Neurodevelopment. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors
The peripheral autonomic nervous system reaches far throughout the body and includes neurons of diverse functions, such as sympathetic and parasympathetic. We show that the parasympathetic system in mice--including trunk ganglia and the cranial ciliary, pterygopalatine, lingual, submandibular, and o...
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Veröffentlicht in: | Science (American Association for the Advancement of Science) 2014-07, Vol.345 (6192), p.82-87 |
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creator | Dyachuk, Vyacheslav Furlan, Alessandro Shahidi, Maryam Khatibi Giovenco, Marcela Kaukua, Nina Konstantinidou, Chrysoula Pachnis, Vassilis Memic, Fatima Marklund, Ulrika Müller, Thomas Birchmeier, Carmen Fried, Kaj Ernfors, Patrik Adameyko, Igor |
description | The peripheral autonomic nervous system reaches far throughout the body and includes neurons of diverse functions, such as sympathetic and parasympathetic. We show that the parasympathetic system in mice--including trunk ganglia and the cranial ciliary, pterygopalatine, lingual, submandibular, and otic ganglia--arise from glial cells in nerves, not neural crest cells. The parasympathetic fate is induced in nerve-associated Schwann cell precursors at distal peripheral sites. We used multicolor Cre-reporter lineage tracing to show that most of these neurons arise from bi-potent progenitors that generate both glia and neurons. This nerve origin places cellular elements for generating parasympathetic neurons in diverse tissues and organs, which may enable wiring of the developing parasympathetic nervous system. |
doi_str_mv | 10.1126/science.1253281 |
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We show that the parasympathetic system in mice--including trunk ganglia and the cranial ciliary, pterygopalatine, lingual, submandibular, and otic ganglia--arise from glial cells in nerves, not neural crest cells. The parasympathetic fate is induced in nerve-associated Schwann cell precursors at distal peripheral sites. We used multicolor Cre-reporter lineage tracing to show that most of these neurons arise from bi-potent progenitors that generate both glia and neurons. This nerve origin places cellular elements for generating parasympathetic neurons in diverse tissues and organs, which may enable wiring of the developing parasympathetic nervous system.</description><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.1253281</identifier><identifier>PMID: 24925909</identifier><language>eng</language><publisher>United States</publisher><subject>Animals ; Basic Helix-Loop-Helix Transcription Factors - genetics ; Basic Helix-Loop-Helix Transcription Factors - metabolism ; Ganglia, Parasympathetic - cytology ; Ganglia, Parasympathetic - embryology ; Mice ; Mice, Mutant Strains ; Neural Stem Cells - cytology ; Neural Stem Cells - metabolism ; Neuroanatomical Tract-Tracing Techniques - methods ; Neurogenesis ; Neuroglia - cytology ; Neuroglia - metabolism ; Neurons - cytology ; Neurons - metabolism ; Parasympathetic Nervous System - cytology ; Parasympathetic Nervous System - embryology ; Schwann Cells - cytology ; Schwann Cells - metabolism ; SOXE Transcription Factors - genetics ; SOXE Transcription Factors - metabolism</subject><ispartof>Science (American Association for the Advancement of Science), 2014-07, Vol.345 (6192), p.82-87</ispartof><rights>Copyright © 2014, American Association for the Advancement of Science.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24925909$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dyachuk, Vyacheslav</creatorcontrib><creatorcontrib>Furlan, Alessandro</creatorcontrib><creatorcontrib>Shahidi, Maryam Khatibi</creatorcontrib><creatorcontrib>Giovenco, Marcela</creatorcontrib><creatorcontrib>Kaukua, Nina</creatorcontrib><creatorcontrib>Konstantinidou, Chrysoula</creatorcontrib><creatorcontrib>Pachnis, Vassilis</creatorcontrib><creatorcontrib>Memic, Fatima</creatorcontrib><creatorcontrib>Marklund, Ulrika</creatorcontrib><creatorcontrib>Müller, Thomas</creatorcontrib><creatorcontrib>Birchmeier, Carmen</creatorcontrib><creatorcontrib>Fried, Kaj</creatorcontrib><creatorcontrib>Ernfors, Patrik</creatorcontrib><creatorcontrib>Adameyko, Igor</creatorcontrib><title>Neurodevelopment. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>The peripheral autonomic nervous system reaches far throughout the body and includes neurons of diverse functions, such as sympathetic and parasympathetic. We show that the parasympathetic system in mice--including trunk ganglia and the cranial ciliary, pterygopalatine, lingual, submandibular, and otic ganglia--arise from glial cells in nerves, not neural crest cells. The parasympathetic fate is induced in nerve-associated Schwann cell precursors at distal peripheral sites. We used multicolor Cre-reporter lineage tracing to show that most of these neurons arise from bi-potent progenitors that generate both glia and neurons. This nerve origin places cellular elements for generating parasympathetic neurons in diverse tissues and organs, which may enable wiring of the developing parasympathetic nervous system.</description><subject>Animals</subject><subject>Basic Helix-Loop-Helix Transcription Factors - genetics</subject><subject>Basic Helix-Loop-Helix Transcription Factors - metabolism</subject><subject>Ganglia, Parasympathetic - cytology</subject><subject>Ganglia, Parasympathetic - embryology</subject><subject>Mice</subject><subject>Mice, Mutant Strains</subject><subject>Neural Stem Cells - cytology</subject><subject>Neural Stem Cells - metabolism</subject><subject>Neuroanatomical Tract-Tracing Techniques - methods</subject><subject>Neurogenesis</subject><subject>Neuroglia - cytology</subject><subject>Neuroglia - metabolism</subject><subject>Neurons - cytology</subject><subject>Neurons - metabolism</subject><subject>Parasympathetic Nervous System - cytology</subject><subject>Parasympathetic Nervous System - embryology</subject><subject>Schwann Cells - cytology</subject><subject>Schwann Cells - metabolism</subject><subject>SOXE Transcription Factors - genetics</subject><subject>SOXE Transcription Factors - metabolism</subject><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo1kEtLxDAUhYMgzvhYu5Mu3XTMs22WMviCQQXdlzS5mYm0SU3agfn3Rhw353IOH-fCQeia4BUhtLpL2oHXsCJUMNqQE7QkWIpSUswW6DylL4yzl-wMLSiXVEgsl8i-whyDgT30YRzAT6viXUWVDsOoph1MThf-l_CpCNFtnVcTFDaGIcdxD6VKKWiXQ1OMEN24g6j6Ytu7rGMMW_BuCjFdolOr-gRXx3uBPh4fPtfP5ebt6WV9vylHUcmy6nitccUJYNkwXUPHK8MaaZkiFTFCcNZxq2tJcGM1UFlr0WElsDFWdMAu0O1fa_78PUOa2sElDX2vPIQ5tSQX5GUwJxm9OaJzN4Bpx-gGFQ_t_zLsB3TUZ2U</recordid><startdate>20140704</startdate><enddate>20140704</enddate><creator>Dyachuk, Vyacheslav</creator><creator>Furlan, Alessandro</creator><creator>Shahidi, Maryam Khatibi</creator><creator>Giovenco, Marcela</creator><creator>Kaukua, Nina</creator><creator>Konstantinidou, Chrysoula</creator><creator>Pachnis, Vassilis</creator><creator>Memic, Fatima</creator><creator>Marklund, Ulrika</creator><creator>Müller, Thomas</creator><creator>Birchmeier, Carmen</creator><creator>Fried, Kaj</creator><creator>Ernfors, Patrik</creator><creator>Adameyko, Igor</creator><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7X8</scope></search><sort><creationdate>20140704</creationdate><title>Neurodevelopment. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors</title><author>Dyachuk, Vyacheslav ; Furlan, Alessandro ; Shahidi, Maryam Khatibi ; Giovenco, Marcela ; Kaukua, Nina ; Konstantinidou, Chrysoula ; Pachnis, Vassilis ; Memic, Fatima ; Marklund, Ulrika ; Müller, Thomas ; Birchmeier, Carmen ; Fried, Kaj ; Ernfors, Patrik ; Adameyko, Igor</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-p569-6b47c0641e0983c7eb46d389f3a161d5543b4fc79108fce297c5b0a50ddf5be3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Basic Helix-Loop-Helix Transcription Factors - genetics</topic><topic>Basic Helix-Loop-Helix Transcription Factors - metabolism</topic><topic>Ganglia, Parasympathetic - cytology</topic><topic>Ganglia, Parasympathetic - embryology</topic><topic>Mice</topic><topic>Mice, Mutant Strains</topic><topic>Neural Stem Cells - cytology</topic><topic>Neural Stem Cells - metabolism</topic><topic>Neuroanatomical Tract-Tracing Techniques - methods</topic><topic>Neurogenesis</topic><topic>Neuroglia - cytology</topic><topic>Neuroglia - metabolism</topic><topic>Neurons - cytology</topic><topic>Neurons - metabolism</topic><topic>Parasympathetic Nervous System - cytology</topic><topic>Parasympathetic Nervous System - embryology</topic><topic>Schwann Cells - cytology</topic><topic>Schwann Cells - metabolism</topic><topic>SOXE Transcription Factors - genetics</topic><topic>SOXE Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dyachuk, Vyacheslav</creatorcontrib><creatorcontrib>Furlan, Alessandro</creatorcontrib><creatorcontrib>Shahidi, Maryam Khatibi</creatorcontrib><creatorcontrib>Giovenco, Marcela</creatorcontrib><creatorcontrib>Kaukua, Nina</creatorcontrib><creatorcontrib>Konstantinidou, Chrysoula</creatorcontrib><creatorcontrib>Pachnis, Vassilis</creatorcontrib><creatorcontrib>Memic, Fatima</creatorcontrib><creatorcontrib>Marklund, Ulrika</creatorcontrib><creatorcontrib>Müller, Thomas</creatorcontrib><creatorcontrib>Birchmeier, Carmen</creatorcontrib><creatorcontrib>Fried, Kaj</creatorcontrib><creatorcontrib>Ernfors, Patrik</creatorcontrib><creatorcontrib>Adameyko, Igor</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>MEDLINE - Academic</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dyachuk, Vyacheslav</au><au>Furlan, Alessandro</au><au>Shahidi, Maryam Khatibi</au><au>Giovenco, Marcela</au><au>Kaukua, Nina</au><au>Konstantinidou, Chrysoula</au><au>Pachnis, Vassilis</au><au>Memic, Fatima</au><au>Marklund, Ulrika</au><au>Müller, Thomas</au><au>Birchmeier, Carmen</au><au>Fried, Kaj</au><au>Ernfors, Patrik</au><au>Adameyko, Igor</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Neurodevelopment. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2014-07-04</date><risdate>2014</risdate><volume>345</volume><issue>6192</issue><spage>82</spage><epage>87</epage><pages>82-87</pages><eissn>1095-9203</eissn><abstract>The peripheral autonomic nervous system reaches far throughout the body and includes neurons of diverse functions, such as sympathetic and parasympathetic. We show that the parasympathetic system in mice--including trunk ganglia and the cranial ciliary, pterygopalatine, lingual, submandibular, and otic ganglia--arise from glial cells in nerves, not neural crest cells. The parasympathetic fate is induced in nerve-associated Schwann cell precursors at distal peripheral sites. 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subjects | Animals Basic Helix-Loop-Helix Transcription Factors - genetics Basic Helix-Loop-Helix Transcription Factors - metabolism Ganglia, Parasympathetic - cytology Ganglia, Parasympathetic - embryology Mice Mice, Mutant Strains Neural Stem Cells - cytology Neural Stem Cells - metabolism Neuroanatomical Tract-Tracing Techniques - methods Neurogenesis Neuroglia - cytology Neuroglia - metabolism Neurons - cytology Neurons - metabolism Parasympathetic Nervous System - cytology Parasympathetic Nervous System - embryology Schwann Cells - cytology Schwann Cells - metabolism SOXE Transcription Factors - genetics SOXE Transcription Factors - metabolism |
title | Neurodevelopment. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors |
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