Self-Segregation of Myelin Membrane Lipids in Model Membranes
Rapid conduction of nerve impulses requires coating of axons by myelin sheaths, which are multilamellar, lipid-rich membranes produced by oligodendrocytes in the central nervous system. To act as an insulator, myelin has to form a stable and firm membrane structure. In this study, we have analyzed t...
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Veröffentlicht in: | Biophysical journal 2011-12, Vol.101 (11), p.2713-2720 |
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creator | Yurlova, Larisa Kahya, Nicoletta Aggarwal, Shweta Kaiser, Hermann-Josef Chiantia, Salvatore Bakhti, Mostafa Pewzner-Jung, Yael Ben-David, Oshrit Futerman, Anthony H. Brügger, Britta Simons, Mikael |
description | Rapid conduction of nerve impulses requires coating of axons by myelin sheaths, which are multilamellar, lipid-rich membranes produced by oligodendrocytes in the central nervous system. To act as an insulator, myelin has to form a stable and firm membrane structure. In this study, we have analyzed the biophysical properties of myelin membranes prepared from wild-type mice and from mouse mutants that are unable to form stable myelin. Using C-Laurdan and fluorescence correlation spectroscopy, we find that lipids are tightly organized and highly ordered in myelin isolated from wild-type mice, but not from shiverer and ceramide synthase 2 null mice. Furthermore, only myelin lipids from wild-type mice laterally segregate into physically distinct lipid phases in giant unilamellar vesicles in a process that requires very long chain glycosphingolipids. Taken together, our findings suggest that oligodendrocytes exploit the potential of lipids to self-segregate to generate a highly ordered membrane for electrical insulation of axons. |
doi_str_mv | 10.1016/j.bpj.2011.10.026 |
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To act as an insulator, myelin has to form a stable and firm membrane structure. In this study, we have analyzed the biophysical properties of myelin membranes prepared from wild-type mice and from mouse mutants that are unable to form stable myelin. Using C-Laurdan and fluorescence correlation spectroscopy, we find that lipids are tightly organized and highly ordered in myelin isolated from wild-type mice, but not from shiverer and ceramide synthase 2 null mice. Furthermore, only myelin lipids from wild-type mice laterally segregate into physically distinct lipid phases in giant unilamellar vesicles in a process that requires very long chain glycosphingolipids. Taken together, our findings suggest that oligodendrocytes exploit the potential of lipids to self-segregate to generate a highly ordered membrane for electrical insulation of axons.</description><identifier>ISSN: 0006-3495</identifier><identifier>EISSN: 1542-0086</identifier><identifier>DOI: 10.1016/j.bpj.2011.10.026</identifier><identifier>PMID: 22261060</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Axons ; Biophysics ; Correlation analysis ; Diffusion ; Fatty Acids - analysis ; Fluorescence ; Lipids ; Membrane ; Membrane Lipids - chemistry ; Membrane Lipids - metabolism ; Membranes ; Membranes - metabolism ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Mice, Neurologic Mutants ; Models, Biological ; Myelin Sheath - metabolism ; Nervous system ; Sphingolipids - metabolism ; Tissue Extracts</subject><ispartof>Biophysical journal, 2011-12, Vol.101 (11), p.2713-2720</ispartof><rights>2011 Biophysical Society</rights><rights>Copyright © 2011 Biophysical Society. Published by Elsevier Inc. All rights reserved.</rights><rights>Copyright Biophysical Society Dec 7, 2011</rights><rights>2011 by the Biophysical Society. 2011 Biophysical Society</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c510t-88956f1814b5b14d7d5d4c254e2fbaa288b7359f8172cfef5a597f43545ced723</citedby><cites>FETCH-LOGICAL-c510t-88956f1814b5b14d7d5d4c254e2fbaa288b7359f8172cfef5a597f43545ced723</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/PMC3297774/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.bpj.2011.10.026$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,3548,27922,27923,45993,53789,53791</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22261060$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yurlova, Larisa</creatorcontrib><creatorcontrib>Kahya, Nicoletta</creatorcontrib><creatorcontrib>Aggarwal, Shweta</creatorcontrib><creatorcontrib>Kaiser, Hermann-Josef</creatorcontrib><creatorcontrib>Chiantia, Salvatore</creatorcontrib><creatorcontrib>Bakhti, Mostafa</creatorcontrib><creatorcontrib>Pewzner-Jung, Yael</creatorcontrib><creatorcontrib>Ben-David, Oshrit</creatorcontrib><creatorcontrib>Futerman, Anthony H.</creatorcontrib><creatorcontrib>Brügger, Britta</creatorcontrib><creatorcontrib>Simons, Mikael</creatorcontrib><title>Self-Segregation of Myelin Membrane Lipids in Model Membranes</title><title>Biophysical journal</title><addtitle>Biophys J</addtitle><description>Rapid conduction of nerve impulses requires coating of axons by myelin sheaths, which are multilamellar, lipid-rich membranes produced by oligodendrocytes in the central nervous system. 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Taken together, our findings suggest that oligodendrocytes exploit the potential of lipids to self-segregate to generate a highly ordered membrane for electrical insulation of axons.</description><subject>Animals</subject><subject>Axons</subject><subject>Biophysics</subject><subject>Correlation analysis</subject><subject>Diffusion</subject><subject>Fatty Acids - analysis</subject><subject>Fluorescence</subject><subject>Lipids</subject><subject>Membrane</subject><subject>Membrane Lipids - chemistry</subject><subject>Membrane Lipids - metabolism</subject><subject>Membranes</subject><subject>Membranes - metabolism</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Mice, Knockout</subject><subject>Mice, Neurologic Mutants</subject><subject>Models, Biological</subject><subject>Myelin Sheath - metabolism</subject><subject>Nervous system</subject><subject>Sphingolipids - metabolism</subject><subject>Tissue Extracts</subject><issn>0006-3495</issn><issn>1542-0086</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUFv1DAQhS1ERbeFH8AFRVzgku2MY8eJEEioKlBpqx4KZ8txxoujbLzY2Ur993i1ZQUcerI8883TzHuMvUZYImB9MSy77bDkgJj_S-D1M7ZAKXgJ0NTP2QIA6rISrTxlZykNAMgl4At2yjmvEWpYsI93NLryjtaR1mb2YSqCK24eaPRTcUObLpqJipXf-j4V-1LoaTw20kt24syY6NXje85-fLn6fvmtXN1-vb78vCqtRJjLpmll7bBB0ckORa962QvLpSDuOmN403Sqkq1rUHHryEkjW-VEJYW01CtenbNPB93trttQb2maoxn1NvqNiQ86GK__7Uz-p16He13xViklssC7R4EYfu0ozXrjk6VxzFeEXdItKsyOgMzk-ydJ5ByxagGrjL79Dx3CLk7ZiKyHEtoK6wzhAbIxpBTJHbdG0PsU9aBzinqf4r6UU8wzb_4-9zjxJ7YMfDgAlE2_9xR1sp6mbJaPZGfdB_-E_G8k0qt0</recordid><startdate>20111207</startdate><enddate>20111207</enddate><creator>Yurlova, Larisa</creator><creator>Kahya, Nicoletta</creator><creator>Aggarwal, Shweta</creator><creator>Kaiser, Hermann-Josef</creator><creator>Chiantia, Salvatore</creator><creator>Bakhti, Mostafa</creator><creator>Pewzner-Jung, Yael</creator><creator>Ben-David, Oshrit</creator><creator>Futerman, Anthony H.</creator><creator>Brügger, Britta</creator><creator>Simons, Mikael</creator><general>Elsevier Inc</general><general>Biophysical Society</general><general>The Biophysical Society</general><scope>6I.</scope><scope>AAFTH</scope><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>7QO</scope><scope>7QP</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>8FD</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20111207</creationdate><title>Self-Segregation of Myelin Membrane Lipids in Model Membranes</title><author>Yurlova, Larisa ; Kahya, Nicoletta ; Aggarwal, Shweta ; Kaiser, Hermann-Josef ; Chiantia, Salvatore ; Bakhti, Mostafa ; Pewzner-Jung, Yael ; Ben-David, Oshrit ; Futerman, Anthony H. ; Brügger, Britta ; Simons, Mikael</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c510t-88956f1814b5b14d7d5d4c254e2fbaa288b7359f8172cfef5a597f43545ced723</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Animals</topic><topic>Axons</topic><topic>Biophysics</topic><topic>Correlation analysis</topic><topic>Diffusion</topic><topic>Fatty Acids - analysis</topic><topic>Fluorescence</topic><topic>Lipids</topic><topic>Membrane</topic><topic>Membrane Lipids - chemistry</topic><topic>Membrane Lipids - metabolism</topic><topic>Membranes</topic><topic>Membranes - metabolism</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Mice, Knockout</topic><topic>Mice, Neurologic Mutants</topic><topic>Models, Biological</topic><topic>Myelin Sheath - metabolism</topic><topic>Nervous system</topic><topic>Sphingolipids - metabolism</topic><topic>Tissue Extracts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yurlova, Larisa</creatorcontrib><creatorcontrib>Kahya, Nicoletta</creatorcontrib><creatorcontrib>Aggarwal, Shweta</creatorcontrib><creatorcontrib>Kaiser, Hermann-Josef</creatorcontrib><creatorcontrib>Chiantia, Salvatore</creatorcontrib><creatorcontrib>Bakhti, Mostafa</creatorcontrib><creatorcontrib>Pewzner-Jung, Yael</creatorcontrib><creatorcontrib>Ben-David, Oshrit</creatorcontrib><creatorcontrib>Futerman, Anthony H.</creatorcontrib><creatorcontrib>Brügger, Britta</creatorcontrib><creatorcontrib>Simons, Mikael</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Biophysical journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yurlova, Larisa</au><au>Kahya, Nicoletta</au><au>Aggarwal, Shweta</au><au>Kaiser, Hermann-Josef</au><au>Chiantia, Salvatore</au><au>Bakhti, Mostafa</au><au>Pewzner-Jung, Yael</au><au>Ben-David, Oshrit</au><au>Futerman, Anthony H.</au><au>Brügger, Britta</au><au>Simons, Mikael</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Self-Segregation of Myelin Membrane Lipids in Model Membranes</atitle><jtitle>Biophysical journal</jtitle><addtitle>Biophys J</addtitle><date>2011-12-07</date><risdate>2011</risdate><volume>101</volume><issue>11</issue><spage>2713</spage><epage>2720</epage><pages>2713-2720</pages><issn>0006-3495</issn><eissn>1542-0086</eissn><abstract>Rapid conduction of nerve impulses requires coating of axons by myelin sheaths, which are multilamellar, lipid-rich membranes produced by oligodendrocytes in the central nervous system. 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subjects | Animals Axons Biophysics Correlation analysis Diffusion Fatty Acids - analysis Fluorescence Lipids Membrane Membrane Lipids - chemistry Membrane Lipids - metabolism Membranes Membranes - metabolism Mice Mice, Inbred C57BL Mice, Knockout Mice, Neurologic Mutants Models, Biological Myelin Sheath - metabolism Nervous system Sphingolipids - metabolism Tissue Extracts |
title | Self-Segregation of Myelin Membrane Lipids in Model Membranes |
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