017 IEEE 14th International Symposium on Biomedical Imaging (ISBI 2017): 2017. p. 337\u2013340. ISSN 1945-8452 \n                    https:\/\/doi.org\/10.1109\/ISBI.2017.7950532\n                    \n                  .","DOI":"10.1109\/ISBI.2017.7950532"},{"issue":"2","key":"2720_CR10","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1083\/jcb.200209006","volume":"160","author":"Katarina Wolf","year":"2003","unstructured":"Wolf K, Mazo I, Leung H, Engelke K, von Andrian UH, Deryugina EI, Strongin AY, Br\u00f6cker E-B, Friedl P. Compensation mechanism in tumor cell migration. J Cell Biol. 2003; 160(2):267\u2013277. \n                    https:\/\/doi.org\/10.1083\/jcb.200209006\n                    \n                  . \n                    http:\/\/jcb.rupress.org\/content\/160\/2\/267.full.pdf\n                    \n                  .","journal-title":"The Journal of Cell Biology"},{"issue":"1","key":"2720_CR11","doi-asserted-by":"publisher","first-page":"19","DOI":"10.1111\/j.1462-5822.2004.00426.x","volume":"7","author":"E Coudrier","year":"2010","unstructured":"Coudrier E, Amblard F, Zimmer C, Roux P, Olivo-Marin JC, Rigothier MC, Guill\u00e9n N. Myosin ii and the gal-galnac lectin play a crucial role in tissue invasion by entamoeba histolytica. Cell Microbiol. 2010; 7(1):19\u201327.","journal-title":"Cell Microbiol"},{"issue":"9","key":"2720_CR12","doi-asserted-by":"publisher","first-page":"1396","DOI":"10.1109\/TIP.2005.852790","volume":"14","author":"D Alexandre","year":"2005","unstructured":"Alexandre D, Vasily S, Shahragim T, Nancy GA, Jean-Christophe OM, Christophe Z. Segmenting and tracking fluorescent cells in dynamic 3-d microscopy with coupled active surfaces. IEEE Trans Image Process. 2005; 14(9):1396\u2013410.","journal-title":"IEEE Trans Image Process"},{"issue":"5","key":"2720_CR13","doi-asserted-by":"publisher","first-page":"1006077","DOI":"10.1371\/journal.pgen.1006077","volume":"12","author":"A Asan","year":"2016","unstructured":"Asan A, Raiders SA, Priess JR. Morphogenesis of the c. elegans intestine involves axon guidance genes. Plos Genet. 2016; 12(5):1006077.","journal-title":"Plos Genet"},{"issue":"6","key":"2720_CR14","doi-asserted-by":"publisher","first-page":"1356","DOI":"10.1016\/j.cell.2013.08.026","volume":"154","author":"P Rangamani","year":"2013","unstructured":"Rangamani P, Lipshtat A, Azeloglu E, Calizo RC, Hu M, Ghassemi S, Hone J, Scarlata S, Neves S, Iyengar R. Decoding information in cell shape. Cell. 2013; 154(6):1356\u201369.","journal-title":"Cell"},{"issue":"6","key":"2720_CR15","doi-asserted-by":"publisher","first-page":"1132","DOI":"10.1016\/j.cell.2014.02.007","volume":"156","author":"M Schmick","year":"2014","unstructured":"Schmick M, Bastiaens PH. The interdependence of membrane shape and cellular signal processing. Cell. 2014; 156(6):1132\u20138.","journal-title":"Cell"},{"key":"2720_CR16","doi-asserted-by":"publisher","unstructured":"Genome sequence of the nematode c. elegans: A platform for investigating biology. Science. 1998; 282(5396):2012\u20138. \n                    https:\/\/doi.org\/10.1126\/science.282.5396.2012\n                    \n                  . \n                    http:\/\/science.sciencemag.org\/content\/282\/5396\/2012.full.pdf\n                    \n                  .","DOI":"10.1126\/science.282.5396.2012"},{"issue":"1","key":"2720_CR17","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1016\/0012-1606(83)90201-4","volume":"100","author":"JE Sulston","year":"1983","unstructured":"Sulston JE, Schierenberg E, White JG, Thomson JN. The embryonic cell lineage of the nematode caenorhabditis elegans. Dev Biol. 1983; 100(1):64\u2013119.","journal-title":"Dev Biol"},{"issue":"4","key":"2720_CR18","doi-asserted-by":"publisher","first-page":"182","DOI":"10.1002\/dvg.22928","volume":"54","author":"AL Zacharias","year":"2016","unstructured":"Zacharias AL, Murray JI. Combinatorial decoding of the invariant c. elegans embryonic lineage in space and time. Genesis. 2016; 54(4):182\u201397.","journal-title":"Genesis"},{"key":"2720_CR19","doi-asserted-by":"publisher","first-page":"251","DOI":"10.1007\/978-3-642-59828-9_16","volume-title":"Development","author":"Michael Krause","year":"1999","unstructured":"Krause M. In: Russo Vincenzo EA, Cove David J, Edgar Lois G, Jaenisch R, Salamini F, (eds).Cell Fate Determination in Caenorhabditis Elegans. Berlin: Springer Berlin Heidelberg; 1999, pp. 251\u2013267. isbn 978-3-642-59828-9. \n                    https:\/\/doi.org\/10.1007\/978-3-642-59828-9_16\n                    \n                  ."},{"issue":"2","key":"2720_CR20","doi-asserted-by":"publisher","first-page":"225","DOI":"10.1016\/j.devcel.2015.12.028","volume":"36","author":"J Stegmaier","year":"2016","unstructured":"Stegmaier J, Amat F, Lemon W, Mcdole K, Wan Y, Teodoro G, Mikut R, Keller PJ. Real-time three-dimensional cell segmentation in large-scale microscopy data of developing embryos. Dev Cell. 2016; 36(2):225\u201340.","journal-title":"Dev Cell"},{"issue":"1","key":"2720_CR21","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1186\/s12859-017-1717-6","volume":"18","author":"Y Azuma","year":"2017","unstructured":"Azuma Y, Onami S. Biologically constrained optimization based cell membrane segmentation in c. elegans embryos. Bmc Bioinformatics. 2017; 18(1):307.","journal-title":"Bmc Bioinformatics"},{"key":"2720_CR22","unstructured":"Source Code of 3DMMS. \n                    https:\/\/github.com\/cao13jf\/3DMMS_public\n                    \n                  . Accessed 15 Feb 2019."},{"key":"2720_CR23","doi-asserted-by":"publisher","unstructured":"Yushkevich PA, Gao Y, Gerig G. Itk-snap: An interactive tool for semi-automatic segmentation of multi-modality biomedical images. In: 2016 38th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC): 2016. p. 3342\u20135. ISSN 1558-4615 \n                    https:\/\/doi.org\/10.1109\/EMBC.2016.7591443\n                    \n                  .","DOI":"10.1109\/EMBC.2016.7591443"},{"issue":"1","key":"2720_CR24","doi-asserted-by":"publisher","first-page":"275","DOI":"10.1186\/1471-2105-7-275","volume":"7","author":"TJ Boyle","year":"2006","unstructured":"Boyle TJ, Bao Z, Murray JI, Araya CL, Waterston RH. Acetree: a tool for visual analysis of caenorhabditis elegans embryogenesis. BMC Bioinformatics. 2006; 7(1):275.","journal-title":"BMC Bioinformatics"},{"issue":"1","key":"2720_CR25","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1534\/genetics.116.197160","volume":"205","author":"O Cohen-Fix","year":"2017","unstructured":"Cohen-Fix O, Askjaer P. Cell biology of the caenorhabditis elegans nucleus. Genetics. 2017; 205(1):25\u201359.","journal-title":"Genetics"},{"issue":"9","key":"2720_CR26","doi-asserted-by":"publisher","first-page":"1487","DOI":"10.1038\/sj.leu.2404296","volume":"20","author":"J Ratajczak","year":"2006","unstructured":"Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, Ratajczak MZ. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia. 2006; 20(9):1487\u201395.","journal-title":"Leukemia"},{"issue":"9","key":"2720_CR27","doi-asserted-by":"publisher","first-page":"951","DOI":"10.1038\/nmeth.3036","volume":"11","author":"F Amat","year":"2014","unstructured":"Amat F, Lemon W, Mossing DP, Mcdole K, Wan Y, Branson K, Myers EW, Keller PJ. Fast, accurate reconstruction of cell lineages from large-scale fluorescence microscopy data. Nat Methods. 2014; 11(9):951\u20138.","journal-title":"Nat Methods"},{"key":"2720_CR28","doi-asserted-by":"publisher","unstructured":"Wolff C, Tinevez JY, Pietzsch T, Stamataki E, Harich B, Guignard L, Preibisch S, Shorte S, Keller PJ, Tomancak P. Multi-view light-sheet imaging and tracking with the mamut software reveals the cell lineage of a direct developing arthropod limb. Elife. 2018; 7:e34410. editor: S\u013a\u0107nchez Alvarado, A,issn 2050-084X, eLife Sciences Publications, Ltd. \n                    https:\/\/doi.org\/10.7554\/eLife.34410\n                    \n                  .","DOI":"10.7554\/eLife.34410"},{"key":"2720_CR29","doi-asserted-by":"publisher","unstructured":"Kalinin AA, Allyn-Feuer A, Ade A, Fon G-V, Meixner W, Dilworth D, Husain SS, de Wet JR, Higgins GA, Zheng G, Creekmore A, Wiley JW, Verdone JE, Veltri RW, Pienta KJ, Coffey DS, Athey BD, Dinov ID. 3d shape modeling for cell nuclear morphological analysis and classification. Sci Rep. 2018; 8:16142. Provided by the SAO\/NASA Astrophysics Data System \n                    https:\/\/doi.org\/10.1038\/s41598-018-33574-w\n                    \n                  . \n                    http:\/\/adsabs.harvard.edu\/abs\/2018NatSR...816142K\n                    \n                  .","DOI":"10.1038\/s41598-018-33574-w"},{"issue":"1","key":"2720_CR30","doi-asserted-by":"publisher","first-page":"62","DOI":"10.1109\/TSMC.1979.4310076","volume":"9","author":"N Otsu","year":"1979","unstructured":"Otsu N. A threshold selection method from gray-level histograms. IEEE Trans Syst Man Cybern. 1979; 9(1):62\u20136.","journal-title":"IEEE Trans Syst Man Cybern"},{"issue":"1","key":"2720_CR31","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1109\/TITB.2007.898006","volume":"12","author":"P Yan","year":"2008","unstructured":"Yan P, Zhou X, Shah M, Wong STC. Automatic segmentation of high-throughput rnai fluorescent cellular images. IEEE Trans Inf Technol Biomed. 2008; 12(1):109\u201317.","journal-title":"IEEE Trans Inf Technol Biomed"},{"issue":"7","key":"2720_CR32","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1038\/nmeth.1472","volume":"7","author":"F Romain","year":"2010","unstructured":"Romain F, Pradeep D, Vincent M, Eric M, Jan T, Jean-Luc V, Gr\u00e9goire M, Christophe G. Imaging plant growth in 4d: robust tissue reconstruction and lineaging at cell resolution. Nat Methods. 2010; 7(7):547.","journal-title":"Nat Methods"},{"key":"2720_CR33","doi-asserted-by":"publisher","unstructured":"Cao J, Zhao Z, Yan H. Accurate cell segmentation based on biological morphology features. In: 2018 IEEE International Conference on Systems, Man, and Cybernetics (SMC): 2018. p. 3380\u20133. ISSN 2577-1655 \n                    https:\/\/doi.org\/10.1109\/SMC.2018.00572\n                    \n                  .","DOI":"10.1109\/SMC.2018.00572"},{"issue":"99","key":"2720_CR34","first-page":"1","volume":"PP","author":"A Tareef","year":"2018","unstructured":"Tareef A, Song Y, Huang H, Feng D, Chen M, Wang Y, Cai W. Multi-pass fast watershed for accurate segmentation of overlapping cervical cells. IEEE Trans Med Imaging. 2018; PP(99):1\u20131.","journal-title":"IEEE Trans Med Imaging"},{"key":"2720_CR35","unstructured":"Supplementary experiments. \n                    https:\/\/figshare.com\/s\/d932c564d5cdd7186679\n                    \n                  . Accessed 28 Feb 2019."}],"container-title":["BMC Bioinformatics"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12859-019-2720-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/s12859-019-2720-x\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/s12859-019-2720-x.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,4,6]],"date-time":"2020-04-06T23:08:21Z","timestamp":1586214501000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmcbioinformatics.biomedcentral.com\/articles\/10.1186\/s12859-019-2720-x"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,4,8]]},"references-count":35,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2019,12]]}},"alternative-id":["2720"],"URL":"https:\/\/doi.org\/10.1186\/s12859-019-2720-x","relation":{},"ISSN":["1471-2105"],"issn-type":[{"value":"1471-2105","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,4,8]]},"assertion":[{"value":"2 November 2018","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 March 2019","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 April 2019","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"Not applicable.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}},{"value":"Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Publisher\u2019s Note"}}],"article-number":"176"}}