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Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites
The geometric and subcellular organization of axon arbors distributes and regulates electrical signaling in neurons and networks, but the underlying mechanisms have remained elusive. In rodent cerebellar cortex, stellate interneurons elaborate characteristic axon arbors that selectively innervate Pu...
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Published in: | PLoS biology 2008-04, Vol.6 (4), p.e103-e103 |
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description | The geometric and subcellular organization of axon arbors distributes and regulates electrical signaling in neurons and networks, but the underlying mechanisms have remained elusive. In rodent cerebellar cortex, stellate interneurons elaborate characteristic axon arbors that selectively innervate Purkinje cell dendrites and likely regulate dendritic integration. We used GFP BAC transgenic reporter mice to examine the cellular processes and molecular mechanisms underlying the development of stellate cell axons and their innervation pattern. We show that stellate axons are organized and guided towards Purkinje cell dendrites by an intermediate scaffold of Bergmann glial (BG) fibers. The L1 family immunoglobulin protein Close Homologue of L1 (CHL1) is localized to apical BG fibers and stellate cells during the development of stellate axon arbors. In the absence of CHL1, stellate axons deviate from BG fibers and show aberrant branching and orientation. Furthermore, synapse formation between aberrant stellate axons and Purkinje dendrites is reduced and cannot be maintained, leading to progressive atrophy of axon terminals. These results establish BG fibers as a guiding scaffold and CHL1 a molecular signal in the organization of stellate axon arbors and in directing their dendritic innervation. |
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In rodent cerebellar cortex, stellate interneurons elaborate characteristic axon arbors that selectively innervate Purkinje cell dendrites and likely regulate dendritic integration. We used GFP BAC transgenic reporter mice to examine the cellular processes and molecular mechanisms underlying the development of stellate cell axons and their innervation pattern. We show that stellate axons are organized and guided towards Purkinje cell dendrites by an intermediate scaffold of Bergmann glial (BG) fibers. The L1 family immunoglobulin protein Close Homologue of L1 (CHL1) is localized to apical BG fibers and stellate cells during the development of stellate axon arbors. In the absence of CHL1, stellate axons deviate from BG fibers and show aberrant branching and orientation. Furthermore, synapse formation between aberrant stellate axons and Purkinje dendrites is reduced and cannot be maintained, leading to progressive atrophy of axon terminals. These results establish BG fibers as a guiding scaffold and CHL1 a molecular signal in the organization of stellate axon arbors and in directing their dendritic innervation.</description><identifier>ISSN: 1545-7885</identifier><identifier>ISSN: 1544-9173</identifier><identifier>EISSN: 1545-7885</identifier><identifier>DOI: 10.1371/journal.pbio.0060103</identifier><identifier>PMID: 18447583</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Animals ; Artificial chromosomes ; Axons ; Axons - metabolism ; Axons - ultrastructure ; Cell adhesion & migration ; Cell Adhesion Molecules ; Cell Adhesion Molecules - immunology ; Cell Adhesion Molecules - metabolism ; Cell Biology ; Cellular Biology ; Cerebellar Cortex ; Cerebellar Cortex - metabolism ; Climbing ; Dendrites ; Dendrites - metabolism ; Dendrites - ultrastructure ; Experiments ; gamma-Aminobutyric Acid ; gamma-Aminobutyric Acid - metabolism ; Life Sciences ; Mice ; Mice, Transgenic ; Microscopy ; Microscopy, Electron ; Neuroglia ; Neuroglia - metabolism ; Neuroglia - ultrastructure ; Neurons ; Neurons and Cognition ; Neuroscience ; Proteins ; Purkinje Cells ; Purkinje Cells - metabolism ; Purkinje Cells - ultrastructure ; Synapses ; Synapses - physiology</subject><ispartof>PLoS biology, 2008-04, Vol.6 (4), p.e103-e103</ispartof><rights>2008 Ango et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Ango F, Wu C, Van der Want JJ, Wu P, Schachner M, et al. (2008) Bergmann Glia and the Recognition Molecule CHL1 Organize GABAergic Axons and Direct Innervation of Purkinje Cell Dendrites. PLoS Biol 6(4): e103. doi:10.1371/journal.pbio.0060103</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2008 Ango et al. 2008</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c627t-ff125572b0bacce651e6d00dd58c274ecab35ae3d02481954cf42863375f84a73</citedby><cites>FETCH-LOGICAL-c627t-ff125572b0bacce651e6d00dd58c274ecab35ae3d02481954cf42863375f84a73</cites><orcidid>0000-0002-5548-209X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1292065593/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1292065593?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25731,27901,27902,36989,36990,44566,53766,53768,74869</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/18447583$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://inserm.hal.science/inserm-00707838$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Ango, Fabrice</creatorcontrib><creatorcontrib>Wu, Caizhi</creatorcontrib><creatorcontrib>Van der Want, Johannes J</creatorcontrib><creatorcontrib>Wu, Priscilla</creatorcontrib><creatorcontrib>Schachner, Melitta</creatorcontrib><creatorcontrib>Huang, Z Josh</creatorcontrib><title>Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites</title><title>PLoS biology</title><addtitle>PLoS Biol</addtitle><description>The geometric and subcellular organization of axon arbors distributes and regulates electrical signaling in neurons and networks, but the underlying mechanisms have remained elusive. In rodent cerebellar cortex, stellate interneurons elaborate characteristic axon arbors that selectively innervate Purkinje cell dendrites and likely regulate dendritic integration. We used GFP BAC transgenic reporter mice to examine the cellular processes and molecular mechanisms underlying the development of stellate cell axons and their innervation pattern. We show that stellate axons are organized and guided towards Purkinje cell dendrites by an intermediate scaffold of Bergmann glial (BG) fibers. The L1 family immunoglobulin protein Close Homologue of L1 (CHL1) is localized to apical BG fibers and stellate cells during the development of stellate axon arbors. In the absence of CHL1, stellate axons deviate from BG fibers and show aberrant branching and orientation. Furthermore, synapse formation between aberrant stellate axons and Purkinje dendrites is reduced and cannot be maintained, leading to progressive atrophy of axon terminals. These results establish BG fibers as a guiding scaffold and CHL1 a molecular signal in the organization of stellate axon arbors and in directing their dendritic innervation.</description><subject>Animals</subject><subject>Artificial chromosomes</subject><subject>Axons</subject><subject>Axons - metabolism</subject><subject>Axons - ultrastructure</subject><subject>Cell adhesion & migration</subject><subject>Cell Adhesion Molecules</subject><subject>Cell Adhesion Molecules - immunology</subject><subject>Cell Adhesion Molecules - metabolism</subject><subject>Cell Biology</subject><subject>Cellular Biology</subject><subject>Cerebellar Cortex</subject><subject>Cerebellar Cortex - metabolism</subject><subject>Climbing</subject><subject>Dendrites</subject><subject>Dendrites - metabolism</subject><subject>Dendrites - ultrastructure</subject><subject>Experiments</subject><subject>gamma-Aminobutyric Acid</subject><subject>gamma-Aminobutyric Acid - metabolism</subject><subject>Life Sciences</subject><subject>Mice</subject><subject>Mice, Transgenic</subject><subject>Microscopy</subject><subject>Microscopy, Electron</subject><subject>Neuroglia</subject><subject>Neuroglia - 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Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><collection>PLoS Biology</collection><jtitle>PLoS biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ango, Fabrice</au><au>Wu, Caizhi</au><au>Van der Want, Johannes J</au><au>Wu, Priscilla</au><au>Schachner, Melitta</au><au>Huang, Z Josh</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites</atitle><jtitle>PLoS biology</jtitle><addtitle>PLoS Biol</addtitle><date>2008-04-01</date><risdate>2008</risdate><volume>6</volume><issue>4</issue><spage>e103</spage><epage>e103</epage><pages>e103-e103</pages><issn>1545-7885</issn><issn>1544-9173</issn><eissn>1545-7885</eissn><abstract>The geometric and subcellular organization of axon arbors distributes and regulates electrical signaling in neurons and networks, but the underlying mechanisms have remained elusive. In rodent cerebellar cortex, stellate interneurons elaborate characteristic axon arbors that selectively innervate Purkinje cell dendrites and likely regulate dendritic integration. We used GFP BAC transgenic reporter mice to examine the cellular processes and molecular mechanisms underlying the development of stellate cell axons and their innervation pattern. We show that stellate axons are organized and guided towards Purkinje cell dendrites by an intermediate scaffold of Bergmann glial (BG) fibers. The L1 family immunoglobulin protein Close Homologue of L1 (CHL1) is localized to apical BG fibers and stellate cells during the development of stellate axon arbors. In the absence of CHL1, stellate axons deviate from BG fibers and show aberrant branching and orientation. Furthermore, synapse formation between aberrant stellate axons and Purkinje dendrites is reduced and cannot be maintained, leading to progressive atrophy of axon terminals. These results establish BG fibers as a guiding scaffold and CHL1 a molecular signal in the organization of stellate axon arbors and in directing their dendritic innervation.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>18447583</pmid><doi>10.1371/journal.pbio.0060103</doi><orcidid>https://orcid.org/0000-0002-5548-209X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Animals Artificial chromosomes Axons Axons - metabolism Axons - ultrastructure Cell adhesion & migration Cell Adhesion Molecules Cell Adhesion Molecules - immunology Cell Adhesion Molecules - metabolism Cell Biology Cellular Biology Cerebellar Cortex Cerebellar Cortex - metabolism Climbing Dendrites Dendrites - metabolism Dendrites - ultrastructure Experiments gamma-Aminobutyric Acid gamma-Aminobutyric Acid - metabolism Life Sciences Mice Mice, Transgenic Microscopy Microscopy, Electron Neuroglia Neuroglia - metabolism Neuroglia - ultrastructure Neurons Neurons and Cognition Neuroscience Proteins Purkinje Cells Purkinje Cells - metabolism Purkinje Cells - ultrastructure Synapses Synapses - physiology |
title | Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites |
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