Melatonin promotes oligodendroglial maturation of injured white matter in neonatal rats
To investigate the effects of melatonin treatment in a rat model of white matter damage (WMD) in the developing brain. Additionally, we aim to delineate the cellular mechanisms of melatonin effect on the oligodendroglial cell lineage. A unilateral ligation of the uterine artery in pregnant rat at th...
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| Veröffentlicht in: | PloS one 2009-09, Vol.4 (9), p.e7128-e7128 |
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| creator | Olivier, Paul Fontaine, Romain H Loron, Gauthier Van Steenwinckel, Juliette Biran, Valérie Massonneau, Véronique Kaindl, Angela Dalous, Jeremie Charriaut-Marlangue, Christiane Aigrot, Marie-Stéphane Pansiot, Julien Verney, Catherine Gressens, Pierre Baud, Olivier |
| description | To investigate the effects of melatonin treatment in a rat model of white matter damage (WMD) in the developing brain. Additionally, we aim to delineate the cellular mechanisms of melatonin effect on the oligodendroglial cell lineage.
A unilateral ligation of the uterine artery in pregnant rat at the embryonic day 17 induces fetal hypoxia and subsequent growth restriction (GR) in neonatal pups. GR and control pups received a daily intra-peritoneal injection of melatonin from birth to post-natal day (P) 3.
Melatonin administration was associated with a dramatic decrease in microglial activation and astroglial reaction compared to untreated GR pups. At P14, melatonin prevented white matter myelination defects with an increased number of mature oligodendrocytes (APC-immunoreactive) in treated GR pups. Conversely, melatonin was not found to be associated with an increased density of total oligodendrocytes (Olig2-immunoreactive), suggesting that melatonin is able to promote oligodendrocyte maturation but not proliferation. These effects appear to be melatonin-receptor dependent and were reproduced in vitro.
These data suggest that melatonin has a strong protective effect on developing damaged white matter through decreased microglial activation and oligodendroglial maturation leading to a normalization of the myelination process. Consequently, melatonin should be a considered as an effective neuroprotective candidate not only in perinatal brain damage but also in inflammatory and demyelinating diseases observed in adults. |
| doi_str_mv | 10.1371/journal.pone.0007128 |
| format | Article |
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A unilateral ligation of the uterine artery in pregnant rat at the embryonic day 17 induces fetal hypoxia and subsequent growth restriction (GR) in neonatal pups. GR and control pups received a daily intra-peritoneal injection of melatonin from birth to post-natal day (P) 3.
Melatonin administration was associated with a dramatic decrease in microglial activation and astroglial reaction compared to untreated GR pups. At P14, melatonin prevented white matter myelination defects with an increased number of mature oligodendrocytes (APC-immunoreactive) in treated GR pups. Conversely, melatonin was not found to be associated with an increased density of total oligodendrocytes (Olig2-immunoreactive), suggesting that melatonin is able to promote oligodendrocyte maturation but not proliferation. These effects appear to be melatonin-receptor dependent and were reproduced in vitro.
These data suggest that melatonin has a strong protective effect on developing damaged white matter through decreased microglial activation and oligodendroglial maturation leading to a normalization of the myelination process. Consequently, melatonin should be a considered as an effective neuroprotective candidate not only in perinatal brain damage but also in inflammatory and demyelinating diseases observed in adults.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0007128</identifier><identifier>PMID: 19771167</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Activation ; Adults ; Animals ; Animals, Newborn ; Antioxidants ; Brain ; Brain - embryology ; Brain - growth & development ; Brain damage ; Brain injury ; Brain research ; Cell Lineage ; Cells, Cultured ; Cytokines ; Demyelinating diseases ; Demyelination ; Embryos ; Fetuses ; Gene Expression Regulation, Developmental ; Hypoxia ; Immunohistochemistry - methods ; Intensive care ; Ischemia ; Laboratory animals ; Maturation ; Melatonin ; Melatonin - metabolism ; Melatonin - physiology ; Metabolites ; Microscopy, Fluorescence - methods ; Myelination ; Narcotics ; Neonates ; Nerve Fibers, Myelinated - metabolism ; Neuroprotection ; Neuroscience/Neurobiology of Disease and Regeneration ; Neuroscience/Neurodevelopment ; Newborn babies ; Olig2 protein ; Oligodendrocytes ; Oligodendroglia - metabolism ; Pediatrics and Child Health/Neonatology ; Peritoneum ; Pregnancy ; Premature birth ; Quantitative analysis ; Rats ; Rats, Sprague-Dawley ; RNA, Messenger - metabolism ; Rodents ; Substantia alba ; Time Factors ; Traumatic brain injury ; Uterus</subject><ispartof>PloS one, 2009-09, Vol.4 (9), p.e7128-e7128</ispartof><rights>COPYRIGHT 2009 Public Library of Science</rights><rights>2009 Olivier et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Olivier et al. 2009</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c663t-d820772f2f582c40f1322a4ed01879bc77093138539500d603d37b1f816c3f463</citedby><cites>FETCH-LOGICAL-c663t-d820772f2f582c40f1322a4ed01879bc77093138539500d603d37b1f816c3f463</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2742165/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2742165/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19771167$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Hashimoto, Kenji</contributor><creatorcontrib>Olivier, Paul</creatorcontrib><creatorcontrib>Fontaine, Romain H</creatorcontrib><creatorcontrib>Loron, Gauthier</creatorcontrib><creatorcontrib>Van Steenwinckel, Juliette</creatorcontrib><creatorcontrib>Biran, Valérie</creatorcontrib><creatorcontrib>Massonneau, Véronique</creatorcontrib><creatorcontrib>Kaindl, Angela</creatorcontrib><creatorcontrib>Dalous, Jeremie</creatorcontrib><creatorcontrib>Charriaut-Marlangue, Christiane</creatorcontrib><creatorcontrib>Aigrot, Marie-Stéphane</creatorcontrib><creatorcontrib>Pansiot, Julien</creatorcontrib><creatorcontrib>Verney, Catherine</creatorcontrib><creatorcontrib>Gressens, Pierre</creatorcontrib><creatorcontrib>Baud, Olivier</creatorcontrib><title>Melatonin promotes oligodendroglial maturation of injured white matter in neonatal rats</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>To investigate the effects of melatonin treatment in a rat model of white matter damage (WMD) in the developing brain. Additionally, we aim to delineate the cellular mechanisms of melatonin effect on the oligodendroglial cell lineage.
A unilateral ligation of the uterine artery in pregnant rat at the embryonic day 17 induces fetal hypoxia and subsequent growth restriction (GR) in neonatal pups. GR and control pups received a daily intra-peritoneal injection of melatonin from birth to post-natal day (P) 3.
Melatonin administration was associated with a dramatic decrease in microglial activation and astroglial reaction compared to untreated GR pups. At P14, melatonin prevented white matter myelination defects with an increased number of mature oligodendrocytes (APC-immunoreactive) in treated GR pups. Conversely, melatonin was not found to be associated with an increased density of total oligodendrocytes (Olig2-immunoreactive), suggesting that melatonin is able to promote oligodendrocyte maturation but not proliferation. These effects appear to be melatonin-receptor dependent and were reproduced in vitro.
These data suggest that melatonin has a strong protective effect on developing damaged white matter through decreased microglial activation and oligodendroglial maturation leading to a normalization of the myelination process. Consequently, melatonin should be a considered as an effective neuroprotective candidate not only in perinatal brain damage but also in inflammatory and demyelinating diseases observed in adults.</description><subject>Activation</subject><subject>Adults</subject><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Antioxidants</subject><subject>Brain</subject><subject>Brain - embryology</subject><subject>Brain - growth & development</subject><subject>Brain damage</subject><subject>Brain injury</subject><subject>Brain research</subject><subject>Cell Lineage</subject><subject>Cells, Cultured</subject><subject>Cytokines</subject><subject>Demyelinating diseases</subject><subject>Demyelination</subject><subject>Embryos</subject><subject>Fetuses</subject><subject>Gene Expression Regulation, Developmental</subject><subject>Hypoxia</subject><subject>Immunohistochemistry - methods</subject><subject>Intensive care</subject><subject>Ischemia</subject><subject>Laboratory animals</subject><subject>Maturation</subject><subject>Melatonin</subject><subject>Melatonin - metabolism</subject><subject>Melatonin - physiology</subject><subject>Metabolites</subject><subject>Microscopy, Fluorescence - methods</subject><subject>Myelination</subject><subject>Narcotics</subject><subject>Neonates</subject><subject>Nerve Fibers, Myelinated - metabolism</subject><subject>Neuroprotection</subject><subject>Neuroscience/Neurobiology of Disease and Regeneration</subject><subject>Neuroscience/Neurodevelopment</subject><subject>Newborn babies</subject><subject>Olig2 protein</subject><subject>Oligodendrocytes</subject><subject>Oligodendroglia - metabolism</subject><subject>Pediatrics and Child Health/Neonatology</subject><subject>Peritoneum</subject><subject>Pregnancy</subject><subject>Premature birth</subject><subject>Quantitative analysis</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>RNA, Messenger - metabolism</subject><subject>Rodents</subject><subject>Substantia alba</subject><subject>Time Factors</subject><subject>Traumatic brain 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promotes oligodendroglial maturation of injured white matter in neonatal rats</title><author>Olivier, Paul ; Fontaine, Romain H ; Loron, Gauthier ; Van Steenwinckel, Juliette ; Biran, Valérie ; Massonneau, Véronique ; Kaindl, Angela ; Dalous, Jeremie ; Charriaut-Marlangue, Christiane ; Aigrot, Marie-Stéphane ; Pansiot, Julien ; Verney, Catherine ; Gressens, Pierre ; Baud, Olivier</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c663t-d820772f2f582c40f1322a4ed01879bc77093138539500d603d37b1f816c3f463</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Activation</topic><topic>Adults</topic><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Antioxidants</topic><topic>Brain</topic><topic>Brain - embryology</topic><topic>Brain - growth & development</topic><topic>Brain damage</topic><topic>Brain injury</topic><topic>Brain research</topic><topic>Cell Lineage</topic><topic>Cells, Cultured</topic><topic>Cytokines</topic><topic>Demyelinating diseases</topic><topic>Demyelination</topic><topic>Embryos</topic><topic>Fetuses</topic><topic>Gene Expression Regulation, Developmental</topic><topic>Hypoxia</topic><topic>Immunohistochemistry - methods</topic><topic>Intensive care</topic><topic>Ischemia</topic><topic>Laboratory animals</topic><topic>Maturation</topic><topic>Melatonin</topic><topic>Melatonin - metabolism</topic><topic>Melatonin - physiology</topic><topic>Metabolites</topic><topic>Microscopy, Fluorescence - methods</topic><topic>Myelination</topic><topic>Narcotics</topic><topic>Neonates</topic><topic>Nerve Fibers, Myelinated - metabolism</topic><topic>Neuroprotection</topic><topic>Neuroscience/Neurobiology of Disease and Regeneration</topic><topic>Neuroscience/Neurodevelopment</topic><topic>Newborn babies</topic><topic>Olig2 protein</topic><topic>Oligodendrocytes</topic><topic>Oligodendroglia - metabolism</topic><topic>Pediatrics 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H</au><au>Loron, Gauthier</au><au>Van Steenwinckel, Juliette</au><au>Biran, Valérie</au><au>Massonneau, Véronique</au><au>Kaindl, Angela</au><au>Dalous, Jeremie</au><au>Charriaut-Marlangue, Christiane</au><au>Aigrot, Marie-Stéphane</au><au>Pansiot, Julien</au><au>Verney, Catherine</au><au>Gressens, Pierre</au><au>Baud, Olivier</au><au>Hashimoto, Kenji</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Melatonin promotes oligodendroglial maturation of injured white matter in neonatal rats</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2009-09-22</date><risdate>2009</risdate><volume>4</volume><issue>9</issue><spage>e7128</spage><epage>e7128</epage><pages>e7128-e7128</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>To investigate the effects of melatonin treatment in a rat model of white matter damage (WMD) in the developing brain. Additionally, we aim to delineate the cellular mechanisms of melatonin effect on the oligodendroglial cell lineage.
A unilateral ligation of the uterine artery in pregnant rat at the embryonic day 17 induces fetal hypoxia and subsequent growth restriction (GR) in neonatal pups. GR and control pups received a daily intra-peritoneal injection of melatonin from birth to post-natal day (P) 3.
Melatonin administration was associated with a dramatic decrease in microglial activation and astroglial reaction compared to untreated GR pups. At P14, melatonin prevented white matter myelination defects with an increased number of mature oligodendrocytes (APC-immunoreactive) in treated GR pups. Conversely, melatonin was not found to be associated with an increased density of total oligodendrocytes (Olig2-immunoreactive), suggesting that melatonin is able to promote oligodendrocyte maturation but not proliferation. These effects appear to be melatonin-receptor dependent and were reproduced in vitro.
These data suggest that melatonin has a strong protective effect on developing damaged white matter through decreased microglial activation and oligodendroglial maturation leading to a normalization of the myelination process. Consequently, melatonin should be a considered as an effective neuroprotective candidate not only in perinatal brain damage but also in inflammatory and demyelinating diseases observed in adults.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>19771167</pmid><doi>10.1371/journal.pone.0007128</doi><tpages>e7128</tpages><oa>free_for_read</oa></addata></record> |
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| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2009-09, Vol.4 (9), p.e7128-e7128 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1292106788 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Public Library of Science (PLoS) Journals Open Access; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry |
| subjects | Activation Adults Animals Animals, Newborn Antioxidants Brain Brain - embryology Brain - growth & development Brain damage Brain injury Brain research Cell Lineage Cells, Cultured Cytokines Demyelinating diseases Demyelination Embryos Fetuses Gene Expression Regulation, Developmental Hypoxia Immunohistochemistry - methods Intensive care Ischemia Laboratory animals Maturation Melatonin Melatonin - metabolism Melatonin - physiology Metabolites Microscopy, Fluorescence - methods Myelination Narcotics Neonates Nerve Fibers, Myelinated - metabolism Neuroprotection Neuroscience/Neurobiology of Disease and Regeneration Neuroscience/Neurodevelopment Newborn babies Olig2 protein Oligodendrocytes Oligodendroglia - metabolism Pediatrics and Child Health/Neonatology Peritoneum Pregnancy Premature birth Quantitative analysis Rats Rats, Sprague-Dawley RNA, Messenger - metabolism Rodents Substantia alba Time Factors Traumatic brain injury Uterus |
| title | Melatonin promotes oligodendroglial maturation of injured white matter in neonatal rats |
| url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-24T11%3A39%3A28IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_plos_&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Melatonin%20promotes%20oligodendroglial%20maturation%20of%20injured%20white%20matter%20in%20neonatal%20rats&rft.jtitle=PloS%20one&rft.au=Olivier,%20Paul&rft.date=2009-09-22&rft.volume=4&rft.issue=9&rft.spage=e7128&rft.epage=e7128&rft.pages=e7128-e7128&rft.issn=1932-6203&rft.eissn=1932-6203&rft_id=info:doi/10.1371/journal.pone.0007128&rft_dat=%3Cgale_plos_%3EA472865963%3C/gale_plos_%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1292106788&rft_id=info:pmid/19771167&rft_galeid=A472865963&rft_doaj_id=oai_doaj_org_article_6497cb32c65c4c3fb7a74fe9497c3960&rfr_iscdi=true |