Arrest of myelination and reduced axon growth when Schwann cells lack mTOR
In developing peripheral nerves, differentiating Schwann cells sort individual axons from bundles and ensheath them to generate multiple layers of myelin. In recent years, there has been an increased understanding of the extracellular and intracellular factors that initiate and stimulate Schwann cel...
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Veröffentlicht in: | The Journal of neuroscience 2012-02, Vol.32 (5), p.1817-1825 |
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creator | Sherman, Diane L Krols, Michiel Wu, Lai-Man N Grove, Matthew Nave, Klaus-Armin Gangloff, Yann-Gaël Brophy, Peter J |
description | In developing peripheral nerves, differentiating Schwann cells sort individual axons from bundles and ensheath them to generate multiple layers of myelin. In recent years, there has been an increased understanding of the extracellular and intracellular factors that initiate and stimulate Schwann cell myelination, together with a growing appreciation of some of the signaling pathways involved. However, our knowledge of how Schwann cell growth is regulated during myelination is still incomplete. The mammalian target of rapamycin (mTOR) is a core kinase in two major complexes, mTORC1 and mTORC2, that regulate cell growth and differentiation in a variety of mammalian cells. Here we show that elimination of mTOR from murine Schwann cells prevented neither radial sorting nor the initiation of myelination. However, normal postnatal growth of myelinating Schwann cells, both radially and longitudinally, was highly retarded. The myelin sheath in the mutant was much thinner than normal; nevertheless, sheath thickness relative to axon diameter (g-ratio) remained constant in both wild-type and mutant nerves from P14 to P90. Although axon diameters were normal in the mutant at the initiation of myelination, further growth as myelination proceeded was retarded, and this was associated with reduced phosphorylation of neurofilaments. Consistent with thinner axonal diameters and internodal lengths, conduction velocities in mutant quadriceps nerves were also reduced. These data establish a critical role for mTOR signaling in both the longitudinal and radial growth of the myelinating Schwann cell. |
doi_str_mv | 10.1523/JNEUROSCI.4814-11.2012 |
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In recent years, there has been an increased understanding of the extracellular and intracellular factors that initiate and stimulate Schwann cell myelination, together with a growing appreciation of some of the signaling pathways involved. However, our knowledge of how Schwann cell growth is regulated during myelination is still incomplete. The mammalian target of rapamycin (mTOR) is a core kinase in two major complexes, mTORC1 and mTORC2, that regulate cell growth and differentiation in a variety of mammalian cells. Here we show that elimination of mTOR from murine Schwann cells prevented neither radial sorting nor the initiation of myelination. However, normal postnatal growth of myelinating Schwann cells, both radially and longitudinally, was highly retarded. The myelin sheath in the mutant was much thinner than normal; nevertheless, sheath thickness relative to axon diameter (g-ratio) remained constant in both wild-type and mutant nerves from P14 to P90. Although axon diameters were normal in the mutant at the initiation of myelination, further growth as myelination proceeded was retarded, and this was associated with reduced phosphorylation of neurofilaments. Consistent with thinner axonal diameters and internodal lengths, conduction velocities in mutant quadriceps nerves were also reduced. These data establish a critical role for mTOR signaling in both the longitudinal and radial growth of the myelinating Schwann cell.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.4814-11.2012</identifier><identifier>PMID: 22302821</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Animals ; Axons - metabolism ; Axons - pathology ; Axons - ultrastructure ; Cell Enlargement ; Life Sciences ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Myelin Sheath - genetics ; Myelin Sheath - pathology ; Myelin Sheath - ultrastructure ; Organ Culture Techniques ; Schwann Cells - metabolism ; Schwann Cells - pathology ; Schwann Cells - ultrastructure ; TOR Serine-Threonine Kinases - deficiency ; TOR Serine-Threonine Kinases - genetics</subject><ispartof>The Journal of neuroscience, 2012-02, Vol.32 (5), p.1817-1825</ispartof><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>Copyright © 2012 the authors 0270-6474/12/321817-09$15.00/0 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c513t-a6f93e6c0c44f70ed63fe68d3fd5f550c01e3fc07cdb98f92d2b773426f45e6f3</citedby><cites>FETCH-LOGICAL-c513t-a6f93e6c0c44f70ed63fe68d3fd5f550c01e3fc07cdb98f92d2b773426f45e6f3</cites><orcidid>0000-0001-9031-1184</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4298696/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4298696/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22302821$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02126912$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Sherman, Diane L</creatorcontrib><creatorcontrib>Krols, Michiel</creatorcontrib><creatorcontrib>Wu, Lai-Man N</creatorcontrib><creatorcontrib>Grove, Matthew</creatorcontrib><creatorcontrib>Nave, Klaus-Armin</creatorcontrib><creatorcontrib>Gangloff, Yann-Gaël</creatorcontrib><creatorcontrib>Brophy, Peter J</creatorcontrib><title>Arrest of myelination and reduced axon growth when Schwann cells lack mTOR</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>In developing peripheral nerves, differentiating Schwann cells sort individual axons from bundles and ensheath them to generate multiple layers of myelin. In recent years, there has been an increased understanding of the extracellular and intracellular factors that initiate and stimulate Schwann cell myelination, together with a growing appreciation of some of the signaling pathways involved. However, our knowledge of how Schwann cell growth is regulated during myelination is still incomplete. The mammalian target of rapamycin (mTOR) is a core kinase in two major complexes, mTORC1 and mTORC2, that regulate cell growth and differentiation in a variety of mammalian cells. Here we show that elimination of mTOR from murine Schwann cells prevented neither radial sorting nor the initiation of myelination. However, normal postnatal growth of myelinating Schwann cells, both radially and longitudinally, was highly retarded. The myelin sheath in the mutant was much thinner than normal; nevertheless, sheath thickness relative to axon diameter (g-ratio) remained constant in both wild-type and mutant nerves from P14 to P90. Although axon diameters were normal in the mutant at the initiation of myelination, further growth as myelination proceeded was retarded, and this was associated with reduced phosphorylation of neurofilaments. Consistent with thinner axonal diameters and internodal lengths, conduction velocities in mutant quadriceps nerves were also reduced. These data establish a critical role for mTOR signaling in both the longitudinal and radial growth of the myelinating Schwann cell.</description><subject>Animals</subject><subject>Axons - metabolism</subject><subject>Axons - pathology</subject><subject>Axons - ultrastructure</subject><subject>Cell Enlargement</subject><subject>Life Sciences</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Myelin Sheath - genetics</subject><subject>Myelin Sheath - pathology</subject><subject>Myelin Sheath - ultrastructure</subject><subject>Organ Culture Techniques</subject><subject>Schwann Cells - metabolism</subject><subject>Schwann Cells - pathology</subject><subject>Schwann Cells - ultrastructure</subject><subject>TOR Serine-Threonine Kinases - deficiency</subject><subject>TOR Serine-Threonine Kinases - genetics</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkV1P2zAUhi3ENDrYX0C-Q1yk87EdJ75BqqoyQNUq8XFtuf4ggcQBO6Xj3y9RWbVxZemc8z7WOQ9Cp0CmkFP24-bX4uF2dTe_nvISeAYwpQToAZoMXZlRTuAQTQgtSCZ4wY_Qt5SeCCEFgeIrOqKUEVpSmKCbWYwu9bjzuH13TR10X3cB62BxdHZjnMX691B4jN22r_C2cgHfmWqrQ8DGNU3CjTbPuL1f3Z6gL143yX3_eI_Rw-Xifn6VLVc_r-ezZWZyYH2mhZfMCUMM574gzgrmnSgt8zb3eU4MAce8IYWxa1l6SS1dFwXjVHieO-HZMbrYcV8269ZZ40IfdaNeYt3q-K46Xav_O6Gu1GP3pjiVpZBiAJzvANWn2NVsqcYaoUCFBPoGw-zZx2exe90Ml1JtncbFdXDdJikJUua8pCNV7CZN7FKKzu_RQNToTO2dqdGZAlCjsyF4-u8--9hfSewPtVuUAg</recordid><startdate>20120201</startdate><enddate>20120201</enddate><creator>Sherman, Diane L</creator><creator>Krols, Michiel</creator><creator>Wu, Lai-Man N</creator><creator>Grove, Matthew</creator><creator>Nave, Klaus-Armin</creator><creator>Gangloff, Yann-Gaël</creator><creator>Brophy, Peter J</creator><general>Society for Neuroscience</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>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9031-1184</orcidid></search><sort><creationdate>20120201</creationdate><title>Arrest of myelination and reduced axon growth when Schwann cells lack mTOR</title><author>Sherman, Diane L ; Krols, Michiel ; Wu, Lai-Man N ; Grove, Matthew ; Nave, Klaus-Armin ; Gangloff, Yann-Gaël ; Brophy, Peter J</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c513t-a6f93e6c0c44f70ed63fe68d3fd5f550c01e3fc07cdb98f92d2b773426f45e6f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Animals</topic><topic>Axons - metabolism</topic><topic>Axons - pathology</topic><topic>Axons - ultrastructure</topic><topic>Cell Enlargement</topic><topic>Life Sciences</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Myelin Sheath - genetics</topic><topic>Myelin Sheath - pathology</topic><topic>Myelin Sheath - ultrastructure</topic><topic>Organ Culture Techniques</topic><topic>Schwann Cells - metabolism</topic><topic>Schwann Cells - pathology</topic><topic>Schwann Cells - ultrastructure</topic><topic>TOR Serine-Threonine Kinases - deficiency</topic><topic>TOR Serine-Threonine Kinases - genetics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sherman, Diane L</creatorcontrib><creatorcontrib>Krols, Michiel</creatorcontrib><creatorcontrib>Wu, Lai-Man N</creatorcontrib><creatorcontrib>Grove, Matthew</creatorcontrib><creatorcontrib>Nave, Klaus-Armin</creatorcontrib><creatorcontrib>Gangloff, Yann-Gaël</creatorcontrib><creatorcontrib>Brophy, Peter J</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sherman, Diane L</au><au>Krols, Michiel</au><au>Wu, Lai-Man N</au><au>Grove, Matthew</au><au>Nave, Klaus-Armin</au><au>Gangloff, Yann-Gaël</au><au>Brophy, Peter J</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Arrest of myelination and reduced axon growth when Schwann cells lack mTOR</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2012-02-01</date><risdate>2012</risdate><volume>32</volume><issue>5</issue><spage>1817</spage><epage>1825</epage><pages>1817-1825</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>In developing peripheral nerves, differentiating Schwann cells sort individual axons from bundles and ensheath them to generate multiple layers of myelin. 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subjects | Animals Axons - metabolism Axons - pathology Axons - ultrastructure Cell Enlargement Life Sciences Mice Mice, Inbred C57BL Mice, Knockout Myelin Sheath - genetics Myelin Sheath - pathology Myelin Sheath - ultrastructure Organ Culture Techniques Schwann Cells - metabolism Schwann Cells - pathology Schwann Cells - ultrastructure TOR Serine-Threonine Kinases - deficiency TOR Serine-Threonine Kinases - genetics |
title | Arrest of myelination and reduced axon growth when Schwann cells lack mTOR |
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