Epsin N-terminal Homology Domain (ENTH) Activity as a Function of Membrane Tension
The epsin N-terminal homology domain (ENTH) is a major player in clathrin-mediated endocytosis. To investigate the influence of initial membrane tension on ENTH binding and activity, we established a bilayer system based on adhered giant unilamellar vesicles (GUVs) to be able to control and adjust t...
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| Veröffentlicht in: | The Journal of biological chemistry 2016-09, Vol.291 (38), p.19953-19961 |
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| container_title | The Journal of biological chemistry |
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| creator | Gleisner, Martin Kroppen, Benjamin Fricke, Christian Teske, Nelli Kliesch, Torben-Tobias Janshoff, Andreas Meinecke, Michael Steinem, Claudia |
| description | The epsin N-terminal homology domain (ENTH) is a major player in clathrin-mediated endocytosis. To investigate the influence of initial membrane tension on ENTH binding and activity, we established a bilayer system based on adhered giant unilamellar vesicles (GUVs) to be able to control and adjust the membrane tension σ covering a broad regime. The shape of each individual adhered GUV as well as its adhesion area was monitored by spinning disc confocal laser microscopy. Control of σ in a range of 0.08-1.02 mN/m was achieved by altering the Mg2+ concentration in solution, which changes the surface adhesion energy per unit area of the GUVs. Specific binding of ENTH to phosphatidylinositol 4,5-bisphosphate leads to a substantial increase in adhesion area of the sessile GUV. At low tension ( |
| doi_str_mv | 10.1074/jbc.M116.731612 |
| format | Article |
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To investigate the influence of initial membrane tension on ENTH binding and activity, we established a bilayer system based on adhered giant unilamellar vesicles (GUVs) to be able to control and adjust the membrane tension σ covering a broad regime. The shape of each individual adhered GUV as well as its adhesion area was monitored by spinning disc confocal laser microscopy. Control of σ in a range of 0.08-1.02 mN/m was achieved by altering the Mg2+ concentration in solution, which changes the surface adhesion energy per unit area of the GUVs. Specific binding of ENTH to phosphatidylinositol 4,5-bisphosphate leads to a substantial increase in adhesion area of the sessile GUV. At low tension (<0.1 mN/m) binding of ENTH can induce tubular structures, whereas at higher membrane tension the ENTH interaction deflates the sessile GUV and thereby increases the adhesion area. The increase in adhesion area is mainly attributed to a decrease in the area compressibility modulus KA. We propose that the insertion of the ENTH helix-0 into the membrane is largely responsible for the observed decrease in KA, which is supported by the observation that the mutant ENTH L6E shows a reduced increase in adhesion area. These results demonstrate that even in the absence of tubule formation, the area compressibility modulus and, as such, the bending rigidity of the membrane is considerably reduced upon ENTH binding. This renders membrane bending and tubule formation energetically less costly.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.M116.731612</identifier><identifier>PMID: 27466364</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Adaptor Proteins, Vesicular Transport - chemistry ; endocytosis ; fluorescence ; Humans ; lipid vesicle ; lipid-protein interaction ; Membrane Biology ; membrane protein ; Protein Domains ; Protein Structure, Secondary ; Surface Tension ; Unilamellar Liposomes - chemistry</subject><ispartof>The Journal of biological chemistry, 2016-09, Vol.291 (38), p.19953-19961</ispartof><rights>2016 © 2016 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology</rights><rights>2016 by The American Society for Biochemistry and Molecular Biology, Inc.</rights><rights>2016 by The American Society for Biochemistry and Molecular Biology, Inc. 2016 The American Society for Biochemistry and Molecular Biology, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c509t-b46a0e1df72d158aec9bdcb7f061b67e20795b96ade16343b9a214b6b66ee9923</citedby><cites>FETCH-LOGICAL-c509t-b46a0e1df72d158aec9bdcb7f061b67e20795b96ade16343b9a214b6b66ee9923</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/PMC5025682/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC5025682/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27466364$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gleisner, Martin</creatorcontrib><creatorcontrib>Kroppen, Benjamin</creatorcontrib><creatorcontrib>Fricke, Christian</creatorcontrib><creatorcontrib>Teske, Nelli</creatorcontrib><creatorcontrib>Kliesch, Torben-Tobias</creatorcontrib><creatorcontrib>Janshoff, Andreas</creatorcontrib><creatorcontrib>Meinecke, Michael</creatorcontrib><creatorcontrib>Steinem, Claudia</creatorcontrib><title>Epsin N-terminal Homology Domain (ENTH) Activity as a Function of Membrane Tension</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>The epsin N-terminal homology domain (ENTH) is a major player in clathrin-mediated endocytosis. To investigate the influence of initial membrane tension on ENTH binding and activity, we established a bilayer system based on adhered giant unilamellar vesicles (GUVs) to be able to control and adjust the membrane tension σ covering a broad regime. The shape of each individual adhered GUV as well as its adhesion area was monitored by spinning disc confocal laser microscopy. Control of σ in a range of 0.08-1.02 mN/m was achieved by altering the Mg2+ concentration in solution, which changes the surface adhesion energy per unit area of the GUVs. Specific binding of ENTH to phosphatidylinositol 4,5-bisphosphate leads to a substantial increase in adhesion area of the sessile GUV. At low tension (<0.1 mN/m) binding of ENTH can induce tubular structures, whereas at higher membrane tension the ENTH interaction deflates the sessile GUV and thereby increases the adhesion area. The increase in adhesion area is mainly attributed to a decrease in the area compressibility modulus KA. We propose that the insertion of the ENTH helix-0 into the membrane is largely responsible for the observed decrease in KA, which is supported by the observation that the mutant ENTH L6E shows a reduced increase in adhesion area. These results demonstrate that even in the absence of tubule formation, the area compressibility modulus and, as such, the bending rigidity of the membrane is considerably reduced upon ENTH binding. This renders membrane bending and tubule formation energetically less costly.</description><subject>Adaptor Proteins, Vesicular Transport - chemistry</subject><subject>endocytosis</subject><subject>fluorescence</subject><subject>Humans</subject><subject>lipid vesicle</subject><subject>lipid-protein interaction</subject><subject>Membrane Biology</subject><subject>membrane protein</subject><subject>Protein Domains</subject><subject>Protein Structure, Secondary</subject><subject>Surface Tension</subject><subject>Unilamellar Liposomes - chemistry</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kUFPJCEQhcnGzTqre96b4aiHHoHuhuZiYnTcMVE3MWPijQBd7WK6YYSeSebfy2TUrAfrQqrq4xXUQ-g3JVNKRHX6bOz0llI-FSXllH1DE0qasihr-riHJoQwWkhWN_voZ0rPJEcl6Q-0z0TFecmrCbqfLZPz-K4YIQ7O6x7PwxD68LTBl2HQuXU8u1vMT_C5Hd3ajRusE9b4auVzHjwOHb6FwUTtAS_Ap1w7RN873Sf49XYeoIer2eJiXtz8_XN9cX5T2JrIsTAV1wRo2wnW0rrRYKVprREd4dRwAYwIWRvJdQuUl1VppGa0MtxwDiAlKw_Q2U53uTIDtBb8GHWvltENOm5U0E597nj3Tz2FtaoJq3mzFTh-E4jhZQVpVINLFvo-fyaskqINI5wwIbbo6Q61MaQUofsYQ4naOqGyE2rrhNo5kW8c_f-6D_599RmQOwDyjtYOokrWgbfQugh2VG1wX4q_AhOxl_g</recordid><startdate>20160916</startdate><enddate>20160916</enddate><creator>Gleisner, Martin</creator><creator>Kroppen, Benjamin</creator><creator>Fricke, Christian</creator><creator>Teske, Nelli</creator><creator>Kliesch, Torben-Tobias</creator><creator>Janshoff, Andreas</creator><creator>Meinecke, Michael</creator><creator>Steinem, Claudia</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</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>7X8</scope><scope>5PM</scope></search><sort><creationdate>20160916</creationdate><title>Epsin N-terminal Homology Domain (ENTH) Activity as a Function of Membrane Tension</title><author>Gleisner, Martin ; Kroppen, Benjamin ; Fricke, Christian ; Teske, Nelli ; Kliesch, Torben-Tobias ; Janshoff, Andreas ; Meinecke, Michael ; Steinem, Claudia</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c509t-b46a0e1df72d158aec9bdcb7f061b67e20795b96ade16343b9a214b6b66ee9923</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Adaptor Proteins, Vesicular Transport - chemistry</topic><topic>endocytosis</topic><topic>fluorescence</topic><topic>Humans</topic><topic>lipid vesicle</topic><topic>lipid-protein interaction</topic><topic>Membrane Biology</topic><topic>membrane protein</topic><topic>Protein Domains</topic><topic>Protein Structure, Secondary</topic><topic>Surface Tension</topic><topic>Unilamellar Liposomes - chemistry</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gleisner, Martin</creatorcontrib><creatorcontrib>Kroppen, Benjamin</creatorcontrib><creatorcontrib>Fricke, Christian</creatorcontrib><creatorcontrib>Teske, Nelli</creatorcontrib><creatorcontrib>Kliesch, Torben-Tobias</creatorcontrib><creatorcontrib>Janshoff, Andreas</creatorcontrib><creatorcontrib>Meinecke, Michael</creatorcontrib><creatorcontrib>Steinem, Claudia</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>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gleisner, Martin</au><au>Kroppen, Benjamin</au><au>Fricke, Christian</au><au>Teske, Nelli</au><au>Kliesch, Torben-Tobias</au><au>Janshoff, Andreas</au><au>Meinecke, Michael</au><au>Steinem, Claudia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Epsin N-terminal Homology Domain (ENTH) Activity as a Function of Membrane Tension</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2016-09-16</date><risdate>2016</risdate><volume>291</volume><issue>38</issue><spage>19953</spage><epage>19961</epage><pages>19953-19961</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>The epsin N-terminal homology domain (ENTH) is a major player in clathrin-mediated endocytosis. To investigate the influence of initial membrane tension on ENTH binding and activity, we established a bilayer system based on adhered giant unilamellar vesicles (GUVs) to be able to control and adjust the membrane tension σ covering a broad regime. The shape of each individual adhered GUV as well as its adhesion area was monitored by spinning disc confocal laser microscopy. Control of σ in a range of 0.08-1.02 mN/m was achieved by altering the Mg2+ concentration in solution, which changes the surface adhesion energy per unit area of the GUVs. Specific binding of ENTH to phosphatidylinositol 4,5-bisphosphate leads to a substantial increase in adhesion area of the sessile GUV. At low tension (<0.1 mN/m) binding of ENTH can induce tubular structures, whereas at higher membrane tension the ENTH interaction deflates the sessile GUV and thereby increases the adhesion area. The increase in adhesion area is mainly attributed to a decrease in the area compressibility modulus KA. We propose that the insertion of the ENTH helix-0 into the membrane is largely responsible for the observed decrease in KA, which is supported by the observation that the mutant ENTH L6E shows a reduced increase in adhesion area. These results demonstrate that even in the absence of tubule formation, the area compressibility modulus and, as such, the bending rigidity of the membrane is considerably reduced upon ENTH binding. This renders membrane bending and tubule formation energetically less costly.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>27466364</pmid><doi>10.1074/jbc.M116.731612</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Adaptor Proteins, Vesicular Transport - chemistry endocytosis fluorescence Humans lipid vesicle lipid-protein interaction Membrane Biology membrane protein Protein Domains Protein Structure, Secondary Surface Tension Unilamellar Liposomes - chemistry |
| title | Epsin N-terminal Homology Domain (ENTH) Activity as a Function of Membrane Tension |
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