{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,30]],"date-time":"2026-07-30T18:40:49Z","timestamp":1785436849757,"version":"3.56.0"},"reference-count":86,"publisher":"eLife Sciences Publications, Ltd","license":[{"start":{"date-parts":[[2023,7,5]],"date-time":"2023-07-05T00:00:00Z","timestamp":1688515200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2023,7,5]],"date-time":"2023-07-05T00:00:00Z","timestamp":1688515200000},"content-version":"am","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"},{"start":{"date-parts":[[2023,7,5]],"date-time":"2023-07-05T00:00:00Z","timestamp":1688515200000},"content-version":"tdm","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000057","name":"National Institute of General Medical Sciences","doi-asserted-by":"crossref","award":["R35GM118049"],"award-info":[{"award-number":["R35GM118049"]}],"id":[{"id":"10.13039\/100000057","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["R21OD028766"],"award-info":[{"award-number":["R21OD028766"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["R21OD032430"],"award-info":[{"award-number":["R21OD032430"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"crossref","award":["F31 HD97901"],"award-info":[{"award-number":["F31 HD97901"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":["elifesciences.org"],"crossmark-restriction":false},"short-container-title":[],"abstract":"<jats:p>\n                    Separate tissues connect through adjoining basement membranes to carry out molecular barrier, exchange, and organ support functions. Cell adhesion at these connections must be robust and balanced to withstand independent tissue movement. Yet, how cells achieve synchronized adhesion to connect tissues is unknown. Here, we have investigated this question using the\n                    <jats:italic>Caenorhabditis elegans<\/jats:italic>\n                    utse-seam tissue connection that supports the uterus during egg-laying. Through genetics, quantitative fluorescence, and cell-specific molecular disruption, we show that type IV collagen, which fastens the linkage, also activates the collagen receptor discoidin domain receptor-2 (DDR-2) in both the utse and seam. RNAi depletion, genome editing, and photobleaching experiments revealed that DDR-2 signals through LET-60\/Ras to coordinately strengthen an integrin adhesion in the utse and seam that stabilizes their connection. These results uncover a synchronizing mechanism for robust adhesion during tissue connection, where collagen both affixes the linkage and signals to both tissues to bolster their adhesion.\n                  <\/jats:p>","DOI":"10.7554\/elife.87037","type":"journal-article","created":{"date-parts":[[2023,5,11]],"date-time":"2023-05-11T03:32:58Z","timestamp":1683775978000},"update-policy":"https:\/\/doi.org\/10.7554\/elife.87037","source":"Crossref","is-referenced-by-count":7,"title":["Reciprocal discoidin domain receptor signaling strengthens integrin adhesion to connect adjacent tissues"],"prefix":"10.7554","volume":"12","author":[{"given":"Kieop","family":"Park","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00py81415","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biology, Duke University","place":["Durham, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0465-0337","authenticated-orcid":true,"given":"Ranjay","family":"Jayadev","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00py81415","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biology, Duke University","place":["Durham, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara G","family":"Payne","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00py81415","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biology, Duke University","place":["Durham, United States"]},{"id":[{"id":"https:\/\/ror.org\/00py81415","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Cell Biology, Duke University Medical Center","place":["Durham, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabel W","family":"Kenny-Ganzert","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00py81415","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biology, Duke University","place":["Durham, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiuyi","family":"Chi","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00py81415","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biology, Duke University","place":["Durham, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel S","family":"Costa","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00py81415","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biology, Duke University","place":["Durham, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"William","family":"Ramos-Lewis","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00py81415","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biology, Duke University","place":["Durham, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Siddharthan B","family":"Thendral","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00py81415","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biology, Duke University","place":["Durham, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4448-6917","authenticated-orcid":true,"given":"David R","family":"Sherwood","sequence":"additional","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00py81415","id-type":"ROR","asserted-by":"publisher"}],"name":"Department of Biology, Duke University","place":["Durham, United States"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"4374","published-online":{"date-parts":[[2023,7,5]]},"reference":[{"key":"bib1","doi-asserted-by":"publisher","first-page":"1988","DOI":"10.1083\/jcb.100.6.1988","article-title":"Origin of the glomerular basement membrane visualized after in vivo labeling of laminin in newborn rat kidneys","volume":"100","author":"Abrahamson","year":"1985","journal-title":"The Journal of Cell Biology"},{"key":"bib2","doi-asserted-by":"publisher","first-page":"1160","DOI":"10.1016\/j.dci.2010.06.010","article-title":"Role of matrix metalloproteinase ZMP-2 in pathogen resistance and development in Caenorhabditis elegans","volume":"34","author":"Altincicek","year":"2010","journal-title":"Developmental and Comparative Immunology"},{"key":"bib3","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.45508","article-title":"DDR2 controls breast tumor stiffness and metastasis by regulating integrin mediated Mechanotransduction in Cafs","volume":"8","author":"Bayer","year":"2019","journal-title":"eLife"},{"key":"bib4","doi-asserted-by":"publisher","first-page":"2999","DOI":"10.1007\/s00018-017-2511-3","article-title":"Vinculin in cell-cell and cell-matrix Adhesions","volume":"74","author":"Bays","year":"2017","journal-title":"Cellular and Molecular Life Sciences"},{"key":"bib5","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-07976-3","article-title":"Discoidin-domain receptor coordinates cell-matrix adhesion and collective polarity in migratory cardiopharyngeal progenitors","volume":"10","author":"Bernadskaya","year":"2019","journal-title":"Nature Communications"},{"key":"bib6","doi-asserted-by":"publisher","first-page":"185","DOI":"10.1016\/j.matbio.2013.12.002","article-title":"Discoidin domain receptors in disease","volume":"34","author":"Borza","year":"2014","journal-title":"Matrix Biology"},{"key":"bib7","doi-asserted-by":"publisher","DOI":"10.3389\/fcell.2022.836797","article-title":"The collagen receptor discoidin domain receptor 1B enhances integrin beta1-mediated cell migration by interacting with talin and promoting Rac1 activation","volume":"10","author":"Borza","year":"2022","journal-title":"Frontiers in Cell and Developmental Biology"},{"key":"bib8","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a005082","article-title":"Extracellular matrix in development: insights from mechanisms conserved between invertebrates and vertebrates","volume":"3","author":"Brown","year":"2011","journal-title":"Cold Spring Harbor Perspectives in Biology"},{"key":"bib9","doi-asserted-by":"publisher","first-page":"2151","DOI":"10.1002\/pro.3283","article-title":"Building collagen IV smart scaffolds on the outside of cells","volume":"26","author":"Brown","year":"2017","journal-title":"Protein Science"},{"key":"bib10","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1000907","article-title":"Genetic analysis of fin development in zebrafish identifies furin and hemicentin1 as potential novel Fraser Syndrome disease genes","volume":"6","author":"Carney","year":"2010","journal-title":"PLOS Genetics"},{"key":"bib11","doi-asserted-by":"publisher","first-page":"843","DOI":"10.1016\/j.ejcb.2010.07.004","article-title":"Native type IV collagen induces cell migration through a CD9 and DDR1-dependent pathway in MDA-MB-231 breast cancer cells","volume":"89","author":"Castro-Sanchez","year":"2010","journal-title":"European Journal of Cell Biology"},{"key":"bib12","doi-asserted-by":"publisher","DOI":"10.1186\/1471-213X-7-30","article-title":"Large-scale RNAi screens identify novel genes that interact with the C. elegans retinoblastoma pathway as well as splicing-related components with synMuv B activity","volume":"7","author":"Ceron","year":"2007","journal-title":"BMC Developmental Biology"},{"key":"bib13","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1016\/j.ydbio.2008.09.014","article-title":"The MIG-15 NIK kinase acts cell-autonomously in neuroblast polarization and migration in C. elegans","volume":"324","author":"Chapman","year":"2008","journal-title":"Developmental Biology"},{"key":"bib14","doi-asserted-by":"publisher","first-page":"R536","DOI":"10.1016\/j.cub.2021.01.038","article-title":"Integrin adhesion complexes","volume":"31","author":"Chastney","year":"2021","journal-title":"Current Biology"},{"key":"bib15","doi-asserted-by":"publisher","DOI":"10.3389\/fcell.2021.747314","article-title":"Recent advances in the role of discoidin domain receptor tyrosine kinase 1 and discoidin domain receptor tyrosine kinase 2 in breast and ovarian cancer","volume":"9","author":"Chen","year":"2021","journal-title":"Frontiers in Cell and Developmental Biology"},{"key":"bib16","doi-asserted-by":"publisher","first-page":"337","DOI":"10.1016\/bs.ctm.2015.08.001","article-title":"Basement membranes in the worm: A dynamic scaffolding that instructs cellular behaviors and shapes tissues","volume":"76","author":"Clay","year":"2015","journal-title":"Current Topics in Membranes"},{"key":"bib17","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2121-11-14","article-title":"R-Ras regulates beta1-integrin trafficking via effects on membrane ruffling and endocytosis","volume":"11","author":"Conklin","year":"2010","journal-title":"BMC Cell Biology"},{"key":"bib18","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-019-53176-4","article-title":"DDR1 autophosphorylation is a result of aggregation into dense clusters","volume":"9","author":"Corcoran","year":"2019","journal-title":"Scientific Reports"},{"key":"bib19","doi-asserted-by":"publisher","first-page":"1028","DOI":"10.1038\/nmeth.2641","article-title":"Engineering the Caenorhabditis elegans genome using Cas9-triggered homologous recombination","volume":"10","author":"Dickinson","year":"2013","journal-title":"Nature Methods"},{"key":"bib20","doi-asserted-by":"publisher","DOI":"10.1002\/0471142727.mb1420s92","article-title":"Computer control of microscopes using microManager","volume":"Chapter 14","author":"Edelstein","year":"2010","journal-title":"Current Protocols in Molecular Biology"},{"key":"bib21","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/j.ydbio.2012.06.023","article-title":"Hemicentin 2 And Fibulin 1 are required for epidermal-dermal junction formation and fin mesenchymal cell migration during zebrafish development","volume":"369","author":"Feitosa","year":"2012","journal-title":"Developmental Biology"},{"key":"bib22","doi-asserted-by":"publisher","DOI":"10.1242\/jcs.203950","article-title":"The triple helix of collagens - an ancient protein structure that enabled animal multicellularity and tissue evolution","volume":"131","author":"Fidler","year":"2018","journal-title":"Journal of Cell Science"},{"key":"bib23","doi-asserted-by":"publisher","first-page":"5083","DOI":"10.1038\/sj.emboj.7601922","article-title":"RAP-1 and the RAL-1\/exocyst pathway coordinate hypodermal cell organization in Caenorhabditis elegans","volume":"26","author":"Frische","year":"2007","journal-title":"The EMBO Journal"},{"key":"bib24","doi-asserted-by":"publisher","first-page":"117","DOI":"10.1038\/nmeth.1865","article-title":"Improved Mos1-mediated transgenesis in C. elegans","volume":"9","author":"Fr\u00f8kj\u00e6r-Jensen","year":"2012","journal-title":"Nature Methods"},{"key":"bib25","doi-asserted-by":"publisher","first-page":"7430","DOI":"10.1074\/jbc.R112.444158","article-title":"Discoidin domain receptors: unique receptor tyrosine kinases in collagen-mediated signaling","volume":"288","author":"Fu","year":"2013","journal-title":"Journal of Biological Chemistry"},{"key":"bib26","doi-asserted-by":"publisher","first-page":"584","DOI":"10.1096\/fj.201600870R","article-title":"Regulation of the blood-testis barrier by a local axis in the testis: role of laminin alpha2 in the basement membrane","volume":"31","author":"Gao","year":"2017","journal-title":"FASEB Journal"},{"key":"bib27","doi-asserted-by":"publisher","first-page":"121","DOI":"10.1016\/j.ydbio.2014.09.028","article-title":"Spatial and molecular cues for cell outgrowth during C. elegans uterine development","volume":"396","author":"Ghosh","year":"2014","journal-title":"Developmental Biology"},{"key":"bib28","doi-asserted-by":"publisher","DOI":"10.1083\/jcb.202112096","article-title":"Hemicentin-mediated type IV collagen assembly strengthens juxtaposed basement membrane linkage","volume":"222","author":"Gianakas","year":"2023","journal-title":"The Journal of Cell Biology"},{"key":"bib29","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1895\/wormbook.1.81.2","article-title":"Development, structure, and maintenance of C. elegans body wall muscle","volume":"2017","author":"Gieseler","year":"2017","journal-title":"WormBook"},{"key":"bib30","doi-asserted-by":"publisher","DOI":"10.1101\/cshperspect.a017459","article-title":"Endocytosis of receptor tyrosine kinases","volume":"5","author":"Goh","year":"2013","journal-title":"Cold Spring Harbor Perspectives in Biology"},{"key":"bib31","doi-asserted-by":"publisher","first-page":"102","DOI":"10.1111\/j.1523-1755.2004.00712.x","article-title":"DDR1-deficient mice show localized subepithelial GBM thickening with focal loss of slit diaphragms and proteinuria","volume":"66","author":"Gross","year":"2004","journal-title":"Kidney International"},{"key":"bib32","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1016\/j.devcel.2009.06.006","article-title":"Integrin acts upstream of netrin signaling to regulate formation of the anchor cell\u2019s invasive membrane in C. elegans","volume":"17","author":"Hagedorn","year":"2009","journal-title":"Developmental Cell"},{"key":"bib33","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1006475","article-title":"The C. elegans discoidin domain receptor DDR-2 modulates the met-like RTK-JNK signaling pathway in axon regeneration","volume":"12","author":"Hisamoto","year":"2016","journal-title":"PLOS Genetics"},{"key":"bib34","doi-asserted-by":"publisher","first-page":"56","DOI":"10.4161\/cam.21831","article-title":"Laminins in basement membrane assembly","volume":"7","author":"Hohenester","year":"2013","journal-title":"Cell Adhesion & Migration"},{"key":"bib35","doi-asserted-by":"publisher","first-page":"R207","DOI":"10.1016\/j.cub.2017.02.006","article-title":"Basement membranes","volume":"27","author":"Jayadev","year":"2017","journal-title":"Current Biology"},{"key":"bib36","doi-asserted-by":"publisher","first-page":"3098","DOI":"10.1083\/jcb.201903124","article-title":"Alpha-integrins dictate distinct modes of type IV collagen recruitment to basement membranes","volume":"218","author":"Jayadev","year":"2019","journal-title":"The Journal of Cell Biology"},{"key":"bib37","doi-asserted-by":"publisher","DOI":"10.1126\/sciadv.abn2265","article-title":"A basement membrane discovery pipeline uncovers network complexity, regulators, and human disease associations","volume":"8","author":"Jayadev","year":"2022","journal-title":"Science Advances"},{"key":"bib38","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.25716","article-title":"Collagen induces activation of DDR1 through lateral dimer association and phosphorylation between dimers","volume":"6","author":"Juskaite","year":"2017","journal-title":"eLife"},{"key":"bib39","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1016\/s1046-2023(03)00050-1","article-title":"Genome-wide RNAi screening in Caenorhabditis elegans","volume":"30","author":"Kamath","year":"2003","journal-title":"Methods"},{"key":"bib40","doi-asserted-by":"publisher","first-page":"58","DOI":"10.1016\/j.matbio.2018.05.009","article-title":"Tissue linkage through adjoining basement membranes: the long and the short term of it","volume":"75\u201376","author":"Keeley","year":"2019","journal-title":"Matrix Biology"},{"key":"bib41","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1016\/j.devcel.2020.05.022","article-title":"Comprehensive endogenous tagging of basement membrane components reveals dynamic movement within the matrix scaffolding","volume":"54","author":"Keeley","year":"2020","journal-title":"Developmental Cell"},{"key":"bib42","doi-asserted-by":"publisher","first-page":"2081","DOI":"10.1038\/nprot.2017.093","article-title":"Live-cell confocal microscopy and quantitative 4D image analysis of anchor-cell invasion through the basement membrane in Caenorhabditis elegans","volume":"12","author":"Kelley","year":"2017","journal-title":"Nature Protocols"},{"key":"bib43","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1016\/j.devcel.2018.12.018","article-title":"Adaptive F-actin polymerization and localized ATP production drive basement membrane invasion in the absence of Mmps","volume":"48","author":"Kelley","year":"2019","journal-title":"Developmental Cell"},{"key":"bib44","doi-asserted-by":"publisher","first-page":"357","DOI":"10.1002\/jemt.20564","article-title":"Mammalian collagen IV","volume":"71","author":"Khoshnoodi","year":"2008","journal-title":"Microscopy Research and Technique"},{"key":"bib45","doi-asserted-by":"publisher","first-page":"36404","DOI":"10.1074\/jbc.M105795200","article-title":"Roles for Beta(Pat-3) integrins in development and function of Caenorhabditis elegans muscles and gonads","volume":"276","author":"Lee","year":"2001","journal-title":"The Journal of Biological Chemistry"},{"key":"bib46","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/B978-0-12-800180-6.00002-5","article-title":"Discoidin domain receptor functions in physiological and pathological conditions","volume":"310","author":"Leitinger","year":"2014","journal-title":"International Review of Cell and Molecular Biology"},{"key":"bib47","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1038\/ncb3487","article-title":"SHANK proteins limit integrin activation by directly interacting with Rap1 and R-Ras","volume":"19","author":"Lilja","year":"2017","journal-title":"Nature Cell Biology"},{"key":"bib48","doi-asserted-by":"publisher","first-page":"729","DOI":"10.1101\/gad.13.6.729","article-title":"Uncoupling integrin adhesion and signaling: the betaPS cytoplasmic domain is sufficient to regulate gene expression in the Drosophila embryo","volume":"13","author":"Martin-Bermudo","year":"1999","journal-title":"Genes & Development"},{"key":"bib49","doi-asserted-by":"publisher","first-page":"1609","DOI":"10.1097\/00005537-200409000-00020","article-title":"Temporal bone histopathology in Alport syndrome","volume":"114","author":"Merchant","year":"2004","journal-title":"The Laryngoscope"},{"key":"bib50","doi-asserted-by":"publisher","first-page":"432","DOI":"10.1016\/j.jmb.2008.10.067","article-title":"Mapping of DDR1 distribution and oligomerization on the cell surface by FRET microscopy","volume":"385","author":"Mihai","year":"2009","journal-title":"Journal of Molecular Biology"},{"key":"bib51","doi-asserted-by":"publisher","DOI":"10.1895\/wormbook.1.81.1","volume-title":"WormBook: Sarcomere Assembly in C. elegans Muscle","author":"Moerman","year":"2006"},{"key":"bib52","doi-asserted-by":"publisher","DOI":"10.1186\/s12861-015-0076-7","article-title":"Morphologically defined sub-stages of C. elegans vulval development in the fourth larval stage","volume":"15","author":"Mok","year":"2015","journal-title":"BMC Developmental Biology"},{"key":"bib53","doi-asserted-by":"publisher","first-page":"319","DOI":"10.1016\/j.devcel.2014.08.024","article-title":"B-LINK: a hemicentin, plakin, and integrin-dependent adhesion system that links tissues by connecting adjacent basement membranes","volume":"31","author":"Morrissey","year":"2014","journal-title":"Developmental Cell"},{"key":"bib54","doi-asserted-by":"publisher","first-page":"1661","DOI":"10.1242\/jcs.168021","article-title":"An active role for basement membrane assembly and modification in tissue sculpting","volume":"128","author":"Morrissey","year":"2015","journal-title":"Journal of Cell Science"},{"key":"bib55","doi-asserted-by":"publisher","first-page":"17615","DOI":"10.1073\/pnas.0906541106","article-title":"Endosomes: a legitimate platform for the signaling train","volume":"106","author":"Murphy","year":"2009","journal-title":"PNAS"},{"key":"bib56","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1038\/s41581-020-0329-y","article-title":"Complexities of the glomerular basement membrane","volume":"17","author":"Naylor","year":"2021","journal-title":"Nature Reviews. Nephrology"},{"key":"bib57","doi-asserted-by":"publisher","first-page":"3617","DOI":"10.1242\/dev.122.11.3617","article-title":"Morphogenesis of the C. elegans hermaphrodite uterus","volume":"122","author":"Newman","year":"1996","journal-title":"Development"},{"key":"bib58","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.38325","article-title":"Direct visualization of a native WNT in vivo reveals that a long-range WNT gradient forms by extracellular dispersal","volume":"7","author":"Pani","year":"2018","journal-title":"eLife"},{"key":"bib59","doi-asserted-by":"publisher","DOI":"10.1186\/1471-213X-10-14","article-title":"Characterization of the astacin family of metalloproteases in C. elegans","volume":"10","author":"Park","year":"2010","journal-title":"BMC Developmental Biology"},{"key":"bib60","doi-asserted-by":"publisher","first-page":"900","DOI":"10.1097\/JTO.0000000000000164","article-title":"Discoidin domain receptor 2 signaling networks and therapy in lung cancer","volume":"9","author":"Payne","year":"2014","journal-title":"Journal of Thoracic Oncology"},{"key":"bib61","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.matbio.2016.12.009","article-title":"The nature and biology of basement membranes","volume":"57\u201358","author":"Pozzi","year":"2017","journal-title":"Matrix Biology"},{"key":"bib62","doi-asserted-by":"publisher","first-page":"2162","DOI":"10.1101\/gr.2505604","article-title":"Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library","volume":"14","author":"Rual","year":"2004","journal-title":"Genome Research"},{"key":"bib63","doi-asserted-by":"publisher","first-page":"1479","DOI":"10.1038\/cr.2012.110","article-title":"The R-Ras\/Rin2\/Rab5 complex controls endothelial cell adhesion and morphogenesis via active integrin endocytosis and RAC signaling","volume":"22","author":"Sandri","year":"2012","journal-title":"Cell Research"},{"key":"bib64","doi-asserted-by":"publisher","DOI":"10.1895\/wormbook.1.77.2","volume-title":"WormBook: The Online Review of C. elegans Biology","author":"Sato","year":"2014"},{"key":"bib65","doi-asserted-by":"publisher","first-page":"676","DOI":"10.1038\/nmeth.2019","article-title":"Fiji: an open-source platform for biological-image analysis","volume":"9","author":"Schindelin","year":"2012","journal-title":"Nature Methods"},{"key":"bib66","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/s1534-5807(03)00168-0","article-title":"Anchor cell invasion into the vulval epithelium in C. elegans","volume":"5","author":"Sherwood","year":"2003","journal-title":"Developmental Cell"},{"key":"bib67","doi-asserted-by":"publisher","first-page":"2251","DOI":"10.1101\/gad.9.18.2251","article-title":"sur-2, a novel gene, functions late in the let-60 ras-mediated signaling pathway during Caenorhabditis elegans Vulval induction","volume":"9","author":"Singh","year":"1995","journal-title":"Genes & Development"},{"key":"bib68","doi-asserted-by":"publisher","first-page":"933","DOI":"10.1083\/jcb.153.5.933","article-title":"Endothelial cell laminin isoforms, laminins 8 and 10, play decisive roles in T cell recruitment across the blood-brain barrier in experimental autoimmune encephalomyelitis","volume":"153","author":"Sixt","year":"2001","journal-title":"The Journal of Cell Biology"},{"key":"bib69","doi-asserted-by":"publisher","first-page":"1148","DOI":"10.1242\/bio.20135090","article-title":"Interactions between the discoidin domain receptor 1 and Beta1 integrin regulate attachment to collagen","volume":"2","author":"Staudinger","year":"2013","journal-title":"Biology Open"},{"key":"bib70","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1895\/wormbook.1.101.1","article-title":"Maintenance of C. elegans","author":"Stiernagle","year":"2006","journal-title":"WormBook"},{"key":"bib71","doi-asserted-by":"publisher","DOI":"10.7554\/eLife.01149","article-title":"Nanoscale protein architecture of the kidney glomerular basement membrane","volume":"2","author":"Suleiman","year":"2013","journal-title":"eLife"},{"key":"bib72","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1016\/j.mcn.2018.03.003","article-title":"The transmembrane collagen COL-99 guides longitudinally extending axons in C. elegans","volume":"89","author":"Taylor","year":"2018","journal-title":"Molecular and Cellular Neurosciences"},{"key":"bib73","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1016\/s0378-1119(00)00579-5","article-title":"Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans","volume":"263","author":"Timmons","year":"2001","journal-title":"Gene"},{"key":"bib74","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1111\/j.1432-1033.1981.tb05690.x","article-title":"A network model for the organization of type IV collagen molecules in basement membranes","volume":"120","author":"Timpl","year":"1981","journal-title":"European Journal of Biochemistry"},{"key":"bib75","doi-asserted-by":"publisher","DOI":"10.1186\/s12862-015-0554-3","article-title":"Membrane-associated collagens with interrupted triple-helices (MACITs): evolution from a bilaterian common ancestor and functional conservation in C. elegans","volume":"15","author":"Tu","year":"2015","journal-title":"BMC Evolutionary Biology"},{"key":"bib76","doi-asserted-by":"publisher","first-page":"142","DOI":"10.1016\/j.ydbio.2012.11.001","article-title":"Discoidin domain receptors guide axons along longitudinal tracts in C. elegans","volume":"374","author":"Unsoeld","year":"2013","journal-title":"Developmental Biology"},{"key":"bib77","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1016\/j.ceb.2016.02.002","article-title":"Signal processing by the endosomal system","volume":"39","author":"Villase\u00f1or","year":"2016","journal-title":"Current Opinion in Cell Biology"},{"key":"bib78","doi-asserted-by":"publisher","first-page":"883","DOI":"10.1242\/dev.128.6.883","article-title":"Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line-shaped junctions","volume":"128","author":"Vogel","year":"2001","journal-title":"Development"},{"key":"bib79","doi-asserted-by":"publisher","first-page":"1108","DOI":"10.1016\/j.cellsig.2006.02.012","article-title":"Sensing extracellular matrix: an update on discoidin domain receptor function","volume":"18","author":"Vogel","year":"2006","journal-title":"Cellular Signalling"},{"key":"bib80","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1006592","article-title":"Beta-integrin de-phosphorylation by the density-enhanced phosphatase DEP-1 attenuates EGFR signaling in C. elegans","volume":"13","author":"Walser","year":"2017","journal-title":"PLOS Genetics"},{"key":"bib81","doi-asserted-by":"publisher","DOI":"10.1038\/s41598-021-96824-4","article-title":"Hemicentin-1 is an essential extracellular matrix component of the dermal-epidermal and myotendinous junctions","volume":"11","author":"Welcker","year":"2021","journal-title":"Scientific Reports"},{"key":"bib82","doi-asserted-by":"publisher","first-page":"4375","DOI":"10.1242\/dev.066431","article-title":"Cell shape and WNT signaling redundantly control the division axis of C. elegans epithelial stem cells","volume":"138","author":"Wildwater","year":"2011","journal-title":"Development"},{"key":"bib83","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pgen.1005249","article-title":"Minor type IV collagen alpha5 chain promotes cancer progression through discoidin domain receptor-1","volume":"11","author":"Xiao","year":"2015","journal-title":"PLOS Genetics"},{"key":"bib84","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0052209","article-title":"Discoidin domain receptors promote alpha1beta1- and alpha2beta1-integrin mediated cell adhesion to collagen by enhancing integrin activation","volume":"7","author":"Xu","year":"2012","journal-title":"PLOS ONE"},{"key":"bib85","doi-asserted-by":"publisher","first-page":"4761","DOI":"10.1242\/dev.00701","article-title":"Investigating C. elegans development through mosaic analysis","volume":"130","author":"Yochem","year":"2003","journal-title":"Development"},{"key":"bib86","doi-asserted-by":"publisher","first-page":"61","DOI":"10.1016\/s0092-8674(00)81082-x","article-title":"Integrin activation by R-Ras","volume":"85","author":"Zhang","year":"1996","journal-title":"Cell"}],"container-title":["eLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/cdn.elifesciences.org\/articles\/87037\/elife-87037-v1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/cdn.elifesciences.org\/articles\/87037\/elife-87037-v1.xml","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/elifesciences.org\/articles\/87037","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,10,13]],"date-time":"2023-10-13T19:02:58Z","timestamp":1697223778000},"score":1,"resource":{"primary":{"URL":"https:\/\/elifesciences.org\/articles\/87037"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,5]]},"references-count":86,"alternative-id":["10.7554\/eLife.87037"],"URL":"https:\/\/doi.org\/10.7554\/elife.87037","archive":["CLOCKSS"],"relation":{"has-preprint":[{"id-type":"doi","id":"10.7554\/eLife.87037.2","asserted-by":"subject"},{"id-type":"doi","id":"10.1101\/2023.03.14.532639","asserted-by":"subject"}],"is-same-as":[{"id-type":"doi","id":"10.7554\/eLife.87037.3","asserted-by":"subject"}],"is-version-of":[{"id-type":"doi","id":"10.7554\/eLife.87037.1","asserted-by":"subject"},{"id-type":"doi","id":"10.7554\/eLife.87037.2","asserted-by":"subject"}]},"ISSN":["2050-084X"],"issn-type":[{"value":"2050-084X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,5]]},"assertion":[{"value":"single anonymised","name":"peer_review_transparency","label":"Peer review transparency","group":{"name":"peer_review_taxonomy"}},{"value":"other reviewer(s), editor","name":"peer_review_interaction","label":"Peer review interaction","group":{"name":"peer_review_taxonomy"}},{"value":"review summaries, review reports, author\/editor communication, reviewer identities reviewer opt in, editor identities","name":"peer_review_published","label":"Peer review published","group":{"name":"peer_review_taxonomy"}},{"value":"open (sign in with ORCID iD required)","name":"post_publication_commenting","label":"Post publication commenting","group":{"name":"post_publication_commenting"}}],"article-number":"RP87037"}}