Myelin-associated oligodendrocytic basic protein-dependent myelin repair confers the long-lasting antidepressant effect of ketamine
Ketamine exhibits rapid and sustained antidepressant effects. As decreased myelination has been linked to depression pathology, changes in myelination may be a pivotal mechanism underlying ketamine’s long-lasting antidepressant effects. Although ketamine has a long-lasting facilitating effect on mye...
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| Veröffentlicht in: | Molecular psychiatry 2024-06, Vol.29 (6), p.1741-1753 |
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| creator | Huang, Chaoli Wu, Zifeng Wang, Di Qu, Youge Zhang, Jichun Jiang, Riyue Xu, Xiangqing Xu, Xiangyang Wang, Yuanyuan Liu, Hanyu He, Teng Liu, Cunming Chen, Guiquan Yang, Jian-jun Hashimoto, Kenji Yang, Chun |
| description | Ketamine exhibits rapid and sustained antidepressant effects. As decreased myelination has been linked to depression pathology, changes in myelination may be a pivotal mechanism underlying ketamine’s long-lasting antidepressant effects. Although ketamine has a long-lasting facilitating effect on myelination, the precise roles of myelination in ketamine’s sustained antidepressant effects remain unknown. In this study, we employed spatial transcriptomics (ST) to examine ketamine’s lasting effects in the medial prefrontal cortex (mPFC) and hippocampus of mice subjected to chronic social defeat stress and identified several differentially expressed myelin-related genes. Ketamine’s ability to restore impaired myelination in the brain by promoting the differentiation of oligodendrocyte precursor cells (OPCs) into mature oligodendrocytes was demonstrated. Moreover, we showed that inhibiting the expression of myelin-associated oligodendrocytic basic protein (Mobp) blocked ketamine’s long-lasting antidepressant effects. We also illustrated that α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) signaling mediated ketamine’s facilitation on myelination. In addition, we found that the (
R
)-stereoisomer of ketamine showed stronger effects on myelination than (
S)
-ketamine, which may explain its longer-lasting antidepressant effects. These findings reveal novel mechanisms underlying the sustained antidepressant effects of ketamine and the differences in antidepressant effects between (
R
)-ketamine and (
S
)-ketamine, providing new insights into the role of myelination in antidepressant mechanisms. |
| doi_str_mv | 10.1038/s41380-023-02288-5 |
| format | Article |
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R
)-stereoisomer of ketamine showed stronger effects on myelination than (
S)
-ketamine, which may explain its longer-lasting antidepressant effects. These findings reveal novel mechanisms underlying the sustained antidepressant effects of ketamine and the differences in antidepressant effects between (
R
)-ketamine and (
S
)-ketamine, providing new insights into the role of myelination in antidepressant mechanisms.</description><identifier>ISSN: 1359-4184</identifier><identifier>ISSN: 1476-5578</identifier><identifier>EISSN: 1476-5578</identifier><identifier>DOI: 10.1038/s41380-023-02288-5</identifier><identifier>PMID: 37848708</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/95 ; 38/47 ; 631/378 ; 692/699/476/1414 ; 96/1 ; Animals ; Antidepressants ; Antidepressive Agents - pharmacology ; Behavioral Sciences ; Biological Psychology ; Cell differentiation ; Cell Differentiation - drug effects ; Depression - drug therapy ; Depression - metabolism ; Glial stem cells ; Hippocampus - drug effects ; Hippocampus - metabolism ; Ketamine ; Ketamine - pharmacology ; Male ; Medicine ; Medicine & Public Health ; Mice ; Mice, Inbred C57BL ; Myelin Basic Protein - metabolism ; Myelin Sheath - drug effects ; Myelin Sheath - metabolism ; Myelination ; Neurosciences ; Oligodendrocyte Precursor Cells - drug effects ; Oligodendrocyte Precursor Cells - metabolism ; Oligodendrocyte-myelin glycoprotein ; Oligodendrocytes ; Oligodendroglia - drug effects ; Oligodendroglia - metabolism ; Pharmacotherapy ; Prefrontal cortex ; Prefrontal Cortex - drug effects ; Prefrontal Cortex - metabolism ; Psychiatry ; Social interactions ; Stereoisomers ; Stress, Psychological - drug therapy ; Stress, Psychological - metabolism ; Transcriptomics ; α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</subject><ispartof>Molecular psychiatry, 2024-06, Vol.29 (6), p.1741-1753</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2023. The Author(s), under exclusive licence to Springer Nature Limited.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c375t-38e2668998412ad891275b5abe59c1dd8b90ed707383ce4092dfbbae01215e383</citedby><cites>FETCH-LOGICAL-c375t-38e2668998412ad891275b5abe59c1dd8b90ed707383ce4092dfbbae01215e383</cites><orcidid>0000-0001-6035-6867 ; 0000-0001-6785-9627 ; 0000-0002-8892-0439 ; 0000-0003-1540-4385 ; 0000-0003-4935-3758</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41380-023-02288-5$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41380-023-02288-5$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37848708$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Huang, Chaoli</creatorcontrib><creatorcontrib>Wu, Zifeng</creatorcontrib><creatorcontrib>Wang, Di</creatorcontrib><creatorcontrib>Qu, Youge</creatorcontrib><creatorcontrib>Zhang, Jichun</creatorcontrib><creatorcontrib>Jiang, Riyue</creatorcontrib><creatorcontrib>Xu, Xiangqing</creatorcontrib><creatorcontrib>Xu, Xiangyang</creatorcontrib><creatorcontrib>Wang, Yuanyuan</creatorcontrib><creatorcontrib>Liu, Hanyu</creatorcontrib><creatorcontrib>He, Teng</creatorcontrib><creatorcontrib>Liu, Cunming</creatorcontrib><creatorcontrib>Chen, Guiquan</creatorcontrib><creatorcontrib>Yang, Jian-jun</creatorcontrib><creatorcontrib>Hashimoto, Kenji</creatorcontrib><creatorcontrib>Yang, Chun</creatorcontrib><title>Myelin-associated oligodendrocytic basic protein-dependent myelin repair confers the long-lasting antidepressant effect of ketamine</title><title>Molecular psychiatry</title><addtitle>Mol Psychiatry</addtitle><addtitle>Mol Psychiatry</addtitle><description>Ketamine exhibits rapid and sustained antidepressant effects. As decreased myelination has been linked to depression pathology, changes in myelination may be a pivotal mechanism underlying ketamine’s long-lasting antidepressant effects. Although ketamine has a long-lasting facilitating effect on myelination, the precise roles of myelination in ketamine’s sustained antidepressant effects remain unknown. In this study, we employed spatial transcriptomics (ST) to examine ketamine’s lasting effects in the medial prefrontal cortex (mPFC) and hippocampus of mice subjected to chronic social defeat stress and identified several differentially expressed myelin-related genes. Ketamine’s ability to restore impaired myelination in the brain by promoting the differentiation of oligodendrocyte precursor cells (OPCs) into mature oligodendrocytes was demonstrated. Moreover, we showed that inhibiting the expression of myelin-associated oligodendrocytic basic protein (Mobp) blocked ketamine’s long-lasting antidepressant effects. We also illustrated that α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) signaling mediated ketamine’s facilitation on myelination. In addition, we found that the (
R
)-stereoisomer of ketamine showed stronger effects on myelination than (
S)
-ketamine, which may explain its longer-lasting antidepressant effects. These findings reveal novel mechanisms underlying the sustained antidepressant effects of ketamine and the differences in antidepressant effects between (
R
)-ketamine and (
S
)-ketamine, providing new insights into the role of myelination in antidepressant mechanisms.</description><subject>13/95</subject><subject>38/47</subject><subject>631/378</subject><subject>692/699/476/1414</subject><subject>96/1</subject><subject>Animals</subject><subject>Antidepressants</subject><subject>Antidepressive Agents - pharmacology</subject><subject>Behavioral Sciences</subject><subject>Biological Psychology</subject><subject>Cell differentiation</subject><subject>Cell Differentiation - drug effects</subject><subject>Depression - drug therapy</subject><subject>Depression - metabolism</subject><subject>Glial stem cells</subject><subject>Hippocampus - drug effects</subject><subject>Hippocampus - metabolism</subject><subject>Ketamine</subject><subject>Ketamine - pharmacology</subject><subject>Male</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Myelin Basic Protein - metabolism</subject><subject>Myelin Sheath - drug effects</subject><subject>Myelin Sheath - metabolism</subject><subject>Myelination</subject><subject>Neurosciences</subject><subject>Oligodendrocyte Precursor Cells - drug effects</subject><subject>Oligodendrocyte Precursor Cells - metabolism</subject><subject>Oligodendrocyte-myelin glycoprotein</subject><subject>Oligodendrocytes</subject><subject>Oligodendroglia - drug effects</subject><subject>Oligodendroglia - metabolism</subject><subject>Pharmacotherapy</subject><subject>Prefrontal cortex</subject><subject>Prefrontal Cortex - drug effects</subject><subject>Prefrontal Cortex - metabolism</subject><subject>Psychiatry</subject><subject>Social interactions</subject><subject>Stereoisomers</subject><subject>Stress, Psychological - drug therapy</subject><subject>Stress, Psychological - metabolism</subject><subject>Transcriptomics</subject><subject>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</subject><issn>1359-4184</issn><issn>1476-5578</issn><issn>1476-5578</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUuPFCEUhYnROA_9Ay4MiRs3KM8GlmYy6iRj3OiaUHCrZayCFuhFr_3j0tOjJi5cADfc7xweB6EXjL5hVJi3TTJhKKFcjMGNIeoROmdSb4hS2jwetVCWSGbkGbpo7Y7SY1M9RWdCG2k0Nefo56cDLCkT31oJyXeIuCxpWyLkWEs49BTw5NuYd7V0GGSE3ehB7ni9l-IKO58qDiXPUBvu3wAvJW_J4ltPeYt97mmIKrQ2SgzzDKHjMuPv0P2aMjxDT2a_NHj-sF6ir--vv1x9JLefP9xcvbslQWjViTDANxtjrZGM-2gs41pNyk-gbGAxmslSiJpqYUQASS2P8zR5oIwzBWPzEr0--Y6n_NhD625NLcCy-Axl3xw3enyKlfKIvvoHvSv7msftnGCUig2zRg-Kn6hQS2sVZrerafX14Bh1x4jcKSI3InL3ETk1RC8frPfTCvGP5HcmAxAnoI1W3kL9e_Z_bH8BQZSerg</recordid><startdate>20240601</startdate><enddate>20240601</enddate><creator>Huang, Chaoli</creator><creator>Wu, Zifeng</creator><creator>Wang, Di</creator><creator>Qu, Youge</creator><creator>Zhang, Jichun</creator><creator>Jiang, Riyue</creator><creator>Xu, Xiangqing</creator><creator>Xu, Xiangyang</creator><creator>Wang, Yuanyuan</creator><creator>Liu, Hanyu</creator><creator>He, Teng</creator><creator>Liu, Cunming</creator><creator>Chen, Guiquan</creator><creator>Yang, Jian-jun</creator><creator>Hashimoto, Kenji</creator><creator>Yang, Chun</creator><general>Nature Publishing Group UK</general><general>Nature Publishing Group</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>7TK</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-6035-6867</orcidid><orcidid>https://orcid.org/0000-0001-6785-9627</orcidid><orcidid>https://orcid.org/0000-0002-8892-0439</orcidid><orcidid>https://orcid.org/0000-0003-1540-4385</orcidid><orcidid>https://orcid.org/0000-0003-4935-3758</orcidid></search><sort><creationdate>20240601</creationdate><title>Myelin-associated oligodendrocytic basic protein-dependent myelin repair confers the long-lasting antidepressant effect of ketamine</title><author>Huang, Chaoli ; Wu, Zifeng ; Wang, Di ; Qu, Youge ; Zhang, Jichun ; Jiang, Riyue ; Xu, Xiangqing ; Xu, Xiangyang ; Wang, Yuanyuan ; Liu, Hanyu ; He, Teng ; Liu, Cunming ; Chen, Guiquan ; Yang, Jian-jun ; Hashimoto, Kenji ; Yang, Chun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c375t-38e2668998412ad891275b5abe59c1dd8b90ed707383ce4092dfbbae01215e383</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>13/95</topic><topic>38/47</topic><topic>631/378</topic><topic>692/699/476/1414</topic><topic>96/1</topic><topic>Animals</topic><topic>Antidepressants</topic><topic>Antidepressive Agents - pharmacology</topic><topic>Behavioral Sciences</topic><topic>Biological Psychology</topic><topic>Cell differentiation</topic><topic>Cell Differentiation - drug effects</topic><topic>Depression - drug therapy</topic><topic>Depression - metabolism</topic><topic>Glial stem cells</topic><topic>Hippocampus - drug effects</topic><topic>Hippocampus - metabolism</topic><topic>Ketamine</topic><topic>Ketamine - pharmacology</topic><topic>Male</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Myelin Basic Protein - metabolism</topic><topic>Myelin Sheath - drug effects</topic><topic>Myelin Sheath - metabolism</topic><topic>Myelination</topic><topic>Neurosciences</topic><topic>Oligodendrocyte Precursor Cells - drug effects</topic><topic>Oligodendrocyte Precursor Cells - metabolism</topic><topic>Oligodendrocyte-myelin glycoprotein</topic><topic>Oligodendrocytes</topic><topic>Oligodendroglia - drug effects</topic><topic>Oligodendroglia - metabolism</topic><topic>Pharmacotherapy</topic><topic>Prefrontal cortex</topic><topic>Prefrontal Cortex - drug effects</topic><topic>Prefrontal Cortex - metabolism</topic><topic>Psychiatry</topic><topic>Social interactions</topic><topic>Stereoisomers</topic><topic>Stress, Psychological - drug therapy</topic><topic>Stress, Psychological - metabolism</topic><topic>Transcriptomics</topic><topic>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Huang, Chaoli</creatorcontrib><creatorcontrib>Wu, Zifeng</creatorcontrib><creatorcontrib>Wang, Di</creatorcontrib><creatorcontrib>Qu, Youge</creatorcontrib><creatorcontrib>Zhang, Jichun</creatorcontrib><creatorcontrib>Jiang, Riyue</creatorcontrib><creatorcontrib>Xu, Xiangqing</creatorcontrib><creatorcontrib>Xu, Xiangyang</creatorcontrib><creatorcontrib>Wang, Yuanyuan</creatorcontrib><creatorcontrib>Liu, Hanyu</creatorcontrib><creatorcontrib>He, Teng</creatorcontrib><creatorcontrib>Liu, Cunming</creatorcontrib><creatorcontrib>Chen, Guiquan</creatorcontrib><creatorcontrib>Yang, Jian-jun</creatorcontrib><creatorcontrib>Hashimoto, Kenji</creatorcontrib><creatorcontrib>Yang, Chun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Molecular psychiatry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Huang, Chaoli</au><au>Wu, Zifeng</au><au>Wang, Di</au><au>Qu, Youge</au><au>Zhang, Jichun</au><au>Jiang, Riyue</au><au>Xu, Xiangqing</au><au>Xu, Xiangyang</au><au>Wang, Yuanyuan</au><au>Liu, Hanyu</au><au>He, Teng</au><au>Liu, Cunming</au><au>Chen, Guiquan</au><au>Yang, Jian-jun</au><au>Hashimoto, Kenji</au><au>Yang, Chun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Myelin-associated oligodendrocytic basic protein-dependent myelin repair confers the long-lasting antidepressant effect of ketamine</atitle><jtitle>Molecular psychiatry</jtitle><stitle>Mol Psychiatry</stitle><addtitle>Mol Psychiatry</addtitle><date>2024-06-01</date><risdate>2024</risdate><volume>29</volume><issue>6</issue><spage>1741</spage><epage>1753</epage><pages>1741-1753</pages><issn>1359-4184</issn><issn>1476-5578</issn><eissn>1476-5578</eissn><abstract>Ketamine exhibits rapid and sustained antidepressant effects. As decreased myelination has been linked to depression pathology, changes in myelination may be a pivotal mechanism underlying ketamine’s long-lasting antidepressant effects. Although ketamine has a long-lasting facilitating effect on myelination, the precise roles of myelination in ketamine’s sustained antidepressant effects remain unknown. In this study, we employed spatial transcriptomics (ST) to examine ketamine’s lasting effects in the medial prefrontal cortex (mPFC) and hippocampus of mice subjected to chronic social defeat stress and identified several differentially expressed myelin-related genes. Ketamine’s ability to restore impaired myelination in the brain by promoting the differentiation of oligodendrocyte precursor cells (OPCs) into mature oligodendrocytes was demonstrated. Moreover, we showed that inhibiting the expression of myelin-associated oligodendrocytic basic protein (Mobp) blocked ketamine’s long-lasting antidepressant effects. We also illustrated that α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) signaling mediated ketamine’s facilitation on myelination. In addition, we found that the (
R
)-stereoisomer of ketamine showed stronger effects on myelination than (
S)
-ketamine, which may explain its longer-lasting antidepressant effects. These findings reveal novel mechanisms underlying the sustained antidepressant effects of ketamine and the differences in antidepressant effects between (
R
)-ketamine and (
S
)-ketamine, providing new insights into the role of myelination in antidepressant mechanisms.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>37848708</pmid><doi>10.1038/s41380-023-02288-5</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-6035-6867</orcidid><orcidid>https://orcid.org/0000-0001-6785-9627</orcidid><orcidid>https://orcid.org/0000-0002-8892-0439</orcidid><orcidid>https://orcid.org/0000-0003-1540-4385</orcidid><orcidid>https://orcid.org/0000-0003-4935-3758</orcidid></addata></record> |
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| ispartof | Molecular psychiatry, 2024-06, Vol.29 (6), p.1741-1753 |
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| subjects | 13/95 38/47 631/378 692/699/476/1414 96/1 Animals Antidepressants Antidepressive Agents - pharmacology Behavioral Sciences Biological Psychology Cell differentiation Cell Differentiation - drug effects Depression - drug therapy Depression - metabolism Glial stem cells Hippocampus - drug effects Hippocampus - metabolism Ketamine Ketamine - pharmacology Male Medicine Medicine & Public Health Mice Mice, Inbred C57BL Myelin Basic Protein - metabolism Myelin Sheath - drug effects Myelin Sheath - metabolism Myelination Neurosciences Oligodendrocyte Precursor Cells - drug effects Oligodendrocyte Precursor Cells - metabolism Oligodendrocyte-myelin glycoprotein Oligodendrocytes Oligodendroglia - drug effects Oligodendroglia - metabolism Pharmacotherapy Prefrontal cortex Prefrontal Cortex - drug effects Prefrontal Cortex - metabolism Psychiatry Social interactions Stereoisomers Stress, Psychological - drug therapy Stress, Psychological - metabolism Transcriptomics α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors |
| title | Myelin-associated oligodendrocytic basic protein-dependent myelin repair confers the long-lasting antidepressant effect of ketamine |
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