{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,20]],"date-time":"2026-09-20T12:30:52Z","timestamp":1789907452949,"version":"4.0.1"},"reference-count":60,"publisher":"Public Library of Science (PLoS)","issue":"2","license":[{"start":{"date-parts":[[2017,2,13]],"date-time":"2017-02-13T00:00:00Z","timestamp":1486944000000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["46651"],"award-info":[{"award-number":["46651"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0171905","type":"journal-article","created":{"date-parts":[[2017,2,13]],"date-time":"2017-02-13T19:48:44Z","timestamp":1487015324000},"page":"e0171905","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":22,"title":["Matrix Metalloproteinases are required for membrane motility and lumenogenesis during Drosophila heart development"],"prefix":"10.1371","volume":"12","author":[{"given":"Qanber S.","family":"Raza","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3404-2797","authenticated-orcid":true,"given":"Jessica L.","family":"Vanderploeg","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5878-5416","authenticated-orcid":true,"given":"J. Roger","family":"Jacobs","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2017,2,13]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1146\/annurev.cellbio.17.1.463","article-title":"How matrix metalloproteinases regulate cell behavior","volume":"17","author":"MD Sternlicht","year":"2001","journal-title":"Annual review of cell and developmental biology"},{"issue":"2","key":"ref2","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1093\/cvr\/cvs141","article-title":"Wnt signalling in smooth muscle cells and its role in cardiovascular disorders","volume":"95","author":"C Mill","year":"2012","journal-title":"Cardiovascular research"},{"issue":"1","key":"ref3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/bdrc.20065","article-title":"Matrix metalloproteinases in development and disease","volume":"78","author":"V Lemaitre","year":"2006","journal-title":"Birth defects research Part C, Embryo today: reviews"},{"issue":"4","key":"ref4","doi-asserted-by":"crossref","first-page":"681","DOI":"10.1083\/jcb.200409115","article-title":"Processing of VEGF-A by matrix metalloproteinases regulates bioavailability and vascular patterning in tumors","volume":"169","author":"S Lee","year":"2005","journal-title":"The Journal of cell biology"},{"issue":"3","key":"ref5","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1038\/nrm2125","article-title":"Matrix metalloproteinases and the regulation of tissue remodelling","volume":"8","author":"A Page-McCaw","year":"2007","journal-title":"Nature reviews Molecular cell biology"},{"issue":"3","key":"ref6","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1016\/j.cardiores.2005.12.002","article-title":"Structure and function of matrix metalloproteinases and TIMPs","volume":"69","author":"H Nagase","year":"2006","journal-title":"Cardiovascular research"},{"issue":"3","key":"ref7","doi-asserted-by":"crossref","first-page":"161","DOI":"10.1038\/nrc745","article-title":"New functions for the matrix metalloproteinases in cancer progression","volume":"2","author":"M Egeblad","year":"2002","journal-title":"Nature reviews Cancer"},{"issue":"46","key":"ref8","doi-asserted-by":"crossref","first-page":"35978","DOI":"10.1074\/jbc.M006045200","article-title":"Dm1-MMP, a matrix metalloproteinase from Drosophila with a potential role in extracellular matrix remodeling during neural development","volume":"275","author":"E Llano","year":"2000","journal-title":"The Journal of biological chemistry"},{"issue":"26","key":"ref9","doi-asserted-by":"crossref","first-page":"23321","DOI":"10.1074\/jbc.M200121200","article-title":"Structural and enzymatic characterization of Drosophila Dm2-MMP, a membrane-bound matrix metalloproteinase with tissue-specific expression","volume":"277","author":"E Llano","year":"2002","journal-title":"The Journal of biological chemistry"},{"issue":"42","key":"ref10","doi-asserted-by":"crossref","first-page":"12200","DOI":"10.1021\/bi035358x","article-title":"Drosophila TIMP is a potent inhibitor of MMPs and TACE: similarities in structure and function to TIMP-3","volume":"42","author":"S Wei","year":"2003","journal-title":"Biochemistry"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/B978-0-12-386041-5.00003-0","article-title":"Molecular basis for endothelial lumen formation and tubulogenesis during vasculogenesis and angiogenic sprouting","volume":"288","author":"GE Davis","year":"2011","journal-title":"International review of cell and molecular biology"},{"issue":"12","key":"ref12","doi-asserted-by":"crossref","first-page":"786","DOI":"10.1038\/nrm3904","article-title":"Remodelling the extracellular matrix in development and disease","volume":"15","author":"C Bonnans","year":"2014","journal-title":"Nature reviews Molecular cell biology"},{"key":"ref13","doi-asserted-by":"crossref","first-page":"4","DOI":"10.3389\/fcell.2015.00004","article-title":"The regulation of MMP targeting to invadopodia during cancer metastasis","volume":"3","author":"A Jacob","year":"2015","journal-title":"Frontiers in cell and developmental biology"},{"issue":"Pt 17","key":"ref14","doi-asserted-by":"crossref","first-page":"3015","DOI":"10.1242\/jcs.034561","article-title":"Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia","volume":"122","author":"R Poincloux","year":"2009","journal-title":"Journal of cell science"},{"issue":"9","key":"ref15","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1038\/nri3499","article-title":"Metalloproteinases and their natural inhibitors in inflammation and immunity","volume":"13","author":"R Khokha","year":"2013","journal-title":"Nature reviews Immunology"},{"issue":"9","key":"ref16","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1038\/nrc884","article-title":"Strategies for MMP inhibition in cancer: innovations for the post-trial era","volume":"2","author":"CM Overall","year":"2002","journal-title":"Nature reviews Cancer"},{"issue":"1","key":"ref17","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/S1534-5807(02)00400-8","article-title":"Drosophila matrix metalloproteinases are required for tissue remodeling, but not embryonic development","volume":"4","author":"A Page-McCaw","year":"2003","journal-title":"Developmental cell"},{"issue":"1","key":"ref18","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1242\/dev.011072","article-title":"Matrix metalloproteinases promote motor axon fasciculation in the Drosophila embryo","volume":"135","author":"CM Miller","year":"2008","journal-title":"Development"},{"issue":"14","key":"ref19","doi-asserted-by":"crossref","first-page":"5335","DOI":"10.1523\/JNEUROSCI.4811-10.2011","article-title":"Drosophila MMP2 regulates the matrix molecule faulty attraction (Frac) to promote motor axon targeting in Drosophila","volume":"31","author":"CM Miller","year":"2011","journal-title":"The Journal of neuroscience: the official journal of the Society for Neuroscience"},{"issue":"2","key":"ref20","doi-asserted-by":"crossref","first-page":"168","DOI":"10.1002\/(SICI)1097-0185(20000601)259:2<168::AID-AR7>3.0.CO;2-U","article-title":"MMP-2 expression during early avian cardiac and neural crest morphogenesis","volume":"259","author":"DH Cai","year":"2000","journal-title":"The Anatomical record"},{"issue":"4","key":"ref21","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1002\/dvdy.20171","article-title":"Tissue inhibitor of metalloproteinase-2 (TIMP-2) expression during cardiac neural crest cell migration and its role in proMMP-2 activation","volume":"231","author":"V Cantemir","year":"2004","journal-title":"Developmental dynamics: an official publication of the American Association of Anatomists"},{"issue":"3","key":"ref22","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1002\/dvdy.20377","article-title":"Cardiac morphogenesis: matrix metalloproteinase coordination of cellular mechanisms underlying heart tube formation and directionality of looping","volume":"233","author":"KK Linask","year":"2005","journal-title":"Developmental dynamics: an official publication of the American Association of Anatomists"},{"issue":"3","key":"ref23","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1002\/(SICI)1097-0177(199707)209:3<261::AID-AJA2>3.0.CO;2-G","article-title":"Spatial and temporal expression of the 72-kDa type IV collagenase (MMP-2) correlates with development and differentiation of valves in the embryonic avian heart","volume":"209","author":"SM Alexander","year":"1997","journal-title":"Developmental dynamics: an official publication of the American Association of Anatomists"},{"issue":"3","key":"ref24","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1002\/(SICI)1520-6408(1998)22:3<181::AID-DVG1>3.0.CO;2-2","article-title":"Heart development in Drosophila and vertebrates: conservation of molecular mechanisms","volume":"22","author":"R Bodmer","year":"1998","journal-title":"Developmental genetics"},{"issue":"1","key":"ref25","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.gene.2004.07.018","article-title":"Drosophila, an emerging model for cardiac disease","volume":"342","author":"E Bier","year":"2004","journal-title":"Gene"},{"issue":"1","key":"ref26","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.semcdb.2006.12.001","article-title":"Heart development in Drosophila","volume":"18","author":"Y Tao","year":"2007","journal-title":"Seminars in cell & developmental biology"},{"issue":"2","key":"ref27","doi-asserted-by":"crossref","first-page":"609","DOI":"10.1006\/dbio.1995.1173","article-title":"Laminin is required for heart, somatic muscles, and gut development in the Drosophila embryo","volume":"169","author":"T Yarnitzky","year":"1995","journal-title":"Developmental biology"},{"issue":"1","key":"ref28","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1006\/dbio.1998.9188","article-title":"The role of cell adhesion molecules in Drosophila heart morphogenesis: faint sausage, shotgun\/DE-cadherin, and laminin A are required for discrete stages in heart development","volume":"208","author":"TA Haag","year":"1999","journal-title":"Developmental biology"},{"issue":"13","key":"ref29","doi-asserted-by":"crossref","first-page":"3241","DOI":"10.1242\/dev.129.13.3241","article-title":"Pericardin, a Drosophila type IV collagen-like protein is involved in the morphogenesis and maintenance of the heart epithelium during dorsal ectoderm closure","volume":"129","author":"A Chartier","year":"2002","journal-title":"Development"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"7535","DOI":"10.1038\/srep07535","article-title":"Mmp1 and Mmp2 cooperatively induce Drosophila fat body cell dissociation with distinct roles","volume":"4","author":"Q Jia","year":"2014","journal-title":"Scientific reports"},{"issue":"2","key":"ref31","doi-asserted-by":"crossref","first-page":"e1004989","DOI":"10.1371\/journal.pgen.1004989","article-title":"Matrix metalloproteinase 2 is required for ovulation and corpus luteum formation in Drosophila","volume":"11","author":"LD Deady","year":"2015","journal-title":"PLoS genetics"},{"issue":"6","key":"ref32","doi-asserted-by":"crossref","first-page":"1068","DOI":"10.1091\/mbc.E11-09-0745","article-title":"A secreted MMP is required for reepithelialization during wound healing","volume":"23","author":"LJ Stevens","year":"2012","journal-title":"Mol Biol Cell"},{"issue":"2","key":"ref33","doi-asserted-by":"crossref","first-page":"772","DOI":"10.1016\/j.ydbio.2010.05.504","article-title":"A matrix metalloproteinase mediates airway remodeling in Drosophila","volume":"344","author":"BM Glasheen","year":"2010","journal-title":"Developmental biology"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1186\/1471-213X-12-8","article-title":"Integrins are required for cardioblast polarisation in Drosophila","volume":"12","author":"J Vanderploeg","year":"2012","journal-title":"BMC developmental biology"},{"issue":"2","key":"ref35","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1083\/jcb.200801100","article-title":"Genetic control of cell morphogenesis during Drosophila melanogaster cardiac tube formation","volume":"182","author":"C Medioni","year":"2008","journal-title":"The Journal of cell biology"},{"issue":"2","key":"ref36","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1083\/jcb.200804120","article-title":"Repulsion by Slit and Roundabout prevents Shotgun\/E-cadherin-mediated cell adhesion during Drosophila heart tube lumen formation","volume":"182","author":"E Santiago-Martinez","year":"2008","journal-title":"The Journal of cell biology"},{"issue":"1","key":"ref37","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1016\/j.ydbio.2006.01.027","article-title":"Slit coordinates cardiac morphogenesis in Drosophila","volume":"293","author":"A MacMullin","year":"2006","journal-title":"Developmental biology"},{"issue":"12","key":"ref38","doi-asserted-by":"crossref","first-page":"4281","DOI":"10.1523\/JNEUROSCI.21-12-04281.2001","article-title":"Diversity and specificity of actions of Slit2 proteolytic fragments in axon guidance","volume":"21","author":"KT Nguyen Ba-Charvet","year":"2001","journal-title":"The Journal of neuroscience: the official journal of the Society for Neuroscience"},{"issue":"6","key":"ref39","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1016\/S0092-8674(00)80588-7","article-title":"Biochemical purification of a mammalian slit protein as a positive regulator of sensory axon elongation and branching","volume":"96","author":"KH Wang","year":"1999","journal-title":"Cell"},{"issue":"10","key":"ref40","doi-asserted-by":"crossref","first-page":"589","DOI":"10.1080\/15216540600962818","article-title":"MT1-MMP: a key regulator of cell migration in tissue","volume":"58","author":"Y Itoh","year":"2006","journal-title":"IUBMB life"},{"issue":"42","key":"ref41","doi-asserted-by":"crossref","first-page":"40764","DOI":"10.1074\/jbc.M306736200","article-title":"Cleavage of syndecan-1 by membrane type matrix metalloproteinase-1 stimulates cell migration","volume":"278","author":"K Endo","year":"2003","journal-title":"The Journal of biological chemistry"},{"issue":"5","key":"ref42","doi-asserted-by":"crossref","first-page":"893","DOI":"10.1083\/jcb.153.5.893","article-title":"Membrane-type 1 matrix metalloproteinase cleaves CD44 and promotes cell migration","volume":"153","author":"M Kajita","year":"2001","journal-title":"The Journal of cell biology"},{"key":"ref43","article-title":"Guidance signalling regulates Leading Edge behaviour during collective cell migration of cardiac cells in Drosophila","author":"Q Raza","year":"2016","journal-title":"Developmental biology"},{"issue":"2","key":"ref44","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.ydbio.2014.08.033","article-title":"Drosophila heart cell movement to the midline occurs through both cell autonomous migration and dorsal closure","volume":"396","author":"T Haack","year":"2014","journal-title":"Developmental biology"},{"issue":"7","key":"ref45","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1078\/0171-9335-00072","article-title":"Inflated wings, tissue autolysis and early death in tissue inhibitor of metalloproteinases mutants of Drosophila","volume":"79","author":"TA Godenschwege","year":"2000","journal-title":"European journal of cell biology"},{"issue":"2","key":"ref46","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/S0925-4773(02)00016-3","article-title":"Expression of tissue inhibitor of metalloproteinases (TIMPs) during early cardiac development","volume":"113","author":"PR Brauer","year":"2002","journal-title":"Mechanisms of development"},{"issue":"24","key":"ref47","doi-asserted-by":"crossref","first-page":"4165","DOI":"10.1242\/dev.044263","article-title":"Drosophila laminins act as key regulators of basement membrane assembly and morphogenesis","volume":"136","author":"JM Urbano","year":"2009","journal-title":"Development"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1186\/1471-213X-14-26","article-title":"Distinct functions of the laminin beta LN domain and collagen IV during cardiac extracellular matrix formation and stabilization of alary muscle attachments revealed by EMS mutagenesis in Drosophila","volume":"14","author":"D Hollfelder","year":"2014","journal-title":"BMC developmental biology"},{"issue":"5","key":"ref49","doi-asserted-by":"crossref","first-page":"e1003086","DOI":"10.1371\/journal.pcbi.1003086","article-title":"Critical role of transient activity of MT1-MMP for ECM degradation in invadopodia","volume":"9","author":"A Watanabe","year":"2013","journal-title":"PLoS computational biology"},{"issue":"1","key":"ref50","doi-asserted-by":"crossref","first-page":"157","DOI":"10.1016\/j.devcel.2009.11.004","article-title":"Spatial restriction of FGF signaling by a matrix metalloprotease controls branching morphogenesis","volume":"18","author":"Q Wang","year":"2010","journal-title":"Developmental cell"},{"key":"ref51","article-title":"Talin is required to position and expand the luminal domain of the Drosophila heart tube","author":"J Vanderploeg","year":"2015","journal-title":"Developmental biology"},{"issue":"7","key":"ref52","doi-asserted-by":"crossref","first-page":"909","DOI":"10.1083\/jcb.201405075","article-title":"Cdc42 and formin activity control non-muscle myosin dynamics during Drosophila heart morphogenesis","volume":"206","author":"G Vogler","year":"2014","journal-title":"The Journal of cell biology"},{"issue":"5","key":"ref53","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1016\/j.sbi.2012.07.003","article-title":"Syndecan and integrin interactomes: large complexes in small spaces","volume":"22","author":"JA Roper","year":"2012","journal-title":"Current opinion in structural biology"},{"issue":"10","key":"ref54","doi-asserted-by":"crossref","first-page":"2320","DOI":"10.1111\/febs.12174","article-title":"Mapping of matrix metalloproteinase cleavage sites on syndecan-1 and syndecan-4 ectodomains","volume":"280","author":"T Manon-Jensen","year":"2013","journal-title":"The FEBS journal"},{"issue":"2","key":"ref55","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1016\/j.ydbio.2011.04.006","article-title":"Syndecan contributes to heart cell specification and lumen formation during Drosophila cardiogenesis","volume":"356","author":"J Knox","year":"2011","journal-title":"Developmental biology"},{"issue":"4","key":"ref56","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1242\/dev.014001","article-title":"Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure","volume":"135","author":"TH Millard","year":"2008","journal-title":"Development"},{"issue":"2","key":"ref57","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1006\/dbio.1995.1243","article-title":"Evidence for engrailed-independent wingless autoregulation in Drosophila","volume":"170","author":"KB Yoffe","year":"1995","journal-title":"Developmental biology"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1016\/S0091-679X(08)60927-9","article-title":"Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes","volume":"44","author":"NH Patel","year":"1994","journal-title":"Methods in cell biology"},{"issue":"25","key":"ref59","article-title":"The preparation of Drosophila embryos for live-imaging using the hanging drop protocol","author":"BH Reed","year":"2009","journal-title":"Journal of visualized experiments: JoVE"},{"issue":"2","key":"ref60","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1038\/nmeth.2811","article-title":"BoxPlotR: a web tool for generation of box plots","volume":"11","author":"M Spitzer","year":"2014","journal-title":"Nature methods"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0171905","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,24]],"date-time":"2022-07-24T02:38:39Z","timestamp":1658630319000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0171905"}},"subtitle":[],"editor":[{"given":"Juan-Pablo","family":"Labrador","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2017,2,13]]},"references-count":60,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2017,2,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0171905","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,2,13]]}}}