BMP/SMAD signaling regulates the cell behaviors that drive the initial dorsal-specific regional morphogenesis of the otocyst
During development of the otocyst, regional morphogenesis establishes a dorsal vestibular chamber and a ventral auditory chamber, which collectively constitute the membranous labyrinth of the inner ear. We identified the earliest morphogenetic event heralding the formation of the vestibular chamber,...
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description | During development of the otocyst, regional morphogenesis establishes a dorsal vestibular chamber and a ventral auditory chamber, which collectively constitute the membranous labyrinth of the inner ear. We identified the earliest morphogenetic event heralding the formation of the vestibular chamber, a rapid thinning and expansion of the dorsolateral wall of the otocyst, and showed that this process is generated by changes in otocyst cell shape from columnar to squamous, as opposed to changes in other cell behaviors, such as localized changes in cell proliferation or cell death. Moreover, we showed that thinning and expansion of the dorsolateral otocyst is regulated by BMP/SMAD signaling, which is both sufficient and necessary for localized thinning and expansion. Finally, we showed that BMP/SMAD signaling causes fragmentation of E-cadherin in the dorsolateral otocyst, occurring concomitantly with cell shape change, suggesting that BMP/SMAD signaling regulates cell–cell adhesion during the initial morphogenesis of the otocyst epithelium. Collectively, our results show that BMP signaling via SMADs regulates the cell behaviors that drive the initial dorsal-specific morphogenesis of the otocyst, providing new information about how regional morphogenesis of a complex organ rudiment, the developing membranous labyrinth, is initiated. |
doi_str_mv | 10.1016/j.ydbio.2010.09.002 |
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We identified the earliest morphogenetic event heralding the formation of the vestibular chamber, a rapid thinning and expansion of the dorsolateral wall of the otocyst, and showed that this process is generated by changes in otocyst cell shape from columnar to squamous, as opposed to changes in other cell behaviors, such as localized changes in cell proliferation or cell death. Moreover, we showed that thinning and expansion of the dorsolateral otocyst is regulated by BMP/SMAD signaling, which is both sufficient and necessary for localized thinning and expansion. Finally, we showed that BMP/SMAD signaling causes fragmentation of E-cadherin in the dorsolateral otocyst, occurring concomitantly with cell shape change, suggesting that BMP/SMAD signaling regulates cell–cell adhesion during the initial morphogenesis of the otocyst epithelium. Collectively, our results show that BMP signaling via SMADs regulates the cell behaviors that drive the initial dorsal-specific morphogenesis of the otocyst, providing new information about how regional morphogenesis of a complex organ rudiment, the developing membranous labyrinth, is initiated.</description><identifier>ISSN: 0012-1606</identifier><identifier>EISSN: 1095-564X</identifier><identifier>DOI: 10.1016/j.ydbio.2010.09.002</identifier><identifier>PMID: 20837004</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Base Sequence ; BMP ; Body Patterning ; Bone Morphogenetic Protein Receptors - genetics ; Bone Morphogenetic Protein Receptors - metabolism ; Bone Morphogenetic Proteins - genetics ; Bone Morphogenetic Proteins - metabolism ; Cadherins - metabolism ; Cell Proliferation ; Cell Shape ; DNA Primers - genetics ; E-cadherin ; Ear, Inner - cytology ; Ear, Inner - embryology ; Ear, Inner - metabolism ; Female ; Gene Expression Regulation, Developmental ; Guinea Pigs ; Inner ear ; Mice ; Morphogenesis ; Otic vesicle ; Patterning ; Pregnancy ; Signal Transduction ; SMAD ; Smad Proteins - genetics ; Smad Proteins - metabolism</subject><ispartof>Developmental biology, 2010-11, Vol.347 (2), p.369-381</ispartof><rights>2010 Elsevier Inc.</rights><rights>Copyright © 2010 Elsevier Inc. All rights reserved.</rights><rights>2010 Elsevier Inc. All rights reserved. 2010</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c458t-4e2bd958cc65e6d60ae641c55dc9b563318c51024e68e5b57ac1f7bac42818ba3</citedby><cites>FETCH-LOGICAL-c458t-4e2bd958cc65e6d60ae641c55dc9b563318c51024e68e5b57ac1f7bac42818ba3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ydbio.2010.09.002$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3536,27903,27904,45974</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20837004$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ohta, Sho</creatorcontrib><creatorcontrib>Mansour, Suzanne L.</creatorcontrib><creatorcontrib>Schoenwolf, Gary C.</creatorcontrib><title>BMP/SMAD signaling regulates the cell behaviors that drive the initial dorsal-specific regional morphogenesis of the otocyst</title><title>Developmental biology</title><addtitle>Dev Biol</addtitle><description>During development of the otocyst, regional morphogenesis establishes a dorsal vestibular chamber and a ventral auditory chamber, which collectively constitute the membranous labyrinth of the inner ear. We identified the earliest morphogenetic event heralding the formation of the vestibular chamber, a rapid thinning and expansion of the dorsolateral wall of the otocyst, and showed that this process is generated by changes in otocyst cell shape from columnar to squamous, as opposed to changes in other cell behaviors, such as localized changes in cell proliferation or cell death. Moreover, we showed that thinning and expansion of the dorsolateral otocyst is regulated by BMP/SMAD signaling, which is both sufficient and necessary for localized thinning and expansion. Finally, we showed that BMP/SMAD signaling causes fragmentation of E-cadherin in the dorsolateral otocyst, occurring concomitantly with cell shape change, suggesting that BMP/SMAD signaling regulates cell–cell adhesion during the initial morphogenesis of the otocyst epithelium. Collectively, our results show that BMP signaling via SMADs regulates the cell behaviors that drive the initial dorsal-specific morphogenesis of the otocyst, providing new information about how regional morphogenesis of a complex organ rudiment, the developing membranous labyrinth, is initiated.</description><subject>Animals</subject><subject>Base Sequence</subject><subject>BMP</subject><subject>Body Patterning</subject><subject>Bone Morphogenetic Protein Receptors - genetics</subject><subject>Bone Morphogenetic Protein Receptors - metabolism</subject><subject>Bone Morphogenetic Proteins - genetics</subject><subject>Bone Morphogenetic Proteins - metabolism</subject><subject>Cadherins - metabolism</subject><subject>Cell Proliferation</subject><subject>Cell Shape</subject><subject>DNA Primers - genetics</subject><subject>E-cadherin</subject><subject>Ear, Inner - cytology</subject><subject>Ear, Inner - embryology</subject><subject>Ear, Inner - metabolism</subject><subject>Female</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Guinea Pigs</subject><subject>Inner ear</subject><subject>Mice</subject><subject>Morphogenesis</subject><subject>Otic vesicle</subject><subject>Patterning</subject><subject>Pregnancy</subject><subject>Signal Transduction</subject><subject>SMAD</subject><subject>Smad Proteins - genetics</subject><subject>Smad Proteins - metabolism</subject><issn>0012-1606</issn><issn>1095-564X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UU2P0zAQtRArthR-ARLKjVO6Yyd2kwNIy8IC0q5AAiRuluNM0qnSuNhupUr8-HXaZcVeOI0072NG7zH2isOCA1cX68WhbcgtBKQN1AsA8YTNONQyl6r89ZTNALjIuQJ1zp6HsAaAoqqKZ-xcQFUsAcoZ-_P-9tvF99vLD1mgfjQDjX3msd8NJmLI4gozi8OQNbgye3J-WpmYtZ72eERppEhmyNqEmSEPW7TUkZ08yCW_bOP8duV6HDFQyFx3VLno7CHEF-ysM0PAl_dzzn5ef_xx9Tm_-frpy9XlTW5LWcW8RNG0taysVRJVq8CgKrmVsrV1I1VR8MpKDqJEVaFs5NJY3i0bY0tR8aoxxZy9O_lud80GW4tj9GbQW08b4w_aGdKPkZFWund7LWolSimSwZt7A-9-7zBEvaEwBWNGdLugl7IuEjHlO2fFiWm9C8Fj93CFg55q02t9rE1PtWmodaotqV7_--CD5m9PifD2RMAU057Q62AJR4stebRRt47-e-AOXgGtlQ</recordid><startdate>20101115</startdate><enddate>20101115</enddate><creator>Ohta, Sho</creator><creator>Mansour, Suzanne L.</creator><creator>Schoenwolf, Gary C.</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>5PM</scope></search><sort><creationdate>20101115</creationdate><title>BMP/SMAD signaling regulates the cell behaviors that drive the initial dorsal-specific regional morphogenesis of the otocyst</title><author>Ohta, Sho ; Mansour, Suzanne L. ; Schoenwolf, Gary C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c458t-4e2bd958cc65e6d60ae641c55dc9b563318c51024e68e5b57ac1f7bac42818ba3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Animals</topic><topic>Base Sequence</topic><topic>BMP</topic><topic>Body Patterning</topic><topic>Bone Morphogenetic Protein Receptors - genetics</topic><topic>Bone Morphogenetic Protein Receptors - metabolism</topic><topic>Bone Morphogenetic Proteins - genetics</topic><topic>Bone Morphogenetic Proteins - metabolism</topic><topic>Cadherins - metabolism</topic><topic>Cell Proliferation</topic><topic>Cell Shape</topic><topic>DNA Primers - genetics</topic><topic>E-cadherin</topic><topic>Ear, Inner - cytology</topic><topic>Ear, Inner - embryology</topic><topic>Ear, Inner - metabolism</topic><topic>Female</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Guinea Pigs</topic><topic>Inner ear</topic><topic>Mice</topic><topic>Morphogenesis</topic><topic>Otic vesicle</topic><topic>Patterning</topic><topic>Pregnancy</topic><topic>Signal Transduction</topic><topic>SMAD</topic><topic>Smad Proteins - genetics</topic><topic>Smad Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ohta, Sho</creatorcontrib><creatorcontrib>Mansour, Suzanne L.</creatorcontrib><creatorcontrib>Schoenwolf, Gary C.</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>PubMed Central (Full Participant titles)</collection><jtitle>Developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ohta, Sho</au><au>Mansour, Suzanne L.</au><au>Schoenwolf, Gary C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>BMP/SMAD signaling regulates the cell behaviors that drive the initial dorsal-specific regional morphogenesis of the otocyst</atitle><jtitle>Developmental biology</jtitle><addtitle>Dev Biol</addtitle><date>2010-11-15</date><risdate>2010</risdate><volume>347</volume><issue>2</issue><spage>369</spage><epage>381</epage><pages>369-381</pages><issn>0012-1606</issn><eissn>1095-564X</eissn><abstract>During development of the otocyst, regional morphogenesis establishes a dorsal vestibular chamber and a ventral auditory chamber, which collectively constitute the membranous labyrinth of the inner ear. We identified the earliest morphogenetic event heralding the formation of the vestibular chamber, a rapid thinning and expansion of the dorsolateral wall of the otocyst, and showed that this process is generated by changes in otocyst cell shape from columnar to squamous, as opposed to changes in other cell behaviors, such as localized changes in cell proliferation or cell death. Moreover, we showed that thinning and expansion of the dorsolateral otocyst is regulated by BMP/SMAD signaling, which is both sufficient and necessary for localized thinning and expansion. Finally, we showed that BMP/SMAD signaling causes fragmentation of E-cadherin in the dorsolateral otocyst, occurring concomitantly with cell shape change, suggesting that BMP/SMAD signaling regulates cell–cell adhesion during the initial morphogenesis of the otocyst epithelium. Collectively, our results show that BMP signaling via SMADs regulates the cell behaviors that drive the initial dorsal-specific morphogenesis of the otocyst, providing new information about how regional morphogenesis of a complex organ rudiment, the developing membranous labyrinth, is initiated.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>20837004</pmid><doi>10.1016/j.ydbio.2010.09.002</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Base Sequence BMP Body Patterning Bone Morphogenetic Protein Receptors - genetics Bone Morphogenetic Protein Receptors - metabolism Bone Morphogenetic Proteins - genetics Bone Morphogenetic Proteins - metabolism Cadherins - metabolism Cell Proliferation Cell Shape DNA Primers - genetics E-cadherin Ear, Inner - cytology Ear, Inner - embryology Ear, Inner - metabolism Female Gene Expression Regulation, Developmental Guinea Pigs Inner ear Mice Morphogenesis Otic vesicle Patterning Pregnancy Signal Transduction SMAD Smad Proteins - genetics Smad Proteins - metabolism |
title | BMP/SMAD signaling regulates the cell behaviors that drive the initial dorsal-specific regional morphogenesis of the otocyst |
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