The SNARE protein SNAP-29 interacts with the GTPase Rab3A: Implications for membrane trafficking in myelinating glia
During myelin formation, vast amounts of specialized membrane proteins and lipids are trafficked toward the growing sheath in cell surface‐directed transport vesicles. Soluble N‐ethylmaleimide‐sensitive factor (NSF) attachment proteins (SNAPs) are important components of molecular complexes required...
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| Veröffentlicht in: | Journal of neuroscience research 2009-11, Vol.87 (15), p.3465-3479 |
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| creator | Schardt, Anke Brinkmann, Bastian G. Mitkovski, Miso Sereda, Michael W. Werner, Hauke B. Nave, Klaus-Armin |
| description | During myelin formation, vast amounts of specialized membrane proteins and lipids are trafficked toward the growing sheath in cell surface‐directed transport vesicles. Soluble N‐ethylmaleimide‐sensitive factor (NSF) attachment proteins (SNAPs) are important components of molecular complexes required for membrane fusion. We have analyzed the expression profile and molecular interactions of SNAP‐29 in the nervous system. In addition to its known enrichment in neuronal synapses, SNAP‐29 is abundant in oligodendrocytes during myelination and in noncompact myelin of the peripheral nervous system. By yeast two‐hybrid screen and coimmunoprecipitation, we found that the GTPases Rab3A, Rab24, and septin 4 bind to the N‐terminal domain of SNAP‐29. The interaction with Rab24 or septin 4 was GTP independent. In contrast, interaction between SNAP‐29 and Rab3A was GTP dependent, and colocalization was extensive both in synapses and in myelinating glia. In HEK293 cells, cytoplasmic SNAP‐29 pools were redistributed upon coexpression with Rab3A, and surface‐directed trafficking of myelin proteolipid protein was enhanced by overexpression of SNAP‐29 and Rab3A. Interestingly, the abundance of SNAP‐29 in sciatic nerves was increased during remyelination and in a rat model of Charcot‐Marie‐Tooth disease, two pathological situations with increased myelin membrane biogenesis. We suggest that Rab3A may regulate SNAP‐29‐mediated membrane fusion during myelination. © 2009 Wiley‐Liss, Inc. |
| doi_str_mv | 10.1002/jnr.22005 |
| format | Article |
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Soluble N‐ethylmaleimide‐sensitive factor (NSF) attachment proteins (SNAPs) are important components of molecular complexes required for membrane fusion. We have analyzed the expression profile and molecular interactions of SNAP‐29 in the nervous system. In addition to its known enrichment in neuronal synapses, SNAP‐29 is abundant in oligodendrocytes during myelination and in noncompact myelin of the peripheral nervous system. By yeast two‐hybrid screen and coimmunoprecipitation, we found that the GTPases Rab3A, Rab24, and septin 4 bind to the N‐terminal domain of SNAP‐29. The interaction with Rab24 or septin 4 was GTP independent. In contrast, interaction between SNAP‐29 and Rab3A was GTP dependent, and colocalization was extensive both in synapses and in myelinating glia. In HEK293 cells, cytoplasmic SNAP‐29 pools were redistributed upon coexpression with Rab3A, and surface‐directed trafficking of myelin proteolipid protein was enhanced by overexpression of SNAP‐29 and Rab3A. Interestingly, the abundance of SNAP‐29 in sciatic nerves was increased during remyelination and in a rat model of Charcot‐Marie‐Tooth disease, two pathological situations with increased myelin membrane biogenesis. We suggest that Rab3A may regulate SNAP‐29‐mediated membrane fusion during myelination. © 2009 Wiley‐Liss, Inc.</description><identifier>ISSN: 0360-4012</identifier><identifier>ISSN: 1097-4547</identifier><identifier>EISSN: 1097-4547</identifier><identifier>DOI: 10.1002/jnr.22005</identifier><identifier>PMID: 19170188</identifier><language>eng</language><publisher>Hoboken: Wiley Subscription Services, Inc., A Wiley Company</publisher><subject>Animals ; Animals, Newborn ; Binding Sites - physiology ; Cell Differentiation - physiology ; Cell Line ; Cell Membrane - metabolism ; Cell Membrane - ultrastructure ; Cells, Cultured ; Central Nervous System - cytology ; Central Nervous System - growth & development ; Central Nervous System - metabolism ; Charcot-Marie-Tooth Disease - metabolism ; Charcot-Marie-Tooth Disease - physiopathology ; Charcot-Marie-Tooth neuropathy ; Cytoskeletal Proteins - metabolism ; Disease Models, Animal ; Gene Expression Regulation, Developmental - physiology ; GTP-Binding Proteins - metabolism ; Guanosine Triphosphate - metabolism ; Membrane Fusion - physiology ; membrane trafficking ; Mice ; Mice, Inbred C57BL ; Myelin Proteolipid Protein - metabolism ; Myelin Sheath - metabolism ; Myelin Sheath - ultrastructure ; Nerve Fibers, Myelinated - metabolism ; Nerve Fibers, Myelinated - ultrastructure ; oligodendrocyte ; Protein Binding - physiology ; Protein Structure, Tertiary - physiology ; Protein Transport - physiology ; Qb-SNARE Proteins - metabolism ; Qc-SNARE Proteins - metabolism ; rab GTP-Binding Proteins - metabolism ; rab3A ; rab3A GTP-Binding Protein - metabolism ; Rats ; remyelination ; Schwann cell ; Septins ; SNARE proteins ; Synaptic Membranes - metabolism ; Two-Hybrid System Techniques</subject><ispartof>Journal of neuroscience research, 2009-11, Vol.87 (15), p.3465-3479</ispartof><rights>Copyright © 2009 Wiley‐Liss, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4295-150df921a6c267648c3784efcdb99504f58316aa5d68fed7ce939f0eaee8b93</citedby><cites>FETCH-LOGICAL-c4295-150df921a6c267648c3784efcdb99504f58316aa5d68fed7ce939f0eaee8b93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fjnr.22005$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fjnr.22005$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19170188$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Schardt, Anke</creatorcontrib><creatorcontrib>Brinkmann, Bastian G.</creatorcontrib><creatorcontrib>Mitkovski, Miso</creatorcontrib><creatorcontrib>Sereda, Michael W.</creatorcontrib><creatorcontrib>Werner, Hauke B.</creatorcontrib><creatorcontrib>Nave, Klaus-Armin</creatorcontrib><title>The SNARE protein SNAP-29 interacts with the GTPase Rab3A: Implications for membrane trafficking in myelinating glia</title><title>Journal of neuroscience research</title><addtitle>J. Neurosci. Res</addtitle><description>During myelin formation, vast amounts of specialized membrane proteins and lipids are trafficked toward the growing sheath in cell surface‐directed transport vesicles. Soluble N‐ethylmaleimide‐sensitive factor (NSF) attachment proteins (SNAPs) are important components of molecular complexes required for membrane fusion. We have analyzed the expression profile and molecular interactions of SNAP‐29 in the nervous system. In addition to its known enrichment in neuronal synapses, SNAP‐29 is abundant in oligodendrocytes during myelination and in noncompact myelin of the peripheral nervous system. By yeast two‐hybrid screen and coimmunoprecipitation, we found that the GTPases Rab3A, Rab24, and septin 4 bind to the N‐terminal domain of SNAP‐29. The interaction with Rab24 or septin 4 was GTP independent. In contrast, interaction between SNAP‐29 and Rab3A was GTP dependent, and colocalization was extensive both in synapses and in myelinating glia. In HEK293 cells, cytoplasmic SNAP‐29 pools were redistributed upon coexpression with Rab3A, and surface‐directed trafficking of myelin proteolipid protein was enhanced by overexpression of SNAP‐29 and Rab3A. Interestingly, the abundance of SNAP‐29 in sciatic nerves was increased during remyelination and in a rat model of Charcot‐Marie‐Tooth disease, two pathological situations with increased myelin membrane biogenesis. We suggest that Rab3A may regulate SNAP‐29‐mediated membrane fusion during myelination. © 2009 Wiley‐Liss, Inc.</description><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Binding Sites - physiology</subject><subject>Cell Differentiation - physiology</subject><subject>Cell Line</subject><subject>Cell Membrane - metabolism</subject><subject>Cell Membrane - ultrastructure</subject><subject>Cells, Cultured</subject><subject>Central Nervous System - cytology</subject><subject>Central Nervous System - growth & development</subject><subject>Central Nervous System - metabolism</subject><subject>Charcot-Marie-Tooth Disease - metabolism</subject><subject>Charcot-Marie-Tooth Disease - physiopathology</subject><subject>Charcot-Marie-Tooth neuropathy</subject><subject>Cytoskeletal Proteins - metabolism</subject><subject>Disease Models, Animal</subject><subject>Gene Expression Regulation, Developmental - physiology</subject><subject>GTP-Binding Proteins - metabolism</subject><subject>Guanosine Triphosphate - metabolism</subject><subject>Membrane Fusion - physiology</subject><subject>membrane trafficking</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Myelin Proteolipid Protein - metabolism</subject><subject>Myelin Sheath - metabolism</subject><subject>Myelin Sheath - ultrastructure</subject><subject>Nerve Fibers, Myelinated - metabolism</subject><subject>Nerve Fibers, Myelinated - ultrastructure</subject><subject>oligodendrocyte</subject><subject>Protein Binding - physiology</subject><subject>Protein Structure, Tertiary - physiology</subject><subject>Protein Transport - physiology</subject><subject>Qb-SNARE Proteins - metabolism</subject><subject>Qc-SNARE Proteins - metabolism</subject><subject>rab GTP-Binding Proteins - metabolism</subject><subject>rab3A</subject><subject>rab3A GTP-Binding Protein - metabolism</subject><subject>Rats</subject><subject>remyelination</subject><subject>Schwann cell</subject><subject>Septins</subject><subject>SNARE proteins</subject><subject>Synaptic Membranes - metabolism</subject><subject>Two-Hybrid System Techniques</subject><issn>0360-4012</issn><issn>1097-4547</issn><issn>1097-4547</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkU1vEzEQhi0EoqFw4A8g3xCHbcfr3bXNLUQlbalCSCNxtLze2dbtfgTbUcm_r0sCnBCn0UjPPJqZl5C3DE4YQH56N_iTPAcon5EJAyWyoizEczIBXkFWAMuPyKsQ7gBAqZK_JEdMMQFMygmJ61uk14vp6oxu_BjRDU_dMssVdUNEb2wM9MHFWxoTOF8vTUC6MjWffqQX_aZz1kQ3DoG2o6c99rU3A9LoTds6e--Gm6Sh_Q47NyQwtTedM6_Ji9Z0Ad8c6jG5_ny2np1nV1_nF7PpVWaLXJUZK6FpVc5MZfNKVIW0XMgCW9vU6Q4o2lJyVhlTNpVssREWFVctoEGUteLH5P3emg77scUQde-Cxa5LG47boKXkwDlX8F9S8AIkyIol8sOetH4MwWOrN971xu80A_2UhU5Z6F9ZJPbdwbqte2z-kofnJ-B0Dzy4Dnf_NunLxeq3MttPuBDx558J4-91Jbgo9ffFXK-_iNW3T7NLveSPkFehjg</recordid><startdate>20091115</startdate><enddate>20091115</enddate><creator>Schardt, Anke</creator><creator>Brinkmann, Bastian G.</creator><creator>Mitkovski, Miso</creator><creator>Sereda, Michael W.</creator><creator>Werner, Hauke B.</creator><creator>Nave, Klaus-Armin</creator><general>Wiley Subscription Services, Inc., A Wiley Company</general><scope>BSCLL</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>7X8</scope><scope>7TK</scope></search><sort><creationdate>20091115</creationdate><title>The SNARE protein SNAP-29 interacts with the GTPase Rab3A: Implications for membrane trafficking in myelinating glia</title><author>Schardt, Anke ; Brinkmann, Bastian G. ; Mitkovski, Miso ; Sereda, Michael W. ; Werner, Hauke B. ; Nave, Klaus-Armin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4295-150df921a6c267648c3784efcdb99504f58316aa5d68fed7ce939f0eaee8b93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Binding Sites - physiology</topic><topic>Cell Differentiation - physiology</topic><topic>Cell Line</topic><topic>Cell Membrane - metabolism</topic><topic>Cell Membrane - ultrastructure</topic><topic>Cells, Cultured</topic><topic>Central Nervous System - cytology</topic><topic>Central Nervous System - growth & development</topic><topic>Central Nervous System - metabolism</topic><topic>Charcot-Marie-Tooth Disease - metabolism</topic><topic>Charcot-Marie-Tooth Disease - physiopathology</topic><topic>Charcot-Marie-Tooth neuropathy</topic><topic>Cytoskeletal Proteins - metabolism</topic><topic>Disease Models, Animal</topic><topic>Gene Expression Regulation, Developmental - physiology</topic><topic>GTP-Binding Proteins - metabolism</topic><topic>Guanosine Triphosphate - metabolism</topic><topic>Membrane Fusion - physiology</topic><topic>membrane trafficking</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Myelin Proteolipid Protein - metabolism</topic><topic>Myelin Sheath - metabolism</topic><topic>Myelin Sheath - ultrastructure</topic><topic>Nerve Fibers, Myelinated - metabolism</topic><topic>Nerve Fibers, Myelinated - ultrastructure</topic><topic>oligodendrocyte</topic><topic>Protein Binding - physiology</topic><topic>Protein Structure, Tertiary - physiology</topic><topic>Protein Transport - physiology</topic><topic>Qb-SNARE Proteins - metabolism</topic><topic>Qc-SNARE Proteins - metabolism</topic><topic>rab GTP-Binding Proteins - metabolism</topic><topic>rab3A</topic><topic>rab3A GTP-Binding Protein - metabolism</topic><topic>Rats</topic><topic>remyelination</topic><topic>Schwann cell</topic><topic>Septins</topic><topic>SNARE proteins</topic><topic>Synaptic Membranes - metabolism</topic><topic>Two-Hybrid System Techniques</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Schardt, Anke</creatorcontrib><creatorcontrib>Brinkmann, Bastian G.</creatorcontrib><creatorcontrib>Mitkovski, Miso</creatorcontrib><creatorcontrib>Sereda, Michael W.</creatorcontrib><creatorcontrib>Werner, Hauke B.</creatorcontrib><creatorcontrib>Nave, Klaus-Armin</creatorcontrib><collection>Istex</collection><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>Neurosciences Abstracts</collection><jtitle>Journal of neuroscience research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Schardt, Anke</au><au>Brinkmann, Bastian G.</au><au>Mitkovski, Miso</au><au>Sereda, Michael W.</au><au>Werner, Hauke B.</au><au>Nave, Klaus-Armin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The SNARE protein SNAP-29 interacts with the GTPase Rab3A: Implications for membrane trafficking in myelinating glia</atitle><jtitle>Journal of neuroscience research</jtitle><addtitle>J. Neurosci. Res</addtitle><date>2009-11-15</date><risdate>2009</risdate><volume>87</volume><issue>15</issue><spage>3465</spage><epage>3479</epage><pages>3465-3479</pages><issn>0360-4012</issn><issn>1097-4547</issn><eissn>1097-4547</eissn><abstract>During myelin formation, vast amounts of specialized membrane proteins and lipids are trafficked toward the growing sheath in cell surface‐directed transport vesicles. Soluble N‐ethylmaleimide‐sensitive factor (NSF) attachment proteins (SNAPs) are important components of molecular complexes required for membrane fusion. We have analyzed the expression profile and molecular interactions of SNAP‐29 in the nervous system. In addition to its known enrichment in neuronal synapses, SNAP‐29 is abundant in oligodendrocytes during myelination and in noncompact myelin of the peripheral nervous system. By yeast two‐hybrid screen and coimmunoprecipitation, we found that the GTPases Rab3A, Rab24, and septin 4 bind to the N‐terminal domain of SNAP‐29. The interaction with Rab24 or septin 4 was GTP independent. In contrast, interaction between SNAP‐29 and Rab3A was GTP dependent, and colocalization was extensive both in synapses and in myelinating glia. In HEK293 cells, cytoplasmic SNAP‐29 pools were redistributed upon coexpression with Rab3A, and surface‐directed trafficking of myelin proteolipid protein was enhanced by overexpression of SNAP‐29 and Rab3A. Interestingly, the abundance of SNAP‐29 in sciatic nerves was increased during remyelination and in a rat model of Charcot‐Marie‐Tooth disease, two pathological situations with increased myelin membrane biogenesis. We suggest that Rab3A may regulate SNAP‐29‐mediated membrane fusion during myelination. © 2009 Wiley‐Liss, Inc.</abstract><cop>Hoboken</cop><pub>Wiley Subscription Services, Inc., A Wiley Company</pub><pmid>19170188</pmid><doi>10.1002/jnr.22005</doi><tpages>15</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Animals, Newborn Binding Sites - physiology Cell Differentiation - physiology Cell Line Cell Membrane - metabolism Cell Membrane - ultrastructure Cells, Cultured Central Nervous System - cytology Central Nervous System - growth & development Central Nervous System - metabolism Charcot-Marie-Tooth Disease - metabolism Charcot-Marie-Tooth Disease - physiopathology Charcot-Marie-Tooth neuropathy Cytoskeletal Proteins - metabolism Disease Models, Animal Gene Expression Regulation, Developmental - physiology GTP-Binding Proteins - metabolism Guanosine Triphosphate - metabolism Membrane Fusion - physiology membrane trafficking Mice Mice, Inbred C57BL Myelin Proteolipid Protein - metabolism Myelin Sheath - metabolism Myelin Sheath - ultrastructure Nerve Fibers, Myelinated - metabolism Nerve Fibers, Myelinated - ultrastructure oligodendrocyte Protein Binding - physiology Protein Structure, Tertiary - physiology Protein Transport - physiology Qb-SNARE Proteins - metabolism Qc-SNARE Proteins - metabolism rab GTP-Binding Proteins - metabolism rab3A rab3A GTP-Binding Protein - metabolism Rats remyelination Schwann cell Septins SNARE proteins Synaptic Membranes - metabolism Two-Hybrid System Techniques |
| title | The SNARE protein SNAP-29 interacts with the GTPase Rab3A: Implications for membrane trafficking in myelinating glia |
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