Developmental Alcohol Exposure Impairs Activity-Dependent S-Nitrosylation of NDEL1 for Neuronal Maturation
Neuronal nitric oxide synthase is involved in diverse signaling cascades that regulate neuronal development and functions via S-Nitrosylation-mediated mechanism or the soluble guanylate cyclase (sGC)/cyclic guanosine monophosphate (cGMP) pathway activated by nitric oxide. Although it has been studie...
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| Veröffentlicht in: | Cerebral cortex (New York, N.Y. 1991) N.Y. 1991), 2017-08, Vol.27 (8), p.3918-3929 |
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| container_title | Cerebral cortex (New York, N.Y. 1991) |
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| creator | Saito, Atsushi Taniguchi, Yu Kim, Sun-Hong Selvakumar, Balakrishnan Perez, Gabriel Ballinger, Michael D Zhu, Xiaolei Sabra, James Jallow, Mariama Yan, Priscilla Ito, Koki Rajendran, Shreenath Hirotsune, Shinji Wynshaw-Boris, Anthony Snyder, Solomon H Sawa, Akira Kamiya, Atsushi |
| description | Neuronal nitric oxide synthase is involved in diverse signaling cascades that regulate neuronal development and functions via S-Nitrosylation-mediated mechanism or the soluble guanylate cyclase (sGC)/cyclic guanosine monophosphate (cGMP) pathway activated by nitric oxide. Although it has been studied extensively in vitro and in invertebrate animals, effects on mammalian brain development and underlying mechanisms remain poorly understood. Here we report that genetic deletion of "Nos1" disrupts dendritic development, whereas pharmacological inhibition of the sGC/cGMP pathway does not alter dendritic growth during cerebral cortex development. Instead, nuclear distribution element-like (NDEL1), a protein that regulates dendritic development, is specifically S-nitrosylated at cysteine 203, thereby accelerating dendritic arborization. This post-translational modification is enhanced by N-methyl-D-aspartate receptor-mediated neuronal activity, the main regulator of dendritic formation. Notably, we found that disruption of S-Nitrosylation of NDEL1 mediates impaired dendritic maturation caused by developmental alcohol exposure, a model of developmental brain abnormalities resulting from maternal alcohol use. These results highlight S-Nitrosylation as a key activity-dependent mechanism underlying neonatal brain maturation and suggest that reduction of S-Nitrosylation of NDEL1 acts as a pathological factor mediating neurodevelopmental abnormalities caused by maternal alcohol exposure. |
| doi_str_mv | 10.1093/cercor/bhw201 |
| format | Article |
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Although it has been studied extensively in vitro and in invertebrate animals, effects on mammalian brain development and underlying mechanisms remain poorly understood. Here we report that genetic deletion of "Nos1" disrupts dendritic development, whereas pharmacological inhibition of the sGC/cGMP pathway does not alter dendritic growth during cerebral cortex development. Instead, nuclear distribution element-like (NDEL1), a protein that regulates dendritic development, is specifically S-nitrosylated at cysteine 203, thereby accelerating dendritic arborization. This post-translational modification is enhanced by N-methyl-D-aspartate receptor-mediated neuronal activity, the main regulator of dendritic formation. Notably, we found that disruption of S-Nitrosylation of NDEL1 mediates impaired dendritic maturation caused by developmental alcohol exposure, a model of developmental brain abnormalities resulting from maternal alcohol use. These results highlight S-Nitrosylation as a key activity-dependent mechanism underlying neonatal brain maturation and suggest that reduction of S-Nitrosylation of NDEL1 acts as a pathological factor mediating neurodevelopmental abnormalities caused by maternal alcohol exposure.</description><identifier>ISSN: 1047-3211</identifier><identifier>EISSN: 1460-2199</identifier><identifier>DOI: 10.1093/cercor/bhw201</identifier><identifier>PMID: 27371763</identifier><language>eng</language><publisher>United States: Oxford University Press</publisher><subject>Animals ; Carrier Proteins - genetics ; Carrier Proteins - metabolism ; Dendrites - drug effects ; Dendrites - metabolism ; Dendrites - pathology ; Disease Models, Animal ; Fetal Alcohol Spectrum Disorders - metabolism ; Fetal Alcohol Spectrum Disorders - pathology ; Humans ; Mice, Inbred C57BL ; Mice, Transgenic ; Mutation ; Nitric Oxide Synthase Type I - deficiency ; Nitric Oxide Synthase Type I - genetics ; Original ; Prefrontal Cortex - drug effects ; Prefrontal Cortex - growth & development ; Prefrontal Cortex - metabolism ; Prefrontal Cortex - pathology ; Pyramidal Cells - drug effects ; Pyramidal Cells - metabolism ; Pyramidal Cells - pathology ; Synaptic Transmission - physiology</subject><ispartof>Cerebral cortex (New York, N.Y. 1991), 2017-08, Vol.27 (8), p.3918-3929</ispartof><rights>The Author 2016. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com.</rights><rights>The Author 2016. Published by Oxford University Press. All rights reserved. For Permissions, please e-mail: journals.permissions@oup.com 2016</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c348t-4b7bbdbc5751a666dee9124e88d60931b169b06b5f4ad374f92218596de91ee83</citedby><cites>FETCH-LOGICAL-c348t-4b7bbdbc5751a666dee9124e88d60931b169b06b5f4ad374f92218596de91ee83</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,315,781,785,886,27926,27927</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27371763$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Saito, Atsushi</creatorcontrib><creatorcontrib>Taniguchi, Yu</creatorcontrib><creatorcontrib>Kim, Sun-Hong</creatorcontrib><creatorcontrib>Selvakumar, Balakrishnan</creatorcontrib><creatorcontrib>Perez, Gabriel</creatorcontrib><creatorcontrib>Ballinger, Michael D</creatorcontrib><creatorcontrib>Zhu, Xiaolei</creatorcontrib><creatorcontrib>Sabra, James</creatorcontrib><creatorcontrib>Jallow, Mariama</creatorcontrib><creatorcontrib>Yan, Priscilla</creatorcontrib><creatorcontrib>Ito, Koki</creatorcontrib><creatorcontrib>Rajendran, Shreenath</creatorcontrib><creatorcontrib>Hirotsune, Shinji</creatorcontrib><creatorcontrib>Wynshaw-Boris, Anthony</creatorcontrib><creatorcontrib>Snyder, Solomon H</creatorcontrib><creatorcontrib>Sawa, Akira</creatorcontrib><creatorcontrib>Kamiya, Atsushi</creatorcontrib><title>Developmental Alcohol Exposure Impairs Activity-Dependent S-Nitrosylation of NDEL1 for Neuronal Maturation</title><title>Cerebral cortex (New York, N.Y. 1991)</title><addtitle>Cereb Cortex</addtitle><description>Neuronal nitric oxide synthase is involved in diverse signaling cascades that regulate neuronal development and functions via S-Nitrosylation-mediated mechanism or the soluble guanylate cyclase (sGC)/cyclic guanosine monophosphate (cGMP) pathway activated by nitric oxide. 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These results highlight S-Nitrosylation as a key activity-dependent mechanism underlying neonatal brain maturation and suggest that reduction of S-Nitrosylation of NDEL1 acts as a pathological factor mediating neurodevelopmental abnormalities caused by maternal alcohol exposure.</description><subject>Animals</subject><subject>Carrier Proteins - genetics</subject><subject>Carrier Proteins - metabolism</subject><subject>Dendrites - drug effects</subject><subject>Dendrites - metabolism</subject><subject>Dendrites - pathology</subject><subject>Disease Models, Animal</subject><subject>Fetal Alcohol Spectrum Disorders - metabolism</subject><subject>Fetal Alcohol Spectrum Disorders - pathology</subject><subject>Humans</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Transgenic</subject><subject>Mutation</subject><subject>Nitric Oxide Synthase Type I - deficiency</subject><subject>Nitric Oxide Synthase Type I - genetics</subject><subject>Original</subject><subject>Prefrontal Cortex - drug effects</subject><subject>Prefrontal Cortex - growth & development</subject><subject>Prefrontal Cortex - metabolism</subject><subject>Prefrontal Cortex - pathology</subject><subject>Pyramidal Cells - drug effects</subject><subject>Pyramidal Cells - metabolism</subject><subject>Pyramidal Cells - pathology</subject><subject>Synaptic Transmission - physiology</subject><issn>1047-3211</issn><issn>1460-2199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVkUFv1DAQhS0Eou3CkSvykUtoxk7s5IK06i5QaVkOwNmynQnryomDnSzsv8d0SwWnGWk-vZl5j5BXUL6FsuXXFqMN8docfrISnpBLqERZMGjbp7kvK1lwBnBBrlK6K0uQrGbPyQWTXIIU_JLcbfCIPkwDjrP2dO1tOARPt7-mkJaI9HaYtIuJru3sjm4-FRuccOwyTb8UezfHkE5ezy6MNPR0v9nugPYh0j0uMYxZ8ZOel3gPvCDPeu0TvnyoK_Lt_fbrzcdi9_nD7c16V1heNXNRGWlMZ2wta9BCiA6xBVZh03QiPwwGRGtKYeq-0h2XVd8yBk3dZrAFxIavyLuz7rSYATubb43aqym6QceTCtqp_yejO6jv4agEqxqZrVmRNw8CMfxYMM1qcMmi93rEsCQFDRMSeC15RoszarMRKWL_uAZK9Scfdc5HnfPJ_Ot_b3uk_wbCfwOYW5Bk</recordid><startdate>20170801</startdate><enddate>20170801</enddate><creator>Saito, Atsushi</creator><creator>Taniguchi, Yu</creator><creator>Kim, Sun-Hong</creator><creator>Selvakumar, Balakrishnan</creator><creator>Perez, Gabriel</creator><creator>Ballinger, Michael D</creator><creator>Zhu, Xiaolei</creator><creator>Sabra, James</creator><creator>Jallow, Mariama</creator><creator>Yan, Priscilla</creator><creator>Ito, Koki</creator><creator>Rajendran, Shreenath</creator><creator>Hirotsune, Shinji</creator><creator>Wynshaw-Boris, Anthony</creator><creator>Snyder, Solomon H</creator><creator>Sawa, Akira</creator><creator>Kamiya, Atsushi</creator><general>Oxford University Press</general><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>5PM</scope></search><sort><creationdate>20170801</creationdate><title>Developmental Alcohol Exposure Impairs Activity-Dependent S-Nitrosylation of NDEL1 for Neuronal Maturation</title><author>Saito, Atsushi ; 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Although it has been studied extensively in vitro and in invertebrate animals, effects on mammalian brain development and underlying mechanisms remain poorly understood. Here we report that genetic deletion of "Nos1" disrupts dendritic development, whereas pharmacological inhibition of the sGC/cGMP pathway does not alter dendritic growth during cerebral cortex development. Instead, nuclear distribution element-like (NDEL1), a protein that regulates dendritic development, is specifically S-nitrosylated at cysteine 203, thereby accelerating dendritic arborization. This post-translational modification is enhanced by N-methyl-D-aspartate receptor-mediated neuronal activity, the main regulator of dendritic formation. Notably, we found that disruption of S-Nitrosylation of NDEL1 mediates impaired dendritic maturation caused by developmental alcohol exposure, a model of developmental brain abnormalities resulting from maternal alcohol use. These results highlight S-Nitrosylation as a key activity-dependent mechanism underlying neonatal brain maturation and suggest that reduction of S-Nitrosylation of NDEL1 acts as a pathological factor mediating neurodevelopmental abnormalities caused by maternal alcohol exposure.</abstract><cop>United States</cop><pub>Oxford University Press</pub><pmid>27371763</pmid><doi>10.1093/cercor/bhw201</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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| source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Oxford University Press Journals All Titles (1996-Current); Alma/SFX Local Collection |
| subjects | Animals Carrier Proteins - genetics Carrier Proteins - metabolism Dendrites - drug effects Dendrites - metabolism Dendrites - pathology Disease Models, Animal Fetal Alcohol Spectrum Disorders - metabolism Fetal Alcohol Spectrum Disorders - pathology Humans Mice, Inbred C57BL Mice, Transgenic Mutation Nitric Oxide Synthase Type I - deficiency Nitric Oxide Synthase Type I - genetics Original Prefrontal Cortex - drug effects Prefrontal Cortex - growth & development Prefrontal Cortex - metabolism Prefrontal Cortex - pathology Pyramidal Cells - drug effects Pyramidal Cells - metabolism Pyramidal Cells - pathology Synaptic Transmission - physiology |
| title | Developmental Alcohol Exposure Impairs Activity-Dependent S-Nitrosylation of NDEL1 for Neuronal Maturation |
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