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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Veröffentlicht in:Developmental biology 2013-09, Vol.381 (2), p.423-433
Hauptverfasser: Kamel, George, Hoyos, Tatiana, Rochard, Lucie, Dougherty, Max, Kong, Yawei, Tse, William, Shubinets, Valeriy, Grimaldi, Michael, Liao, Eric C.
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container_end_page 433
container_issue 2
container_start_page 423
container_title Developmental biology
container_volume 381
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
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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. 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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 &amp; 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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 &amp; 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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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