Requirement for frzb and fzd7a in cranial neural crest convergence and extension mechanisms during zebrafish palate and jaw morphogenesis
Regulation of convergence and extension by wnt-frizzled signaling is a common theme in embryogenesis. This study examines the functional requirements of frzb and fzd7a in convergence and extension mechanisms during craniofacial development. Using a morpholino knockdown approach, we found that frzb a...
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creator | Kamel, George Hoyos, Tatiana Rochard, Lucie Dougherty, Max Kong, Yawei Tse, William Shubinets, Valeriy Grimaldi, Michael Liao, Eric C. |
description | Regulation of convergence and extension by wnt-frizzled signaling is a common theme in embryogenesis. This study examines the functional requirements of frzb and fzd7a in convergence and extension mechanisms during craniofacial development. Using a morpholino knockdown approach, we found that frzb and fzd7a are dispensable for directed migration of the bilateral trabeculae, but necessary for the convergence and extension of the palatal elements, where the extension process is mediated by chondrocyte proliferation, morphologic change and intercalation. In contrast, frzb and fzd7a are required for convergence of the mandibular prominences, where knockdown of either frzb or fzd7a resulted in complete loss of lower jaw structures. Further, we found that bapx1 was specifically downregulated in the wnt9a/frzb/fzd7a morphants, while general neural crest markers were unaffected. In addition, expression of wnt9a and frzb was also absent in the edn−/− mutant. Notably, over-expression of bapx1 was sufficient to partially rescue mandibular elements in the wnt9a/frzb/fzd7a morphants, demonstrating genetic epistasis of bapx1 acting downstream of edn1 and wnt9a/frzb/fzd7a in lower jaw development. This study underscores the important role of wnt-frizzled signaling in convergence and extension in palate and craniofacial morphogenesis, distinct regulation of upper vs. lower jaw structures, and integration of wnt-frizzled with endothelin signaling to coordinate shaping of the facial form.
•Bridges knowledge gap between cranial neural crest patterning and jaw morphogenesis.•Requirement for wnt-frizzled in craniofacial convergence and extension.•frzb, fzd7a and wnt9a are required for ethmoid plate extension.•Ethmoid plate extension involves cell proliferation, intercalation, and morphologic change.•frzb, fzd7a, and wnt9a are required for lower jaw convergence. |
doi_str_mv | 10.1016/j.ydbio.2013.06.012 |
format | Article |
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•Bridges knowledge gap between cranial neural crest patterning and jaw morphogenesis.•Requirement for wnt-frizzled in craniofacial convergence and extension.•frzb, fzd7a and wnt9a are required for ethmoid plate extension.•Ethmoid plate extension involves cell proliferation, intercalation, and morphologic change.•frzb, fzd7a, and wnt9a are required for lower jaw convergence.</description><identifier>ISSN: 0012-1606</identifier><identifier>EISSN: 1095-564X</identifier><identifier>DOI: 10.1016/j.ydbio.2013.06.012</identifier><identifier>PMID: 23806211</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Apoptosis ; Body Patterning ; Cell Proliferation ; Chondrocytes - metabolism ; Convergence extension ; Cranial neural crest ; Craniofacial ; Danio rerio ; Embryo, Nonmammalian - metabolism ; embryogenesis ; epistasis ; Epistasis, Genetic ; Freshwater ; frizzled ; frzb ; fzd7a ; Gene Expression Regulation, Developmental ; gene overexpression ; Glycoproteins - genetics ; Glycoproteins - metabolism ; HEK293 Cells ; Homeodomain Proteins - genetics ; Homeodomain Proteins - metabolism ; Humans ; Intracellular Signaling Peptides and Proteins ; Jaw - embryology ; Jaw - metabolism ; Morphogenesis ; mutants ; neural crest ; Neural Crest - embryology ; Neural Crest - metabolism ; palate ; Palate - growth & development ; Palate - metabolism ; Receptors, Cell Surface - genetics ; Receptors, Cell Surface - metabolism ; Transcription Factors - genetics ; Transcription Factors - metabolism ; wnt ; Wnt Proteins - genetics ; Wnt Proteins - metabolism ; Wnt9a ; Zebrafish ; Zebrafish - embryology ; Zebrafish - genetics ; Zebrafish - metabolism ; Zebrafish Proteins - genetics ; Zebrafish Proteins - metabolism</subject><ispartof>Developmental biology, 2013-09, Vol.381 (2), p.423-433</ispartof><rights>2013 Elsevier Inc.</rights><rights>Copyright © 2013 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c461t-3b1bb75b18ceb4b68c9b578e9d86d80400023227db9210de03a5eac2a7bd3763</citedby><cites>FETCH-LOGICAL-c461t-3b1bb75b18ceb4b68c9b578e9d86d80400023227db9210de03a5eac2a7bd3763</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.2013.06.012$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>315,782,786,3554,27933,27934,46004</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23806211$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kamel, George</creatorcontrib><creatorcontrib>Hoyos, Tatiana</creatorcontrib><creatorcontrib>Rochard, Lucie</creatorcontrib><creatorcontrib>Dougherty, Max</creatorcontrib><creatorcontrib>Kong, Yawei</creatorcontrib><creatorcontrib>Tse, William</creatorcontrib><creatorcontrib>Shubinets, Valeriy</creatorcontrib><creatorcontrib>Grimaldi, Michael</creatorcontrib><creatorcontrib>Liao, Eric C.</creatorcontrib><title>Requirement for frzb and fzd7a in cranial neural crest convergence and extension mechanisms during zebrafish palate and jaw morphogenesis</title><title>Developmental biology</title><addtitle>Dev Biol</addtitle><description>Regulation of convergence and extension by wnt-frizzled signaling is a common theme in embryogenesis. This study examines the functional requirements of frzb and fzd7a in convergence and extension mechanisms during craniofacial development. Using a morpholino knockdown approach, we found that frzb and fzd7a are dispensable for directed migration of the bilateral trabeculae, but necessary for the convergence and extension of the palatal elements, where the extension process is mediated by chondrocyte proliferation, morphologic change and intercalation. In contrast, frzb and fzd7a are required for convergence of the mandibular prominences, where knockdown of either frzb or fzd7a resulted in complete loss of lower jaw structures. Further, we found that bapx1 was specifically downregulated in the wnt9a/frzb/fzd7a morphants, while general neural crest markers were unaffected. In addition, expression of wnt9a and frzb was also absent in the edn−/− mutant. Notably, over-expression of bapx1 was sufficient to partially rescue mandibular elements in the wnt9a/frzb/fzd7a morphants, demonstrating genetic epistasis of bapx1 acting downstream of edn1 and wnt9a/frzb/fzd7a in lower jaw development. This study underscores the important role of wnt-frizzled signaling in convergence and extension in palate and craniofacial morphogenesis, distinct regulation of upper vs. lower jaw structures, and integration of wnt-frizzled with endothelin signaling to coordinate shaping of the facial form.
•Bridges knowledge gap between cranial neural crest patterning and jaw morphogenesis.•Requirement for wnt-frizzled in craniofacial convergence and extension.•frzb, fzd7a and wnt9a are required for ethmoid plate extension.•Ethmoid plate extension involves cell proliferation, intercalation, and morphologic change.•frzb, fzd7a, and wnt9a are required for lower jaw convergence.</description><subject>Animals</subject><subject>Apoptosis</subject><subject>Body Patterning</subject><subject>Cell Proliferation</subject><subject>Chondrocytes - metabolism</subject><subject>Convergence extension</subject><subject>Cranial neural crest</subject><subject>Craniofacial</subject><subject>Danio rerio</subject><subject>Embryo, Nonmammalian - metabolism</subject><subject>embryogenesis</subject><subject>epistasis</subject><subject>Epistasis, Genetic</subject><subject>Freshwater</subject><subject>frizzled</subject><subject>frzb</subject><subject>fzd7a</subject><subject>Gene Expression Regulation, Developmental</subject><subject>gene overexpression</subject><subject>Glycoproteins - genetics</subject><subject>Glycoproteins - metabolism</subject><subject>HEK293 Cells</subject><subject>Homeodomain Proteins - genetics</subject><subject>Homeodomain Proteins - metabolism</subject><subject>Humans</subject><subject>Intracellular Signaling Peptides and Proteins</subject><subject>Jaw - embryology</subject><subject>Jaw - metabolism</subject><subject>Morphogenesis</subject><subject>mutants</subject><subject>neural crest</subject><subject>Neural Crest - embryology</subject><subject>Neural Crest - metabolism</subject><subject>palate</subject><subject>Palate - growth & development</subject><subject>Palate - metabolism</subject><subject>Receptors, Cell Surface - genetics</subject><subject>Receptors, Cell Surface - metabolism</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><subject>wnt</subject><subject>Wnt Proteins - genetics</subject><subject>Wnt Proteins - metabolism</subject><subject>Wnt9a</subject><subject>Zebrafish</subject><subject>Zebrafish - embryology</subject><subject>Zebrafish - genetics</subject><subject>Zebrafish - metabolism</subject><subject>Zebrafish Proteins - genetics</subject><subject>Zebrafish Proteins - metabolism</subject><issn>0012-1606</issn><issn>1095-564X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkctu1DAUhi0EokPhCZDASzYJviSOs2CBKm5SJSQoEjvLl5MZjxJ7aieFzhvw1niawhJWR7K-_7ePP4SeU1JTQsXrfX3rjI81I5TXRNSEsgdoQ0nfVq1ovj9EG1KOKiqIOENPct4TQriU_DE6Y1wSwSjdoF9f4HrxCSYIMx5iwkM6GqyDw8PRdRr7gG3SwesRB1hSGTZBnrGN4QbSFoKFOxp-zhCyjwFPYHclkKeM3ZJ82OIjmKQHn3f4oEc9r4G9_oGnmA67WEog-_wUPRr0mOHZ_TxHV-_fXV18rC4_f_h08fayso2gc8UNNaZrDZUWTGOEtL1pOwm9k8JJ0pQlGWesc6ZnlDggXLegLdOdcbwT_By9WmsPKV4vZRU1-WxhHHWAuGRFW9Y0tCkd_0cbJlvaEyoLylfUpphzgkEdkp90ulWUqJMttVd3ttTJliJCFTUl9eL-gsVM4P5m_ugpwMsVGHRUept8Vt--lgZRtpQF6grxZiWgfNmNh6Sy9Scrrki1s3LR__MJvwEBs7JJ</recordid><startdate>20130915</startdate><enddate>20130915</enddate><creator>Kamel, George</creator><creator>Hoyos, Tatiana</creator><creator>Rochard, Lucie</creator><creator>Dougherty, Max</creator><creator>Kong, Yawei</creator><creator>Tse, William</creator><creator>Shubinets, Valeriy</creator><creator>Grimaldi, Michael</creator><creator>Liao, Eric C.</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</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>7TK</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope></search><sort><creationdate>20130915</creationdate><title>Requirement for frzb and fzd7a in cranial neural crest convergence and extension mechanisms during zebrafish palate and jaw morphogenesis</title><author>Kamel, George ; Hoyos, Tatiana ; Rochard, Lucie ; Dougherty, Max ; Kong, Yawei ; Tse, William ; Shubinets, Valeriy ; Grimaldi, Michael ; Liao, Eric C.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c461t-3b1bb75b18ceb4b68c9b578e9d86d80400023227db9210de03a5eac2a7bd3763</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Animals</topic><topic>Apoptosis</topic><topic>Body Patterning</topic><topic>Cell Proliferation</topic><topic>Chondrocytes - metabolism</topic><topic>Convergence extension</topic><topic>Cranial neural crest</topic><topic>Craniofacial</topic><topic>Danio rerio</topic><topic>Embryo, Nonmammalian - metabolism</topic><topic>embryogenesis</topic><topic>epistasis</topic><topic>Epistasis, Genetic</topic><topic>Freshwater</topic><topic>frizzled</topic><topic>frzb</topic><topic>fzd7a</topic><topic>Gene Expression Regulation, Developmental</topic><topic>gene overexpression</topic><topic>Glycoproteins - genetics</topic><topic>Glycoproteins - metabolism</topic><topic>HEK293 Cells</topic><topic>Homeodomain Proteins - genetics</topic><topic>Homeodomain Proteins - metabolism</topic><topic>Humans</topic><topic>Intracellular Signaling Peptides and Proteins</topic><topic>Jaw - embryology</topic><topic>Jaw - metabolism</topic><topic>Morphogenesis</topic><topic>mutants</topic><topic>neural crest</topic><topic>Neural Crest - embryology</topic><topic>Neural Crest - metabolism</topic><topic>palate</topic><topic>Palate - growth & development</topic><topic>Palate - metabolism</topic><topic>Receptors, Cell Surface - genetics</topic><topic>Receptors, Cell Surface - metabolism</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><topic>wnt</topic><topic>Wnt Proteins - genetics</topic><topic>Wnt Proteins - metabolism</topic><topic>Wnt9a</topic><topic>Zebrafish</topic><topic>Zebrafish - embryology</topic><topic>Zebrafish - genetics</topic><topic>Zebrafish - metabolism</topic><topic>Zebrafish Proteins - genetics</topic><topic>Zebrafish Proteins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kamel, George</creatorcontrib><creatorcontrib>Hoyos, Tatiana</creatorcontrib><creatorcontrib>Rochard, Lucie</creatorcontrib><creatorcontrib>Dougherty, Max</creatorcontrib><creatorcontrib>Kong, Yawei</creatorcontrib><creatorcontrib>Tse, William</creatorcontrib><creatorcontrib>Shubinets, Valeriy</creatorcontrib><creatorcontrib>Grimaldi, Michael</creatorcontrib><creatorcontrib>Liao, Eric C.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</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>Neurosciences Abstracts</collection><collection>ASFA: Aquatic Sciences and Fisheries Abstracts</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) 1: Biological Sciences & Living Resources</collection><collection>Aquatic Science & Fisheries Abstracts (ASFA) Professional</collection><jtitle>Developmental biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kamel, George</au><au>Hoyos, Tatiana</au><au>Rochard, Lucie</au><au>Dougherty, Max</au><au>Kong, Yawei</au><au>Tse, William</au><au>Shubinets, Valeriy</au><au>Grimaldi, Michael</au><au>Liao, Eric C.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Requirement for frzb and fzd7a in cranial neural crest convergence and extension mechanisms during zebrafish palate and jaw morphogenesis</atitle><jtitle>Developmental biology</jtitle><addtitle>Dev Biol</addtitle><date>2013-09-15</date><risdate>2013</risdate><volume>381</volume><issue>2</issue><spage>423</spage><epage>433</epage><pages>423-433</pages><issn>0012-1606</issn><eissn>1095-564X</eissn><abstract>Regulation of convergence and extension by wnt-frizzled signaling is a common theme in embryogenesis. This study examines the functional requirements of frzb and fzd7a in convergence and extension mechanisms during craniofacial development. Using a morpholino knockdown approach, we found that frzb and fzd7a are dispensable for directed migration of the bilateral trabeculae, but necessary for the convergence and extension of the palatal elements, where the extension process is mediated by chondrocyte proliferation, morphologic change and intercalation. In contrast, frzb and fzd7a are required for convergence of the mandibular prominences, where knockdown of either frzb or fzd7a resulted in complete loss of lower jaw structures. Further, we found that bapx1 was specifically downregulated in the wnt9a/frzb/fzd7a morphants, while general neural crest markers were unaffected. In addition, expression of wnt9a and frzb was also absent in the edn−/− mutant. Notably, over-expression of bapx1 was sufficient to partially rescue mandibular elements in the wnt9a/frzb/fzd7a morphants, demonstrating genetic epistasis of bapx1 acting downstream of edn1 and wnt9a/frzb/fzd7a in lower jaw development. This study underscores the important role of wnt-frizzled signaling in convergence and extension in palate and craniofacial morphogenesis, distinct regulation of upper vs. lower jaw structures, and integration of wnt-frizzled with endothelin signaling to coordinate shaping of the facial form.
•Bridges knowledge gap between cranial neural crest patterning and jaw morphogenesis.•Requirement for wnt-frizzled in craniofacial convergence and extension.•frzb, fzd7a and wnt9a are required for ethmoid plate extension.•Ethmoid plate extension involves cell proliferation, intercalation, and morphologic change.•frzb, fzd7a, and wnt9a are required for lower jaw convergence.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>23806211</pmid><doi>10.1016/j.ydbio.2013.06.012</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Apoptosis Body Patterning Cell Proliferation Chondrocytes - metabolism Convergence extension Cranial neural crest Craniofacial Danio rerio Embryo, Nonmammalian - metabolism embryogenesis epistasis Epistasis, Genetic Freshwater frizzled frzb fzd7a Gene Expression Regulation, Developmental gene overexpression Glycoproteins - genetics Glycoproteins - metabolism HEK293 Cells Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Humans Intracellular Signaling Peptides and Proteins Jaw - embryology Jaw - metabolism Morphogenesis mutants neural crest Neural Crest - embryology Neural Crest - metabolism palate Palate - growth & development Palate - metabolism Receptors, Cell Surface - genetics Receptors, Cell Surface - metabolism Transcription Factors - genetics Transcription Factors - metabolism wnt Wnt Proteins - genetics Wnt Proteins - metabolism Wnt9a Zebrafish Zebrafish - embryology Zebrafish - genetics Zebrafish - metabolism Zebrafish Proteins - genetics Zebrafish Proteins - metabolism |
title | Requirement for frzb and fzd7a in cranial neural crest convergence and extension mechanisms during zebrafish palate and jaw morphogenesis |
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