{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,23]],"date-time":"2026-09-23T17:42:32Z","timestamp":1790185352892,"version":"4.1.0"},"reference-count":57,"publisher":"Elsevier BV","issue":"2","license":[{"start":{"date-parts":[[2015,8,1]],"date-time":"2015-08-01T00:00:00Z","timestamp":1438387200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.elsevier.com\/tdm\/userlicense\/1.0\/"},{"start":{"date-parts":[[2016,8,15]],"date-time":"2016-08-15T00:00:00Z","timestamp":1471219200000},"content-version":"vor","delay-in-days":380,"URL":"https:\/\/www.elsevier.com\/open-access\/userlicense\/1.0\/"}],"content-domain":{"domain":["elsevier.com","sciencedirect.com"],"crossmark-restriction":true},"short-container-title":["Developmental Biology"],"published-print":{"date-parts":[[2015,8]]},"DOI":"10.1016\/j.ydbio.2015.05.023","type":"journal-article","created":{"date-parts":[[2015,6,23]],"date-time":"2015-06-23T16:18:15Z","timestamp":1435076295000},"page":"88-102","update-policy":"https:\/\/doi.org\/10.1016\/elsevier_cm_policy","source":"Crossref","is-referenced-by-count":39,"title":["ROBO2 restricts the nephrogenic field and regulates Wolffian duct\u2013nephrogenic cord separation"],"prefix":"10.1016","volume":"404","author":[{"given":"Elanor N.","family":"Wainwright","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dagmar","family":"Wilhelm","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander N.","family":"Combes","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melissa H.","family":"Little","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter","family":"Koopman","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"78","reference":[{"key":"10.1016\/j.ydbio.2015.05.023_bib1","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1172\/JCI26027","article-title":"Tbx18 regulates the development of the ureteral mesenchyme","volume":"116","author":"Airik","year":"2006","journal-title":"J. Clin. Investig."},{"key":"10.1016\/j.ydbio.2015.05.023_bib2","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1016\/j.devcel.2012.04.018","article-title":"FGF9 and FGF20 maintain the stemness of nephron progenitors in mice and man","volume":"22","author":"Barak","year":"2012","journal-title":"Dev. Cell"},{"key":"10.1016\/j.ydbio.2015.05.023_bib3","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.ydbio.2013.04.036","article-title":"Tbx18 expression demarcates multipotent precursor populations in the developing urogenital system but is exclusively required within the ureteric mesenchymal lineage to suppress a renal stromal fate","volume":"380","author":"Bohnenpoll","year":"2013","journal-title":"Dev. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib4","doi-asserted-by":"crossref","first-page":"2958","DOI":"10.1101\/gad.240102","article-title":"Nephric lineage specification by Pax2 and Pax8","volume":"16","author":"Bouchard","year":"2002","journal-title":"Genes Dev."},{"key":"10.1016\/j.ydbio.2015.05.023_bib5","doi-asserted-by":"crossref","first-page":"1211","DOI":"10.1016\/j.mod.2004.05.019","article-title":"The transcription factor Six2 activates expression of the Gdnf gene as well as its own promoter","volume":"121","author":"Brodbeck","year":"2004","journal-title":"Mech. Dev."},{"key":"10.1016\/j.ydbio.2015.05.023_bib6","doi-asserted-by":"crossref","first-page":"199","DOI":"10.1016\/j.devcel.2009.07.013","article-title":"Ret-dependent cell rearrangements in the Wolffian duct epithelium initiate ureteric bud morphogenesis","volume":"17","author":"Chi","year":"2009","journal-title":"Dev. Cell"},{"key":"10.1016\/j.ydbio.2015.05.023_bib7","doi-asserted-by":"crossref","first-page":"693","DOI":"10.1002\/wdev.52","article-title":"Genetic controls and cellular behaviors in branching morphogenesis of the renal collecting system","volume":"1","author":"Costantini","year":"2012","journal-title":"Wiley Interdiscip. Rev. Dev. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib8","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1016\/j.celrep.2014.03.063","article-title":"Pkd1 regulates lymphatic vascular morphogenesis during development","volume":"7","author":"Coxam","year":"2014","journal-title":"Cell Rep."},{"key":"10.1016\/j.ydbio.2015.05.023_bib9","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.1038\/ncb2828","article-title":"Stromal-epithelial crosstalk regulates kidney progenitor cell differentiation","volume":"15","author":"Das","year":"2013","journal-title":"Nat. Cell Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib10","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1083\/jcb.200301041","article-title":"Dual function of Slit2 in repulsion and enhanced migration of trunk, but not vagal, neural crest cells","volume":"162","author":"De Bellard","year":"2003","journal-title":"J. Cell Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib11","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.devcel.2012.11.018","article-title":"Roundabout receptors are critical for foregut separation from the body wall","volume":"24","author":"Domyan","year":"2013","journal-title":"Dev. Cell"},{"key":"10.1016\/j.ydbio.2015.05.023_bib12","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1016\/S0896-6273(03)00591-9","article-title":"Slit stimulation recruits Dock and Pak to the roundabout receptor and increases Rac activity to regulate axon repulsion at the CNS midline","volume":"40","author":"Fan","year":"2003","journal-title":"Neuron"},{"key":"10.1016\/j.ydbio.2015.05.023_bib13","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1016\/j.devcel.2010.02.013","article-title":"Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis","volume":"18","author":"Gavet","year":"2010","journal-title":"Dev. Cell"},{"key":"10.1016\/j.ydbio.2015.05.023_bib14","doi-asserted-by":"crossref","first-page":"7661","DOI":"10.1128\/MCB.00465-07","article-title":"A Hox\u2013Eya\u2013Pax complex regulates early kidney developmental gene expression","volume":"27","author":"Gong","year":"2007","journal-title":"Mol. Cell. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib15","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1016\/S1534-5807(04)00108-X","article-title":"SLIT2-mediated ROBO2 signaling restricts kidney induction to a single site","volume":"6","author":"Grieshammer","year":"2004","journal-title":"Dev. Cell"},{"key":"10.1016\/j.ydbio.2015.05.023_bib16","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1242\/dev.02184","article-title":"Pax 2\/8-regulated Gata 3 expression is necessary for morphogenesis and guidance of the nephric duct in the developing kidney","volume":"133","author":"Grote","year":"2006","journal-title":"Development"},{"key":"10.1016\/j.ydbio.2015.05.023_bib17","series-title":"In situ Hybridization Protocols","first-page":"279","article-title":"In situ hybridization of whole mount embryos","author":"Hargrave","year":"1999"},{"key":"10.1016\/j.ydbio.2015.05.023_bib18","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/0925-4773(95)00464-5","article-title":"Embryonic expression of glial cell-line derived neurotrophic factor (GDNF) suggests multiple developmental roles in neural differentiation and epithelial\u2013mesenchymal interactions","volume":"54","author":"Hellmich","year":"1996","journal-title":"Mech. Dev."},{"key":"10.1016\/j.ydbio.2015.05.023_bib19","doi-asserted-by":"crossref","first-page":"288","DOI":"10.1016\/j.ajhg.2013.12.017","article-title":"Integrin alpha 8 recessive mutations are responsible for bilateral renal agenesis in humans","volume":"94","author":"Humbert","year":"2014","journal-title":"Am. J. Hum. Genet."},{"key":"10.1016\/j.ydbio.2015.05.023_bib20","doi-asserted-by":"crossref","first-page":"85","DOI":"10.2353\/ajpath.2010.090517","article-title":"Fate tracing reveals the pericyte and not epithelial origin of myofibroblasts in kidney fibrosis","volume":"176","author":"Humphreys","year":"2010","journal-title":"Am. J. Pathol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib21","doi-asserted-by":"crossref","first-page":"1325","DOI":"10.1038\/ncb1976","article-title":"Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity","volume":"11","author":"Jones","year":"2009","journal-title":"Nat. Cell Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib22","doi-asserted-by":"crossref","first-page":"2584","DOI":"10.1681\/ASN.2013080896","article-title":"Sall1 maintains nephron progenitors and nascent nephrons by acting as both an activator and a repressor","volume":"25","author":"Kanda","year":"2014","journal-title":"J. Am. Soc. Nephrol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib23","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/j.stem.2008.05.020","article-title":"Six2 defines and regulates a multipotent self-renewing nephron progenitor population throughout mammalian kidney development","volume":"3","author":"Kobayashi","year":"2008","journal-title":"Cell Stem Cell"},{"key":"10.1016\/j.ydbio.2015.05.023_bib24","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1126\/science.1058766","article-title":"Switching repulsion to attraction: changing responses to slit during transition in mesoderm migration","volume":"292","author":"Kramer","year":"2001","journal-title":"Science"},{"key":"10.1016\/j.ydbio.2015.05.023_bib25","doi-asserted-by":"crossref","first-page":"2501","DOI":"10.1242\/dev.005033","article-title":"The ECM protein nephronectin promotes kidney development via integrin alpha8beta1-mediated stimulation of Gdnf expression","volume":"134","author":"Linton","year":"2007","journal-title":"Development"},{"key":"10.1016\/j.ydbio.2015.05.023_bib26","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/S0070-2153(10)90005-7","article-title":"Kidney development: two tales of tubulogenesis","volume":"90","author":"Little","year":"2010","journal-title":"Curr. Top. Dev. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib27","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1016\/j.modgep.2007.03.002","article-title":"A high-resolution anatomical ontology of the developing murine genitourinary tract","volume":"7","author":"Little","year":"2007","journal-title":"Gene Expr. Patterns"},{"key":"10.1016\/j.ydbio.2015.05.023_bib28","doi-asserted-by":"crossref","first-page":"616","DOI":"10.1086\/512735","article-title":"Disruption of ROBO2 is associated with urinary tract anomalies and confers risk of vesicoureteral reflux","volume":"80","author":"Lu","year":"2007","journal-title":"Am. J. Hum. Genet."},{"key":"10.1016\/j.ydbio.2015.05.023_bib29","doi-asserted-by":"crossref","first-page":"2161","DOI":"10.1101\/gad.310204","article-title":"Vilse, a conserved Rac\/Cdc42 GAP mediating Robo repulsion in tracheal cells and axons","volume":"18","author":"Lundstrom","year":"2004","journal-title":"Genes Dev."},{"key":"10.1016\/j.ydbio.2015.05.023_bib30","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1016\/j.devcel.2011.05.012","article-title":"SLIT\/ROBO1 signaling suppresses mammary branching morphogenesis by limiting basal cell number","volume":"20","author":"Macias","year":"2011","journal-title":"Dev. Cell"},{"key":"10.1016\/j.ydbio.2015.05.023_bib31","doi-asserted-by":"crossref","first-page":"2397","DOI":"10.1242\/dev.02861","article-title":"Reduction of BMP4 activity by gremlin 1 enables ureteric bud outgrowth and GDNF\/WNT11 feedback signalling during kidney branching morphogenesis","volume":"134","author":"Michos","year":"2007","journal-title":"Development"},{"key":"10.1016\/j.ydbio.2015.05.023_bib32","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1038\/382076a0","article-title":"Renal and neuronal abnormalities in mice lacking GDNF","volume":"382","author":"Moore","year":"1996","journal-title":"Nature"},{"key":"10.1016\/j.ydbio.2015.05.023_bib33","doi-asserted-by":"crossref","DOI":"10.1128\/MCB.00491-14","article-title":"Role of Wnt5a-Ror2 signaling in morphogenesis of the metanephric mesenchyme during ureteric budding","author":"Nishita","year":"2014","journal-title":"Mol. Cell. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib34","doi-asserted-by":"crossref","first-page":"1005","DOI":"10.1242\/dev.119.4.1005","article-title":"Expression of the c-ret proto-oncogene during mouse embryogenesis","volume":"119","author":"Pachnis","year":"1993","journal-title":"Development"},{"key":"10.1016\/j.ydbio.2015.05.023_bib35","doi-asserted-by":"crossref","first-page":"2533","DOI":"10.1242\/dev.006155","article-title":"Wnt\/beta-catenin signaling regulates nephron induction during mouse kidney development","volume":"134","author":"Park","year":"2007","journal-title":"Development"},{"key":"10.1016\/j.ydbio.2015.05.023_bib36","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/S0012-1606(03)00258-6","article-title":"Robo4 is a vascular-specific receptor that inhibits endothelial migration","volume":"261","author":"Park","year":"2003","journal-title":"Dev. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib37","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1016\/j.ydbio.2005.09.027","article-title":"Lim 1 is required for nephric duct extension and ureteric bud morphogenesis","volume":"288","author":"Pedersen","year":"2005","journal-title":"Dev. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib38","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1101\/SQB.1996.061.01.047","article-title":"GDNF is required for kidney development and enteric innervation","volume":"61","author":"Pichel","year":"1996","journal-title":"Cold Spring Harb. Symp. Quant. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib39","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1016\/S0925-4773(00)00313-0","article-title":"Expression of the vertebrate Slit gene family and their putative receptors, the Robo genes, in the developing murine kidney","volume":"94","author":"Piper","year":"2000","journal-title":"Mech. Dev."},{"key":"10.1016\/j.ydbio.2015.05.023_bib40","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1002\/bies.10199","article-title":"Movement through Slits: cellular migration via the Slit family","volume":"25","author":"Piper","year":"2003","journal-title":"Bioessays"},{"key":"10.1016\/j.ydbio.2015.05.023_bib41","doi-asserted-by":"crossref","first-page":"506","DOI":"10.1093\/hmg\/ddp520","article-title":"Sox10 gain-of-function causes XX sex reversal in mice: implications for human 22q-linked disorders of sex development","volume":"19","author":"Polanco","year":"2010","journal-title":"Hum. Mol. Genet."},{"key":"10.1016\/j.ydbio.2015.05.023_bib42","doi-asserted-by":"crossref","first-page":"883","DOI":"10.1038\/ncb1614","article-title":"Cables links Robo-bound Abl kinase to N-cadherin-bound beta-catenin to mediate Slit-induced modulation of adhesion and transcription","volume":"9","author":"Rhee","year":"2007","journal-title":"Nat. Cell Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib43","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1016\/0092-8674(88)90249-8","article-title":"slit: an EGF-homologous locus of D. melanogaster involved in the development of the embryonic central nervous system","volume":"55","author":"Rothberg","year":"1988","journal-title":"Cell"},{"key":"10.1016\/j.ydbio.2015.05.023_bib44","doi-asserted-by":"crossref","first-page":"4077","DOI":"10.1242\/dev.124.20.4077","article-title":"Glial-cell-line-derived neurotrophic factor is required for bud initiation from ureteric epithelium","volume":"124","author":"Sainio","year":"1997","journal-title":"Development"},{"key":"10.1016\/j.ydbio.2015.05.023_bib45","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1038\/382070a0","article-title":"Renal agenesis and the absence of enteric neurons in mice lacking GDNF","volume":"382","author":"Sanchez","year":"1996","journal-title":"Nature"},{"key":"10.1016\/j.ydbio.2015.05.023_bib46","doi-asserted-by":"crossref","first-page":"791","DOI":"10.1038\/nrg2205","article-title":"Renal abnormalities and their developmental origin","volume":"8","author":"Schedl","year":"2007","journal-title":"Nat. Rev. Genet."},{"key":"10.1016\/j.ydbio.2015.05.023_bib47","doi-asserted-by":"crossref","first-page":"409","DOI":"10.1016\/0896-6273(93)90330-T","article-title":"Mutations affecting growth cone guidance in Drosophila: genes necessary for guidance toward or away from the midline","volume":"10","author":"Seeger","year":"1993","journal-title":"Neuron"},{"key":"10.1016\/j.ydbio.2015.05.023_bib48","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.ydbio.2005.04.008","article-title":"The role of GDNF in patterning the excretory system","volume":"283","author":"Shakya","year":"2005","journal-title":"Dev. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib49","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1016\/j.devcel.2014.02.017","article-title":"Global quantification of tissue dynamics in the developing mouse kidney","volume":"29","author":"Short","year":"2014","journal-title":"Dev. Cell"},{"key":"10.1016\/j.ydbio.2015.05.023_bib50","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1111\/j.1460-9568.1996.tb01267.x","article-title":"Localization of glial cell line-derived neurotrophic factor (GDNF) mRNA in embryonic rat by in situ hybridization","volume":"8","author":"Suvanto","year":"1996","journal-title":"Eur. J. Neurosci."},{"key":"10.1016\/j.ydbio.2015.05.023_bib51","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1159\/000228720","article-title":"Identification of suitable normalizing genes for quantitative real-time RT-PCR analysis of gene expression in fetal mouse gonads","volume":"3","author":"Svingen","year":"2009","journal-title":"Sex Dev."},{"key":"10.1016\/j.ydbio.2015.05.023_bib52","doi-asserted-by":"crossref","first-page":"1337","DOI":"10.1083\/jcb.142.5.1337","article-title":"The RET-glial cell-derived neurotrophic factor (GDNF) pathway stimulates migration and chemoattraction of epithelial cells","volume":"142","author":"Tang","year":"1998","journal-title":"J. Cell Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib53","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1016\/j.ydbio.2014.08.037","article-title":"Primary cilia function regulates the length of the embryonic trunk axis and urogenital field in mice","volume":"395","author":"Wainwright","year":"2014","journal-title":"Dev. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib54","doi-asserted-by":"crossref","first-page":"10553","DOI":"10.1074\/jbc.M609578200","article-title":"SOX9 regulates prostaglandin D synthase gene transcription in vivo to ensure testis development","volume":"282","author":"Wilhelm","year":"2007","journal-title":"J. Biol. Chem."},{"key":"10.1016\/j.ydbio.2015.05.023_bib55","doi-asserted-by":"crossref","first-page":"1211","DOI":"10.1242\/dev.126.6.1211","article-title":"A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo","volume":"126","author":"Yamaguchi","year":"1999","journal-title":"Development"},{"key":"10.1016\/j.ydbio.2015.05.023_bib56","doi-asserted-by":"crossref","first-page":"503","DOI":"10.1006\/dbio.2000.0100","article-title":"GDNF is a chemoattractant for enteric neural cells","volume":"229","author":"Young","year":"2001","journal-title":"Dev. Biol."},{"key":"10.1016\/j.ydbio.2015.05.023_bib57","doi-asserted-by":"crossref","first-page":"6807","DOI":"10.1093\/hmg\/ddu397","article-title":"Non-canonical Wnt5a\/Ror2 signaling regulates kidney morphogenesis by controlling intermediate mesoderm extension","volume":"23","author":"Yun","year":"2014","journal-title":"Hum. Mol. Genet."}],"container-title":["Developmental Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0012160615300063?httpAccept=text\/plain","content-type":"text\/plain","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/api.elsevier.com\/content\/article\/PII:S0012160615300063?httpAccept=text\/xml","content-type":"text\/xml","content-version":"vor","intended-application":"text-mining"}],"deposited":{"date-parts":[[2022,5,14]],"date-time":"2022-05-14T22:09:02Z","timestamp":1652566142000},"score":1,"resource":{"primary":{"URL":"https:\/\/linkinghub.elsevier.com\/retrieve\/pii\/S0012160615300063"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,8]]},"references-count":57,"journal-issue":{"issue":"2","published-print":{"date-parts":[[2015,8]]}},"alternative-id":["S0012160615300063"],"URL":"https:\/\/doi.org\/10.1016\/j.ydbio.2015.05.023","relation":{},"ISSN":["0012-1606"],"issn-type":[{"value":"0012-1606","type":"print"}],"subject":[],"published":{"date-parts":[[2015,8]]},"assertion":[{"value":"Elsevier","name":"publisher","label":"This article is maintained by"},{"value":"ROBO2 restricts the nephrogenic field and regulates Wolffian duct\u2013nephrogenic cord separation","name":"articletitle","label":"Article Title"},{"value":"Developmental Biology","name":"journaltitle","label":"Journal Title"},{"value":"https:\/\/doi.org\/10.1016\/j.ydbio.2015.05.023","name":"articlelink","label":"CrossRef DOI link to publisher maintained version"},{"value":"article","name":"content_type","label":"Content Type"},{"value":"Copyright \u00a9 2015 Elsevier Inc. All rights reserved.","name":"copyright","label":"Copyright"}]}}