The cochlear sensory epithelium derives from Wnt responsive cells in the dorsomedial otic cup
Wnt1 and Wnt3a secreted from the dorsal neural tube were previously shown to regulate a gene expression program in the dorsal otic vesicle that is necessary for vestibular morphogenesis (Riccomagno et al., 2005. Genes Dev. 19, 1612–1623). Unexpectedly, Wnt1−/−; Wnt3a−/− embryos also displayed a pron...
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| Veröffentlicht in: | Developmental biology 2015-03, Vol.399 (1), p.177-187 |
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| description | Wnt1 and Wnt3a secreted from the dorsal neural tube were previously shown to regulate a gene expression program in the dorsal otic vesicle that is necessary for vestibular morphogenesis (Riccomagno et al., 2005. Genes Dev. 19, 1612–1623). Unexpectedly, Wnt1−/−; Wnt3a−/− embryos also displayed a pronounced defect in the outgrowth of the ventrally derived cochlear duct. To determine how Wnt signaling in the dorsal otocyst contributes to cochlear development we performed a series of genetic fate mapping experiments using two independent Wnt responsive driver strains (TopCreER and Gbx2CreER) that when crossed to inducible responder lines (RosalacZ or RosazsGreen) permanently labeled dorsomedial otic progenitors and their derivatives. Tamoxifen time course experiments revealed that most vestibular structures showed some degree of labeling when recombination was induced between E7.75 and E12.5, consistent with continuous Wnt signaling activity in this tissue. Remarkably, a population of Wnt responsive cells in the dorsal otocyst was also found to contribute to the sensory epithelium of the cochlear duct, including auditory hair and support cells. Similar results were observed with both TopCreER and Gbx2CreER strains. The ventral displacement of Wnt responsive cells followed a spatiotemporal sequence that initiated in the anterior otic cup at, or immediately prior to, the 17-somite stage (E9) and then spread progressively to the posterior pole of the otic vesicle by the 25-somite stage (E9.5). These lineage-tracing experiments identify the earliest known origin of auditory sensory progenitors within a population of Wnt responsive cells in the dorsomedial otic cup.
•Wnt responsive cells in the dorsomedial otic cup contribute to both vestibular and auditory progenitors.•TopCreER; RosaZsGreen labeled cells mark the earliest known origin of auditory hair cells.•Ventral displacement of Wnt responsive progenitors proceeds in an anteroposterior direction. |
| doi_str_mv | 10.1016/j.ydbio.2015.01.001 |
| format | Article |
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•Wnt responsive cells in the dorsomedial otic cup contribute to both vestibular and auditory progenitors.•TopCreER; RosaZsGreen labeled cells mark the earliest known origin of auditory hair cells.•Ventral displacement of Wnt responsive progenitors proceeds in an anteroposterior direction.</description><identifier>ISSN: 0012-1606</identifier><identifier>EISSN: 1095-564X</identifier><identifier>DOI: 10.1016/j.ydbio.2015.01.001</identifier><identifier>PMID: 25592224</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Cell Lineage - genetics ; Cell Movement - genetics ; Cell Proliferation - genetics ; Cochlea ; Cochlea - cytology ; Cochlea - embryology ; Cochlea - metabolism ; Ear, Inner - cytology ; Ear, Inner - embryology ; Ear, Inner - metabolism ; Embryo, Mammalian - drug effects ; Embryo, Mammalian - embryology ; Embryo, Mammalian - metabolism ; epithelium ; Epithelium - embryology ; Epithelium - metabolism ; Estrogen Antagonists - pharmacology ; Fate map ; Female ; gene expression ; Gene Expression Regulation, Developmental ; genes ; Green Fluorescent Proteins - genetics ; Green Fluorescent Proteins - metabolism ; Immunohistochemistry ; In Situ Hybridization ; Inner ear ; Male ; Mice, Transgenic ; Microscopy, Confocal ; morphogenesis ; Morphogenesis - drug effects ; Morphogenesis - genetics ; Sensory progenitors ; tamoxifen ; Tamoxifen - pharmacology ; Time Factors ; Wnt signaling ; Wnt Signaling Pathway - genetics</subject><ispartof>Developmental biology, 2015-03, Vol.399 (1), p.177-187</ispartof><rights>2015 Elsevier Inc.</rights><rights>Copyright © 2015 Elsevier Inc. All rights reserved.</rights><rights>2015 Elsevier Inc. All rights reserved. 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c562t-9d0e1c538da20e7fcbe9cbbbfa02fc33baaf8e84855c95c7c613caa4276593673</citedby><cites>FETCH-LOGICAL-c562t-9d0e1c538da20e7fcbe9cbbbfa02fc33baaf8e84855c95c7c613caa4276593673</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S001216061500007X$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25592224$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Brown, Alexander S.</creatorcontrib><creatorcontrib>Rakowiecki, Staci M.</creatorcontrib><creatorcontrib>Li, James Y.H.</creatorcontrib><creatorcontrib>Epstein, Douglas J.</creatorcontrib><title>The cochlear sensory epithelium derives from Wnt responsive cells in the dorsomedial otic cup</title><title>Developmental biology</title><addtitle>Dev Biol</addtitle><description>Wnt1 and Wnt3a secreted from the dorsal neural tube were previously shown to regulate a gene expression program in the dorsal otic vesicle that is necessary for vestibular morphogenesis (Riccomagno et al., 2005. Genes Dev. 19, 1612–1623). Unexpectedly, Wnt1−/−; Wnt3a−/− embryos also displayed a pronounced defect in the outgrowth of the ventrally derived cochlear duct. To determine how Wnt signaling in the dorsal otocyst contributes to cochlear development we performed a series of genetic fate mapping experiments using two independent Wnt responsive driver strains (TopCreER and Gbx2CreER) that when crossed to inducible responder lines (RosalacZ or RosazsGreen) permanently labeled dorsomedial otic progenitors and their derivatives. Tamoxifen time course experiments revealed that most vestibular structures showed some degree of labeling when recombination was induced between E7.75 and E12.5, consistent with continuous Wnt signaling activity in this tissue. Remarkably, a population of Wnt responsive cells in the dorsal otocyst was also found to contribute to the sensory epithelium of the cochlear duct, including auditory hair and support cells. Similar results were observed with both TopCreER and Gbx2CreER strains. The ventral displacement of Wnt responsive cells followed a spatiotemporal sequence that initiated in the anterior otic cup at, or immediately prior to, the 17-somite stage (E9) and then spread progressively to the posterior pole of the otic vesicle by the 25-somite stage (E9.5). These lineage-tracing experiments identify the earliest known origin of auditory sensory progenitors within a population of Wnt responsive cells in the dorsomedial otic cup.
•Wnt responsive cells in the dorsomedial otic cup contribute to both vestibular and auditory progenitors.•TopCreER; RosaZsGreen labeled cells mark the earliest known origin of auditory hair cells.•Ventral displacement of Wnt responsive progenitors proceeds in an anteroposterior direction.</description><subject>Animals</subject><subject>Cell Lineage - genetics</subject><subject>Cell Movement - genetics</subject><subject>Cell Proliferation - genetics</subject><subject>Cochlea</subject><subject>Cochlea - cytology</subject><subject>Cochlea - embryology</subject><subject>Cochlea - metabolism</subject><subject>Ear, Inner - cytology</subject><subject>Ear, Inner - embryology</subject><subject>Ear, Inner - metabolism</subject><subject>Embryo, Mammalian - drug effects</subject><subject>Embryo, Mammalian - embryology</subject><subject>Embryo, Mammalian - metabolism</subject><subject>epithelium</subject><subject>Epithelium - embryology</subject><subject>Epithelium - metabolism</subject><subject>Estrogen Antagonists - pharmacology</subject><subject>Fate map</subject><subject>Female</subject><subject>gene expression</subject><subject>Gene Expression Regulation, Developmental</subject><subject>genes</subject><subject>Green Fluorescent Proteins - genetics</subject><subject>Green Fluorescent Proteins - metabolism</subject><subject>Immunohistochemistry</subject><subject>In Situ Hybridization</subject><subject>Inner ear</subject><subject>Male</subject><subject>Mice, Transgenic</subject><subject>Microscopy, Confocal</subject><subject>morphogenesis</subject><subject>Morphogenesis - drug effects</subject><subject>Morphogenesis - genetics</subject><subject>Sensory progenitors</subject><subject>tamoxifen</subject><subject>Tamoxifen - pharmacology</subject><subject>Time Factors</subject><subject>Wnt signaling</subject><subject>Wnt Signaling Pathway - genetics</subject><issn>0012-1606</issn><issn>1095-564X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1v1DAQhi0EokvhFyAhH7kk-DvJASRUlQ-pEpei9oIsZzJhvUriYCcr7b-vly0VXMrJ0viZd2bel5DXnJWccfNuVx661odSMK5LxkvG-BOy4azRhTbq9inZ5IoouGHmjLxIaccYk3Utn5MzoXUjhFAb8uN6ixQCbAd0kSacUogHirNftjj4daQdRr_HRPsYRnozLTRimsOUcpECDkOifqIZpl2IKYzYeTfQsHigsM4vybPeDQlf3b_n5Puny-uLL8XVt89fLz5eFaCNWIqmY8hBy7pzgmHVQ4sNtG3bOyZ6kLJ1rq-xVrXW0GiowHAJzilRGd1IU8lz8uGkO69tXgFwWqIb7Bz96OLBBuftvz-T39qfYW-VlI1UKgu8vReI4deKabGjT8fz3IRhTVZkx6WquJb_RbnRteK1rk1G5QmFGFKK2D9sxJk9Zmh39neG9pihZdzmxHLXm7-Peej5E1oG3p8AzJbuPUabwOME2fuIsNgu-EcH3AGNCbEn</recordid><startdate>20150301</startdate><enddate>20150301</enddate><creator>Brown, Alexander S.</creator><creator>Rakowiecki, Staci M.</creator><creator>Li, James Y.H.</creator><creator>Epstein, Douglas J.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20150301</creationdate><title>The cochlear sensory epithelium derives from Wnt responsive cells in the dorsomedial otic cup</title><author>Brown, Alexander S. ; Rakowiecki, Staci M. ; Li, James Y.H. ; Epstein, Douglas J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c562t-9d0e1c538da20e7fcbe9cbbbfa02fc33baaf8e84855c95c7c613caa4276593673</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Cell Lineage - genetics</topic><topic>Cell Movement - genetics</topic><topic>Cell Proliferation - genetics</topic><topic>Cochlea</topic><topic>Cochlea - cytology</topic><topic>Cochlea - embryology</topic><topic>Cochlea - metabolism</topic><topic>Ear, Inner - cytology</topic><topic>Ear, Inner - embryology</topic><topic>Ear, Inner - metabolism</topic><topic>Embryo, Mammalian - drug effects</topic><topic>Embryo, Mammalian - embryology</topic><topic>Embryo, Mammalian - metabolism</topic><topic>epithelium</topic><topic>Epithelium - embryology</topic><topic>Epithelium - metabolism</topic><topic>Estrogen Antagonists - pharmacology</topic><topic>Fate map</topic><topic>Female</topic><topic>gene expression</topic><topic>Gene Expression Regulation, Developmental</topic><topic>genes</topic><topic>Green Fluorescent Proteins - genetics</topic><topic>Green Fluorescent Proteins - metabolism</topic><topic>Immunohistochemistry</topic><topic>In Situ Hybridization</topic><topic>Inner ear</topic><topic>Male</topic><topic>Mice, Transgenic</topic><topic>Microscopy, Confocal</topic><topic>morphogenesis</topic><topic>Morphogenesis - drug effects</topic><topic>Morphogenesis - genetics</topic><topic>Sensory progenitors</topic><topic>tamoxifen</topic><topic>Tamoxifen - pharmacology</topic><topic>Time Factors</topic><topic>Wnt signaling</topic><topic>Wnt Signaling Pathway - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Brown, Alexander S.</creatorcontrib><creatorcontrib>Rakowiecki, Staci M.</creatorcontrib><creatorcontrib>Li, James Y.H.</creatorcontrib><creatorcontrib>Epstein, Douglas J.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Brown, Alexander S.</au><au>Rakowiecki, Staci M.</au><au>Li, James Y.H.</au><au>Epstein, Douglas J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The cochlear sensory epithelium derives from Wnt responsive cells in the dorsomedial otic cup</atitle><jtitle>Developmental biology</jtitle><addtitle>Dev Biol</addtitle><date>2015-03-01</date><risdate>2015</risdate><volume>399</volume><issue>1</issue><spage>177</spage><epage>187</epage><pages>177-187</pages><issn>0012-1606</issn><eissn>1095-564X</eissn><abstract>Wnt1 and Wnt3a secreted from the dorsal neural tube were previously shown to regulate a gene expression program in the dorsal otic vesicle that is necessary for vestibular morphogenesis (Riccomagno et al., 2005. Genes Dev. 19, 1612–1623). Unexpectedly, Wnt1−/−; Wnt3a−/− embryos also displayed a pronounced defect in the outgrowth of the ventrally derived cochlear duct. To determine how Wnt signaling in the dorsal otocyst contributes to cochlear development we performed a series of genetic fate mapping experiments using two independent Wnt responsive driver strains (TopCreER and Gbx2CreER) that when crossed to inducible responder lines (RosalacZ or RosazsGreen) permanently labeled dorsomedial otic progenitors and their derivatives. Tamoxifen time course experiments revealed that most vestibular structures showed some degree of labeling when recombination was induced between E7.75 and E12.5, consistent with continuous Wnt signaling activity in this tissue. Remarkably, a population of Wnt responsive cells in the dorsal otocyst was also found to contribute to the sensory epithelium of the cochlear duct, including auditory hair and support cells. Similar results were observed with both TopCreER and Gbx2CreER strains. The ventral displacement of Wnt responsive cells followed a spatiotemporal sequence that initiated in the anterior otic cup at, or immediately prior to, the 17-somite stage (E9) and then spread progressively to the posterior pole of the otic vesicle by the 25-somite stage (E9.5). These lineage-tracing experiments identify the earliest known origin of auditory sensory progenitors within a population of Wnt responsive cells in the dorsomedial otic cup.
•Wnt responsive cells in the dorsomedial otic cup contribute to both vestibular and auditory progenitors.•TopCreER; RosaZsGreen labeled cells mark the earliest known origin of auditory hair cells.•Ventral displacement of Wnt responsive progenitors proceeds in an anteroposterior direction.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>25592224</pmid><doi>10.1016/j.ydbio.2015.01.001</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Cell Lineage - genetics Cell Movement - genetics Cell Proliferation - genetics Cochlea Cochlea - cytology Cochlea - embryology Cochlea - metabolism Ear, Inner - cytology Ear, Inner - embryology Ear, Inner - metabolism Embryo, Mammalian - drug effects Embryo, Mammalian - embryology Embryo, Mammalian - metabolism epithelium Epithelium - embryology Epithelium - metabolism Estrogen Antagonists - pharmacology Fate map Female gene expression Gene Expression Regulation, Developmental genes Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Immunohistochemistry In Situ Hybridization Inner ear Male Mice, Transgenic Microscopy, Confocal morphogenesis Morphogenesis - drug effects Morphogenesis - genetics Sensory progenitors tamoxifen Tamoxifen - pharmacology Time Factors Wnt signaling Wnt Signaling Pathway - genetics |
| title | The cochlear sensory epithelium derives from Wnt responsive cells in the dorsomedial otic cup |
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