{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,27]],"date-time":"2026-02-27T16:26:35Z","timestamp":1772209595271,"version":"3.50.1"},"reference-count":33,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2020,12,2]],"date-time":"2020-12-02T00:00:00Z","timestamp":1606867200000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100007428","name":"Naito Foundation","doi-asserted-by":"publisher","id":[{"id":"10.13039\/100007428","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"\n During development of the\n Caenorhabditis elegans<\/jats:italic>\n gonad, the gonadal leader cells, called distal tip cells (DTCs), migrate in a U-shaped pattern to form the U-shaped gonad arms. The ADAMTS (\n a<\/jats:underline>\n d<\/jats:underline>\n isintegrin\n a<\/jats:underline>\n nd\n m<\/jats:underline>\n etalloprotease with\n t<\/jats:underline>\n hrombo\n s<\/jats:underline>\n pondin motifs) family metalloproteases MIG-17 and GON-1 are required for correct DTC migration. Mutations in\n mig-17<\/jats:italic>\n result in misshapen gonads due to the misdirected DTC migration, and mutations in\n gon-1<\/jats:italic>\n result in shortened and swollen gonads due to the premature termination of DTC migration. Although the phenotypes shown by\n mig-17<\/jats:italic>\n and\n gon-1<\/jats:italic>\n mutants are very different from one another, mutations that result in amino acid substitutions in the same basement membrane protein genes,\n emb-9\/collagen IV a1<\/jats:italic>\n ,\n let-2<\/jats:italic>\n \/\n collagen IV a2<\/jats:italic>\n and\n fbl-1\/fibulin-1<\/jats:italic>\n , were identified as genetic suppressors of\n mig-17<\/jats:italic>\n and\n gon-1<\/jats:italic>\n mutants. To understand the roles shared by these two proteases, we examined the effects of the\n mig-17<\/jats:italic>\n suppressors on\n gon-1<\/jats:italic>\n and the effects of the\n gon-1<\/jats:italic>\n suppressors and enhancers on\n mig-17<\/jats:italic>\n gonadal defects. Some of the\n emb-9<\/jats:italic>\n ,\n let-2<\/jats:italic>\n and\n fbl-1<\/jats:italic>\n mutations suppressed both\n mig-17<\/jats:italic>\n and\n gon-1<\/jats:italic>\n , whereas others acted only on\n mig-17<\/jats:italic>\n or\n gon-1<\/jats:italic>\n . These results suggest that\n mig-17<\/jats:italic>\n and\n gon-1<\/jats:italic>\n have their specific functions as well as functions commonly shared between them for gonad formation. The levels of collagen IV accumulation in the DTC basement membrane were significantly higher in the\n gon-1<\/jats:italic>\n mutants as compared with wild type and were reduced to the wild-type levels when combined with suppressor mutations, but not with enhancer mutations, suggesting that the ability to reduce collagen IV levels is important for\n gon-1<\/jats:italic>\n suppression.\n <\/jats:p>","DOI":"10.1371\/journal.pone.0240571","type":"journal-article","created":{"date-parts":[[2020,12,2]],"date-time":"2020-12-02T14:18:23Z","timestamp":1606918703000},"page":"e0240571","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":15,"title":["Genetic interactions among ADAMTS metalloproteases and basement membrane molecules in cell migration in Caenorhabditis elegans"],"prefix":"10.1371","volume":"15","author":[{"given":"Ayaka","family":"Imanishi","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yuma","family":"Aoki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Masaki","family":"Kakehi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shunsuke","family":"Mori","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tomomi","family":"Takano","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yukihiko","family":"Kubota","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hon-Song","family":"Kim","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yukimasa","family":"Shibata","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1338-1979","authenticated-orcid":true,"given":"Kiyoji","family":"Nishiwaki","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2020,12,2]]},"reference":[{"issue":"46","key":"pone.0240571.ref001","doi-asserted-by":"crossref","first-page":"31493","DOI":"10.1074\/jbc.R109.052340","article-title":"A disintegrin-like and metalloprotease (reprolysin-type) with thrombospondin type 1 motif (ADAMTS) superfamily: functions and mechanisms","volume":"284","author":"SS Apte","year":"2009","journal-title":"J Biol Chem"},{"key":"pone.0240571.ref002","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/j.matbio.2018.06.002","article-title":"ADAMTS proteins in human disorders","volume":"71\u201372","author":"TJ Mead","year":"2018","journal-title":"Matrix Biol"},{"key":"pone.0240571.ref003","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1186\/s13059-015-0676-3","article-title":"The ADAMTS (A Disintegrin and Metalloproteinase with Thrombospondin motifs) family","volume":"16","author":"R Kelwick","year":"2015","journal-title":"Genome Biol"},{"issue":"5","key":"pone.0240571.ref004","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1016\/j.devcel.2009.09.008","article-title":"ADAMTS metalloproteases generate active versican fragments that regulate interdigital web regression","volume":"17","author":"DR McCulloch","year":"2009","journal-title":"Dev Cell"},{"issue":"1","key":"pone.0240571.ref005","doi-asserted-by":"crossref","first-page":"953","DOI":"10.1038\/s41467-019-08520-7","article-title":"Secreted metalloproteases ADAMTS9 and ADAMTS20 have a non-canonical role in ciliary vesicle growth during ciliogenesis","volume":"10","author":"S Nandadasa","year":"2019","journal-title":"Nat Commun"},{"issue":"3","key":"pone.0240571.ref006","doi-asserted-by":"crossref","first-page":"1907","DOI":"10.1074\/jbc.M112.429647","article-title":"Versican processing by a disintegrin-like and metalloproteinase domain with thrombospondin-1 repeats proteinases-5 and -15 facilitates myoblast fusion","volume":"288","author":"N Stupka","year":"2013","journal-title":"J Biol Chem"},{"issue":"6736","key":"pone.0240571.ref007","doi-asserted-by":"crossref","first-page":"586","DOI":"10.1038\/21196","article-title":"Control of organ shape by a secreted metalloprotease in the nematode Caenorhabditis elegans","volume":"399","author":"R Blelloch","year":"1999","journal-title":"Nature"},{"issue":"5474","key":"pone.0240571.ref008","doi-asserted-by":"crossref","first-page":"2205","DOI":"10.1126\/science.288.5474.2205","article-title":"A metalloprotease disintegrin that controls cell migration in Caenorhabditis elegans","volume":"288","author":"K Nishiwaki","year":"2000","journal-title":"Science"},{"issue":"11","key":"pone.0240571.ref009","doi-asserted-by":"crossref","first-page":"2607","DOI":"10.1038\/sj.emboj.7601718","article-title":"Prodomain-dependent tissue targeting of an ADAMTS protease controls cell migration in Caenorhabditis elegans","volume":"26","author":"S Ihara","year":"2007","journal-title":"EMBO J"},{"issue":"1","key":"pone.0240571.ref010","doi-asserted-by":"crossref","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":"DP Keeley","year":"2020","journal-title":"Dev Cell"},{"issue":"22","key":"pone.0240571.ref011","doi-asserted-by":"crossref","first-page":"2011","DOI":"10.1016\/j.cub.2004.10.047","article-title":"A fibulin-1 homolog interacts with an ADAM protease that controls cell migration in C. elegans","volume":"14","author":"Y Kubota","year":"2004","journal-title":"Curr Biol"},{"issue":"52","key":"pone.0240571.ref012","doi-asserted-by":"crossref","first-page":"20804","DOI":"10.1073\/pnas.0804055106","article-title":"MIG-17\/ADAMTS controls cell migration by recruiting nidogen to the basement membrane in C. elegans","volume":"105","author":"Y Kubota","year":"2008","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"22","key":"pone.0240571.ref013","doi-asserted-by":"crossref","first-page":"2005","DOI":"10.1016\/j.cub.2004.11.006","article-title":"GON-1 and fibulin have antagonistic roles in control of organ shape","volume":"14","author":"D Hesselson","year":"2004","journal-title":"Curr Biol"},{"issue":"4","key":"pone.0240571.ref014","doi-asserted-by":"crossref","first-page":"1379","DOI":"10.1534\/genetics.111.133173","article-title":"Tissue architecture in the Caenorhabditis elegans gonad depends on interactions among fibulin-1, type IV collagen and the ADAMTS extracellular protease","volume":"190","author":"Y Kubota","year":"2012","journal-title":"Genetics"},{"issue":"1","key":"pone.0240571.ref015","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1093\/genetics\/77.1.71","article-title":"The genetics of Caenorhabditis elegans","volume":"77","author":"S. Brenner","year":"1974","journal-title":"Genetics"},{"issue":"5","key":"pone.0240571.ref016","doi-asserted-by":"crossref","first-page":"1185","DOI":"10.1083\/jcb.137.5.1185","article-title":"Characterization of \u03b11(IV) collagen mutations in Caenorhabditis elegans and the effects of \u03b11 and \u03b12(IV) mutations on type IV collagen distribution","volume":"137","author":"MC Gupta","year":"1997","journal-title":"J Cell Biol"},{"issue":"14","key":"pone.0240571.ref017","doi-asserted-by":"crossref","first-page":"3278","DOI":"10.1002\/j.1460-2075.1994.tb06629.x","article-title":"Mutations in the \u03b12(IV) basement membrane collagen gene of Caenorhabditis elegans produce phenotypes of differing severities","volume":"13","author":"MH Sibley","year":"1994","journal-title":"EMBO J"},{"issue":"2","key":"pone.0240571.ref018","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1534\/genetics.113.157685","article-title":"The novel secreted factor MIG-18 acts with MIG-17\/ADAMTS to control cell migration in Caenorhabditis elegans","volume":"196","author":"HS Kim","year":"2014","journal-title":"Genetics"},{"issue":"2","key":"pone.0240571.ref019","doi-asserted-by":"crossref","first-page":"160","DOI":"10.1038\/88878","article-title":"Rapid gene mapping in Caenorhabditis elegans using a high density polymorphism map","volume":"28","author":"SR Wicks","year":"2001","journal-title":"Nat Genet"},{"issue":"3","key":"pone.0240571.ref020","doi-asserted-by":"crossref","first-page":"985","DOI":"10.1093\/genetics\/152.3.985","article-title":"Mutations affecting symmetrical migration of distal tip cells in Caenorhabditis elegans","volume":"152","author":"K. Nishiwaki","year":"1999","journal-title":"Genetics"},{"issue":"12","key":"pone.0240571.ref021","doi-asserted-by":"crossref","first-page":"3959","DOI":"10.1002\/j.1460-2075.1991.tb04966.x","article-title":"Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences","volume":"10","author":"CC Mello","year":"1991","journal-title":"EMBO J"},{"issue":"3","key":"pone.0240571.ref022","doi-asserted-by":"crossref","first-page":"977","DOI":"10.1093\/genetics\/141.3.977","article-title":"Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system","volume":"141","author":"M Maduro","year":"1995","journal-title":"Genetics"},{"issue":"3","key":"pone.0240571.ref023","doi-asserted-by":"crossref","first-page":"1323","DOI":"10.1093\/genetics\/149.3.1323","article-title":"A new marker for mosaic analysis in Caenorhabditis elegans indicates a fusion between hyp6 and hyp7, two major components of the hypodermis","volume":"149","author":"J Yochem","year":"1998","journal-title":"Genetics"},{"issue":"34","key":"pone.0240571.ref024","doi-asserted-by":"crossref","first-page":"31142","DOI":"10.1074\/jbc.M201740200","article-title":"Crystal structure of NC1 domains. Structural basis for type IV collagen assembly in basement membranes","volume":"277","author":"M Sundaramoorthy","year":"2002","journal-title":"J Biol Chem"},{"issue":"17","key":"pone.0240571.ref025","doi-asserted-by":"crossref","first-page":"4296","DOI":"10.1111\/j.1742-4658.2008.06573.x","article-title":"Stage-specific activation of MIG-17\/ADAMTS controls cell migration in Caenorhabditis elegans","volume":"275","author":"S Ihara","year":"2008","journal-title":"FEBS J"},{"issue":"1","key":"pone.0240571.ref026","doi-asserted-by":"crossref","first-page":"382","DOI":"10.1006\/dbio.1999.9491","article-title":"The gon-1 gene is required for gonadal morphogenesis in Caenorhabditis elegans","volume":"216","author":"R Blelloch","year":"1999","journal-title":"Dev Biol"},{"issue":"31","key":"pone.0240571.ref027","doi-asserted-by":"crossref","first-page":"10311","DOI":"10.1523\/JNEUROSCI.5128-13.2014","article-title":"Perlecan antagonizes collagen IV and ADAMTS9\/GON-1 in restricting the growth of presynaptic boutons","volume":"34","author":"J Qin","year":"2014","journal-title":"J Neurosci"},{"issue":"38","key":"pone.0240571.ref028","doi-asserted-by":"crossref","first-page":"12678","DOI":"10.1523\/JNEUROSCI.1183-14.2014","article-title":"Regulation of synaptic extracellular matrix composition is critical for proper synapse morphology","volume":"34","author":"PT Kurshan","year":"2014","journal-title":"J Neurosci"},{"issue":"9","key":"pone.0240571.ref029","doi-asserted-by":"crossref","first-page":"1728","DOI":"10.1091\/mbc.e11-10-0857","article-title":"Identification of a novel ADAMTS9\/GON-1 function for protein transport from the ER to the Golgi","volume":"23","author":"S Yoshina","year":"2012","journal-title":"Mol Biol Cell"},{"issue":"13","key":"pone.0240571.ref030","doi-asserted-by":"crossref","first-page":"1615","DOI":"10.1101\/gad.1534807","article-title":"Control of C. elegans hermaphrodite gonad size and shape by vab-3\/Pax6-mediated regulation of integrin receptors","volume":"21","author":"CM Meighan","year":"2007","journal-title":"Genes Dev"},{"issue":"3","key":"pone.0240571.ref031","doi-asserted-by":"crossref","first-page":"144","DOI":"10.1111\/iep.12329","article-title":"Extracellular matrix dynamics in cell migration, invasion and tissue morphogenesis","volume":"100","author":"KM Yamada","year":"2019","journal-title":"Int J Exp Pathol"},{"issue":"9","key":"pone.0240571.ref032","doi-asserted-by":"crossref","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":"MA Morrissey","year":"2015","journal-title":"J Cell Sci"},{"issue":"51","key":"pone.0240571.ref033","doi-asserted-by":"crossref","first-page":"53762","DOI":"10.1074\/jbc.M411202200","article-title":"Regulation of human beta-cell adhesion, motility, and insulin secretion by collagen IV and its receptor \u03b11\u03b21","volume":"279","author":"T Kaido","year":"2004","journal-title":"J Biol Chem"}],"updated-by":[{"DOI":"10.1371\/journal.pone.0261880","type":"correction","label":"Correction","source":"publisher","updated":{"date-parts":[[2021,12,21]],"date-time":"2021-12-21T00:00:00Z","timestamp":1640044800000}}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0240571","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,12,1]],"date-time":"2022-12-01T20:31:01Z","timestamp":1669926661000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0240571"}},"subtitle":[],"editor":[{"given":"Myeongwoo","family":"Lee","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2020,12,2]]},"references-count":33,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2020,12,2]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0240571","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.09.30.320093","asserted-by":"object"}]},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,12,2]]}}}