{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,20]],"date-time":"2025-10-20T10:11:11Z","timestamp":1760955071335},"reference-count":30,"publisher":"Oxford University Press (OUP)","issue":"12","license":[{"start":{"date-parts":[[2008,9,11]],"date-time":"2008-09-11T00:00:00Z","timestamp":1221091200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2008,12,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Ciliary epithelium (CE), which consists of nonpigmented and pigmented layers, develops from the optic vesicle. However, the molecular mechanisms underlying CE development have not been closely examined, in part because cell-surface markers suitable for specific labeling of subregions of the retina were unknown. Here, we identified CD138\/syndecan-1 and stage specific embryonic antigen-1 (SSEA-1) CD15 as cell-surface antigens marking nonpigmented and pigmented CE, respectively. During retinal development, both CD138 and SSEA-1 were expressed in the early stage, and segregation of these markers in the tissue began at around embryonic day (E) 10. As a result, CD138-positive (CD138+) cells were found at the most distal tip of the retina, and SSEA-1+ cells were found in the periphery adjacent to the area of CD138 expression. In vitro characterization of isolated CD138+ or SSEA-1+ cell subpopulations revealed that CD138+ cells lose their retinal progenitor characteristics between E13 and E16, suggesting that they commit to becoming nonpigmented CE cells within this period. By in vivo mouse models, we found that stabilized \u03b2-catenin expanded the area of CD138+ nonpigmented CE and that elimination of \u03b2-catenin inhibited development of nonpigmented CE cells. These findings are the first to use cell-surface markers to ascertain the spatial and temporal transitions that occur in developing CE.<\/jats:p>\n               <jats:p>Disclosure of potential conflicts of interest is found at the end of this article.<\/jats:p>","DOI":"10.1634\/stemcells.2008-0303","type":"journal-article","created":{"date-parts":[[2008,9,12]],"date-time":"2008-09-12T01:38:11Z","timestamp":1221183491000},"page":"3162-3171","source":"Crossref","is-referenced-by-count":8,"title":["CD138\/Syndecan-1 and SSEA-1 Mark Distinct Populations of Developing Ciliary Epithelium That Are Regulated Differentially by Wnt Signal"],"prefix":"10.1093","volume":"26","author":[{"given":"Hideto","family":"Koso","sequence":"first","affiliation":[{"name":"Department of Molecular and Developmental Biology, Institute of Medical Science, University of Tokyo, Tokyo, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Atsumi","family":"Iida","sequence":"additional","affiliation":[{"name":"Department of Molecular and Developmental Biology, Institute of Medical Science, University of Tokyo, Tokyo, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yoko","family":"Tabata","sequence":"additional","affiliation":[{"name":"Department of Molecular and Developmental Biology, Institute of Medical Science, University of Tokyo, Tokyo, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Yukihiro","family":"Baba","sequence":"additional","affiliation":[{"name":"Department of Molecular and Developmental Biology, Institute of Medical Science, University of Tokyo, Tokyo, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Shinya","family":"Satoh","sequence":"additional","affiliation":[{"name":"Department of Molecular and Developmental Biology, Institute of Medical Science, University of Tokyo, Tokyo, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mark M.","family":"Taketo","sequence":"additional","affiliation":[{"name":"Department of Pharmacology, Graduate School of Medicine, Kyoto University, Kyoto, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Sumiko","family":"Watanabe","sequence":"additional","affiliation":[{"name":"Department of Molecular and Developmental Biology, Institute of Medical Science, University of Tokyo, Tokyo, Japan"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"286","published-online":{"date-parts":[[2008,9,11]]},"reference":[{"key":"2022011315271229000_bib1","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1006\/bbrc.2000.2473","article-title":"Identification of neural progenitors in the adult mammalian eye","volume":"270","author":"Ahmad","year":"2000","journal-title":"Biochem Biophys Res Commun"},{"key":"2022011315271229000_bib2","doi-asserted-by":"crossref","first-page":"2032","DOI":"10.1126\/science.287.5460.2032","article-title":"Retinal stem cells in the adult mammalian eye","volume":"287","author":"Tropepe","year":"2000","journal-title":"Science"},{"key":"2022011315271229000_bib3","first-page":"123","article-title":"Development of the ciliary body: A brief review","volume":"105","author":"Beebe","year":"1986","journal-title":"Trans Ophthalmol Soc U K"},{"key":"2022011315271229000_bib4","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/S0006-291X(02)02126-5","article-title":"Differentiation of embryonic stem cells into retinal neurons","volume":"297","author":"Zhao","year":"2002","journal-title":"Biochem Biophys Res Commun"},{"key":"2022011315271229000_bib5","doi-asserted-by":"crossref","first-page":"4473","DOI":"10.1242\/jcs.02575","article-title":"Negative regulation of retinal-neurite extension by \u03b2-catenin signalling pathway","volume":"118","author":"Ouchi","year":"2005","journal-title":"J Cell Sci"},{"key":"2022011315271229000_bib6","doi-asserted-by":"crossref","first-page":"424","DOI":"10.1016\/j.ydbio.2006.08.015","article-title":"\u03b2-Catenin is essential for lamination but not neurogenesis in mouse retinal development","volume":"299","author":"Fu","year":"2006","journal-title":"Dev Biol"},{"key":"2022011315271229000_bib7","doi-asserted-by":"crossref","first-page":"469","DOI":"10.1016\/j.cell.2006.10.018","article-title":"Wnt\/\u03b2-catenin signaling in development and disease","volume":"127","author":"Clevers","year":"2006","journal-title":"Cell"},{"key":"2022011315271229000_bib8","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1002\/dvdy.10315","article-title":"Characterization of Wnt signaling components and activation of the Wnt canonical pathway in the murine retina","volume":"227","author":"Liu","year":"2003","journal-title":"Dev Dyn"},{"key":"2022011315271229000_bib9","doi-asserted-by":"crossref","first-page":"5088","DOI":"10.1167\/iovs.06-0403","article-title":"Mapping canonical Wnt signaling in the developing and adult retina","volume":"47","author":"Liu","year":"2006","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"2022011315271229000_bib10","doi-asserted-by":"crossref","first-page":"3167","DOI":"10.1242\/dev.02474","article-title":"Wnt2b\/\u03b2-catenin-mediated canonical Wnt signaling determines the peripheral fates of the chick eye","volume":"133","author":"Cho","year":"2006","journal-title":"Development"},{"key":"2022011315271229000_bib11","doi-asserted-by":"crossref","first-page":"54","DOI":"10.1016\/j.ydbio.2007.04.052","article-title":"Ciliary margin transdifferentiation from neural retina is controlled by canonical Wnt signaling","volume":"308","author":"Liu","year":"2007","journal-title":"Dev Biol"},{"key":"2022011315271229000_bib12","doi-asserted-by":"crossref","first-page":"5931","DOI":"10.1093\/emboj\/18.21.5931","article-title":"Intestinal polyposis in mice with a dominant stable mutation of the \u03b2-catenin gene","volume":"18","author":"Harada","year":"1999","journal-title":"EMBO J"},{"key":"2022011315271229000_bib13","doi-asserted-by":"crossref","first-page":"1253","DOI":"10.1242\/dev.128.8.1253","article-title":"Inactivation of the \u03b2-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development","volume":"128","author":"Brault","year":"2001","journal-title":"Development"},{"key":"2022011315271229000_bib14","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1016\/S0092-8674(01)00295-1","article-title":"Pax6 is required for the multipotent state of retinal progenitor cells","volume":"105","author":"Marquardt","year":"2001","journal-title":"Cell"},{"key":"2022011315271229000_bib15","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1006\/dbio.1998.9128","article-title":"Distinct cis-essential modules direct the time-space pattern of the Pax6 gene activity","volume":"205","author":"Kammandel","year":"1999","journal-title":"Dev Biol"},{"key":"2022011315271229000_bib16","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/S0014-5793(97)00313-X","article-title":"\u2018Green mice\u2019 as a source of ubiquitous green cells","volume":"407","author":"Okabe","year":"1997","journal-title":"FEBS Lett"},{"key":"2022011315271229000_bib17","first-page":"1","article-title":"Green fluorescent protein (GFP) as a vital marker in mammals","volume":"44","author":"Ikawa","year":"1999","journal-title":"Curr Top Dev Biol"},{"key":"2022011315271229000_bib18","doi-asserted-by":"crossref","first-page":"4513","DOI":"10.1128\/MCB.24.10.4513-4521.2004","article-title":"Retinal fate specification of mouse embryonic stem cells by ectopic expression of Rx\/rax, a homeobox gene","volume":"24","author":"Tabata","year":"2004","journal-title":"Mol Cell Biol"},{"key":"2022011315271229000_bib19","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/S0166-6851(99)00102-4","article-title":"A monoclonal antibody against a glycolipid SEGLx from Spirometra erinaceieuropaei plerocercoid","volume":"102","author":"Yanagisawa","year":"1999","journal-title":"Mol Biochem Parasitol"},{"key":"2022011315271229000_bib20","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1016\/j.ydbio.2005.09.051","article-title":"SSEA-1 marks regionally restricted immature subpopulations of embryonic retinal progenitor cells","volume":"292","author":"Koso","year":"2006","journal-title":"Dev Biol"},{"key":"2022011315271229000_bib21","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/j.ydbio.2006.09.027","article-title":"c-kit marks late retinal progenitor cells and regulates their differentiation in developing mouse retina","volume":"301","author":"Koso","year":"2007","journal-title":"Dev Biol"},{"key":"2022011315271229000_bib22","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1091\/mbc.5.7.797","article-title":"Members of the syndecan family of heparan sulfate proteoglycans are expressed in distinct cell-, tissue-, and development-specific patterns","volume":"5","author":"Kim","year":"1994","journal-title":"Mol Biol Cell"},{"key":"2022011315271229000_bib23","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1016\/j.exer.2004.02.010","article-title":"Distribution of syndecans 1\u20134 within the anterior segment of the human eye: Expression of a variant syndecan-3 and matrix-associated syndecan-2","volume":"79","author":"Filla","year":"2004","journal-title":"Exp Eye Res"},{"key":"2022011315271229000_bib24","doi-asserted-by":"crossref","first-page":"374","DOI":"10.1002\/bies.20009","article-title":"Anterior eye development and ocular mesenchyme: New insights from mouse models and human diseases","volume":"26","author":"Cvekl","year":"2004","journal-title":"Bioessays"},{"key":"2022011315271229000_bib25","doi-asserted-by":"crossref","first-page":"4435","DOI":"10.1242\/dev.129.19.4435","article-title":"BMP signaling is required for development of the ciliary body","volume":"129","author":"Zhao","year":"2002","journal-title":"Development"},{"key":"2022011315271229000_bib26","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1002\/dvdy.10298","article-title":"Localisation of specific heparan sulfate proteoglycans during the proliferative phase of brain development","volume":"227","author":"Ford-Perriss","year":"2003","journal-title":"Dev Dyn"},{"key":"2022011315271229000_bib27","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1002\/ijc.2910310104","article-title":"Production of a mouse monoclonal antibody reactive with a human nuclear antigen associated with cell proliferation","volume":"31","author":"Gerdes","year":"1983","journal-title":"Int J Cancer"},{"key":"2022011315271229000_bib28","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1016\/S0012-1606(03)00178-7","article-title":"Growth factors induce neurogenesis in the ciliary body","volume":"259","author":"Fischer","year":"2003","journal-title":"Dev Biol"},{"key":"2022011315271229000_bib29","doi-asserted-by":"crossref","first-page":"2203","DOI":"10.1242\/dev.124.11.2203","article-title":"Bone morphogenetic proteins (BMPs) are regulators of dorsal forebrain development","volume":"124","author":"Furuta","year":"1997","journal-title":"Development"},{"key":"2022011315271229000_bib30","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1016\/S0925-4773(00)00467-6","article-title":"Transgenically ectopic expression of Bmp4 to the Msx1 mutant dental mesenchyme restores downstream gene expression but represses Shh and Bmp2 in the enamel knot of wild type tooth germ","volume":"99","author":"Zhao","year":"2000","journal-title":"Mech Dev"}],"container-title":["Stem Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1634%2Fstemcells.2008-0303","content-type":"unspecified","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1634\/stemcells.2008-0303","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1634\/stemcells.2008-0303","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/academic.oup.com\/stmcls\/article-pdf\/26\/12\/3162\/41944779\/stmcls_26_12_3162.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/stmcls\/article-pdf\/26\/12\/3162\/41944779\/stmcls_26_12_3162.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,1,19]],"date-time":"2022-01-19T02:56:02Z","timestamp":1642560962000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/stmcls\/article\/26\/12\/3162-3171\/6403037"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2008,9,11]]},"references-count":30,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2008,9,11]]},"published-print":{"date-parts":[[2008,12,1]]}},"URL":"https:\/\/doi.org\/10.1634\/stemcells.2008-0303","relation":{},"ISSN":["1066-5099","1549-4918"],"issn-type":[{"value":"1066-5099","type":"print"},{"value":"1549-4918","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2008,12,1]]},"published":{"date-parts":[[2008,9,11]]}}}