High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities
The neural crest (NC) is a vertebrate innovation that distinguishes vertebrates from other chordates and was critical for the development and evolution of a "New Head and Brain." In early vertebrates, the NC was the source of dermal armor of fossil jawless fish. In extant vertebrates, incl...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2009-06, Vol.106 (22), p.8947-8952 |
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| creator | Calloni, Giordano W Le Douarin, Nicole M Dupin, Elisabeth |
| description | The neural crest (NC) is a vertebrate innovation that distinguishes vertebrates from other chordates and was critical for the development and evolution of a "New Head and Brain." In early vertebrates, the NC was the source of dermal armor of fossil jawless fish. In extant vertebrates, including mammals, the NC forms the peripheral nervous system, melanocytes, and the cartilage and bone of the face. Here, we show that in avian embryos, a large majority of cephalic NC cells (CNCCs) have the ability to differentiate into cell types as diverse as neurons, melanocytes, osteocytes, and chondrocytes. Moreover, we find that the morphogen Sonic hedgehog (Shh) acts on CNCCs to increase endochondral osteogenesis while having no effect on osteoblasts prone to membranous ossification. We have developed culture conditions that demonstrate that "neural-mesenchymal" differentiation abilities are present in more than 90% of CNCCs. A highly multipotent progenitor (able to yield neurons, glia, melanocytes, myofibroblasts, chondrocytes, and osteocytes) comprises 7-13% of the clonogenic cells in the absence and presence of Shh, respectively. This progenitor is a good candidate for a cephalic NC stem cell. |
| doi_str_mv | 10.1073/pnas.0903780106 |
| format | Article |
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In early vertebrates, the NC was the source of dermal armor of fossil jawless fish. In extant vertebrates, including mammals, the NC forms the peripheral nervous system, melanocytes, and the cartilage and bone of the face. Here, we show that in avian embryos, a large majority of cephalic NC cells (CNCCs) have the ability to differentiate into cell types as diverse as neurons, melanocytes, osteocytes, and chondrocytes. Moreover, we find that the morphogen Sonic hedgehog (Shh) acts on CNCCs to increase endochondral osteogenesis while having no effect on osteoblasts prone to membranous ossification. We have developed culture conditions that demonstrate that "neural-mesenchymal" differentiation abilities are present in more than 90% of CNCCs. A highly multipotent progenitor (able to yield neurons, glia, melanocytes, myofibroblasts, chondrocytes, and osteocytes) comprises 7-13% of the clonogenic cells in the absence and presence of Shh, respectively. This progenitor is a good candidate for a cephalic NC stem cell.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.0903780106</identifier><identifier>PMID: 19447928</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Biological Sciences ; Bones ; Brain - cytology ; Brain - metabolism ; Cell Differentiation ; Chondrocytes ; Chordata ; Core Binding Factor Alpha 1 Subunit - genetics ; Core Binding Factor Alpha 1 Subunit - metabolism ; Cultured cells ; Embryos ; Gene Expression - drug effects ; Hedgehog Proteins - metabolism ; Hedgehog Proteins - pharmacology ; Melanocytes - cytology ; Mesenchymal stem cells ; Multipotent stem cells ; Multipotent Stem Cells - cytology ; Neural Crest - cytology ; Neural stem cells ; Neurogenesis ; Neuroglia ; Neurons ; Oncogene Proteins - genetics ; Osteoblasts ; Osteogenesis ; Progenitor cells ; Quail ; Stem cells ; Trans-Activators - genetics ; Vertebrates ; Zinc Finger Protein GLI1</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2009-06, Vol.106 (22), p.8947-8952</ispartof><rights>Copyright 1993-2008 National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Jun 2, 2009</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c618t-35df91ffab8276e4ce29058af0d9cfcbb6f75265962070cdd33e2afc42a12d593</citedby><cites>FETCH-LOGICAL-c618t-35df91ffab8276e4ce29058af0d9cfcbb6f75265962070cdd33e2afc42a12d593</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/106/22.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/40482794$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/40482794$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19447928$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Calloni, Giordano W</creatorcontrib><creatorcontrib>Le Douarin, Nicole M</creatorcontrib><creatorcontrib>Dupin, Elisabeth</creatorcontrib><title>High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The neural crest (NC) is a vertebrate innovation that distinguishes vertebrates from other chordates and was critical for the development and evolution of a "New Head and Brain." 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Le Douarin, Nicole M ; Dupin, Elisabeth</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c618t-35df91ffab8276e4ce29058af0d9cfcbb6f75265962070cdd33e2afc42a12d593</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Animals</topic><topic>Biological Sciences</topic><topic>Bones</topic><topic>Brain - cytology</topic><topic>Brain - metabolism</topic><topic>Cell Differentiation</topic><topic>Chondrocytes</topic><topic>Chordata</topic><topic>Core Binding Factor Alpha 1 Subunit - genetics</topic><topic>Core Binding Factor Alpha 1 Subunit - metabolism</topic><topic>Cultured cells</topic><topic>Embryos</topic><topic>Gene Expression - drug effects</topic><topic>Hedgehog Proteins - metabolism</topic><topic>Hedgehog Proteins - pharmacology</topic><topic>Melanocytes - cytology</topic><topic>Mesenchymal stem cells</topic><topic>Multipotent stem cells</topic><topic>Multipotent Stem Cells - cytology</topic><topic>Neural Crest - cytology</topic><topic>Neural stem cells</topic><topic>Neurogenesis</topic><topic>Neuroglia</topic><topic>Neurons</topic><topic>Oncogene Proteins - genetics</topic><topic>Osteoblasts</topic><topic>Osteogenesis</topic><topic>Progenitor cells</topic><topic>Quail</topic><topic>Stem cells</topic><topic>Trans-Activators - genetics</topic><topic>Vertebrates</topic><topic>Zinc Finger Protein GLI1</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Calloni, Giordano W</creatorcontrib><creatorcontrib>Le Douarin, Nicole M</creatorcontrib><creatorcontrib>Dupin, Elisabeth</creatorcontrib><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>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Calloni, Giordano W</au><au>Le Douarin, Nicole M</au><au>Dupin, Elisabeth</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2009-06-02</date><risdate>2009</risdate><volume>106</volume><issue>22</issue><spage>8947</spage><epage>8952</epage><pages>8947-8952</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>The neural crest (NC) is a vertebrate innovation that distinguishes vertebrates from other chordates and was critical for the development and evolution of a "New Head and Brain." In early vertebrates, the NC was the source of dermal armor of fossil jawless fish. In extant vertebrates, including mammals, the NC forms the peripheral nervous system, melanocytes, and the cartilage and bone of the face. Here, we show that in avian embryos, a large majority of cephalic NC cells (CNCCs) have the ability to differentiate into cell types as diverse as neurons, melanocytes, osteocytes, and chondrocytes. Moreover, we find that the morphogen Sonic hedgehog (Shh) acts on CNCCs to increase endochondral osteogenesis while having no effect on osteoblasts prone to membranous ossification. We have developed culture conditions that demonstrate that "neural-mesenchymal" differentiation abilities are present in more than 90% of CNCCs. A highly multipotent progenitor (able to yield neurons, glia, melanocytes, myofibroblasts, chondrocytes, and osteocytes) comprises 7-13% of the clonogenic cells in the absence and presence of Shh, respectively. This progenitor is a good candidate for a cephalic NC stem cell.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>19447928</pmid><doi>10.1073/pnas.0903780106</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biological Sciences Bones Brain - cytology Brain - metabolism Cell Differentiation Chondrocytes Chordata Core Binding Factor Alpha 1 Subunit - genetics Core Binding Factor Alpha 1 Subunit - metabolism Cultured cells Embryos Gene Expression - drug effects Hedgehog Proteins - metabolism Hedgehog Proteins - pharmacology Melanocytes - cytology Mesenchymal stem cells Multipotent stem cells Multipotent Stem Cells - cytology Neural Crest - cytology Neural stem cells Neurogenesis Neuroglia Neurons Oncogene Proteins - genetics Osteoblasts Osteogenesis Progenitor cells Quail Stem cells Trans-Activators - genetics Vertebrates Zinc Finger Protein GLI1 |
| title | High frequency of cephalic neural crest cells shows coexistence of neurogenic, melanogenic, and osteogenic differentiation capacities |
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