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pH sensing by lipids in membranes: The fundamentals of pH-driven migration, polarization and deformations of lipid bilayer assemblies
Most biological molecules contain acido-basic groups that modulate their structure and interactions. A consequence is that pH gradients, local heterogeneities and dynamic variations are used by cells and organisms to drive or regulate specific biological functions including energetic metabolism, ves...
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Published in: | Biochimica et biophysica acta. Biomembranes 2018-10, Vol.1860 (10), p.2042-2063 |
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container_title | Biochimica et biophysica acta. Biomembranes |
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creator | Angelova, Miglena I. Bitbol, Anne-Florence Seigneuret, Michel Staneva, Galya Kodama, Atsuji Sakuma, Yuka Kawakatsu, Toshihiro Imai, Masayuki Puff, Nicolas |
description | Most biological molecules contain acido-basic groups that modulate their structure and interactions. A consequence is that pH gradients, local heterogeneities and dynamic variations are used by cells and organisms to drive or regulate specific biological functions including energetic metabolism, vesicular traffic, migration and spatial patterning of tissues in development. While the direct or regulatory role of pH in protein function is well documented, the role of hydrogen and hydroxyl ions in modulating the properties of lipid assemblies such as bilayer membranes is only beginning to be understood. Here, we review approaches using artificial lipid vesicles that have been instrumental in providing an understanding of the influence of pH gradients and local variations on membrane vectorial motional processes: migration, membrane curvature effects promoting global or local deformations, crowding generation by segregative polarization processes. In the case of pH induced local deformations, an extensive theoretical framework is given and an application to a specific biological issue, namely the structure and stability of mitochondrial cristae, is described. This article is part of a Special Issue entitled: Emergence of Complex Behavior in Biomembranes edited by Marjorie Longo.
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•Membrane lipids are directly affected by pH, due to their acido-basic properties.•pH change can induce lipid vesicle migration and global deformation.•pH change can cause polarization in phase-separated membrane of GUVs.•Localized pH heterogeneities can induce local dynamical membrane deformations.•Mitochondrial cristae formation has been mimicked using lipid-only systems. |
doi_str_mv | 10.1016/j.bbamem.2018.02.026 |
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[Display omitted]
•Membrane lipids are directly affected by pH, due to their acido-basic properties.•pH change can induce lipid vesicle migration and global deformation.•pH change can cause polarization in phase-separated membrane of GUVs.•Localized pH heterogeneities can induce local dynamical membrane deformations.•Mitochondrial cristae formation has been mimicked using lipid-only systems.</description><identifier>ISSN: 0005-2736</identifier><identifier>EISSN: 1879-2642</identifier><identifier>DOI: 10.1016/j.bbamem.2018.02.026</identifier><identifier>PMID: 29501601</identifier><language>eng</language><publisher>Netherlands: Elsevier B.V</publisher><subject>Alzheimer's disease ; Biological Physics ; Giant unilamellar vesicle ; Lipid membrane dynamics ; Local chemical gradient ; Local chemical modification ; Mitochondria ; Physics</subject><ispartof>Biochimica et biophysica acta. Biomembranes, 2018-10, Vol.1860 (10), p.2042-2063</ispartof><rights>2018 Elsevier B.V.</rights><rights>Copyright © 2018 Elsevier B.V. All rights reserved.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c442t-93dc170bc4f4f380bbf1c60409cb68b9456a66db16a5d9ada471da8c1419ac913</citedby><cites>FETCH-LOGICAL-c442t-93dc170bc4f4f380bbf1c60409cb68b9456a66db16a5d9ada471da8c1419ac913</cites><orcidid>0000-0003-1020-494X ; 0000-0002-4460-133X ; 0000-0001-8501-6893</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29501601$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-01901246$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Angelova, Miglena I.</creatorcontrib><creatorcontrib>Bitbol, Anne-Florence</creatorcontrib><creatorcontrib>Seigneuret, Michel</creatorcontrib><creatorcontrib>Staneva, Galya</creatorcontrib><creatorcontrib>Kodama, Atsuji</creatorcontrib><creatorcontrib>Sakuma, Yuka</creatorcontrib><creatorcontrib>Kawakatsu, Toshihiro</creatorcontrib><creatorcontrib>Imai, Masayuki</creatorcontrib><creatorcontrib>Puff, Nicolas</creatorcontrib><title>pH sensing by lipids in membranes: The fundamentals of pH-driven migration, polarization and deformations of lipid bilayer assemblies</title><title>Biochimica et biophysica acta. Biomembranes</title><addtitle>Biochim Biophys Acta Biomembr</addtitle><description>Most biological molecules contain acido-basic groups that modulate their structure and interactions. A consequence is that pH gradients, local heterogeneities and dynamic variations are used by cells and organisms to drive or regulate specific biological functions including energetic metabolism, vesicular traffic, migration and spatial patterning of tissues in development. While the direct or regulatory role of pH in protein function is well documented, the role of hydrogen and hydroxyl ions in modulating the properties of lipid assemblies such as bilayer membranes is only beginning to be understood. Here, we review approaches using artificial lipid vesicles that have been instrumental in providing an understanding of the influence of pH gradients and local variations on membrane vectorial motional processes: migration, membrane curvature effects promoting global or local deformations, crowding generation by segregative polarization processes. In the case of pH induced local deformations, an extensive theoretical framework is given and an application to a specific biological issue, namely the structure and stability of mitochondrial cristae, is described. This article is part of a Special Issue entitled: Emergence of Complex Behavior in Biomembranes edited by Marjorie Longo.
[Display omitted]
•Membrane lipids are directly affected by pH, due to their acido-basic properties.•pH change can induce lipid vesicle migration and global deformation.•pH change can cause polarization in phase-separated membrane of GUVs.•Localized pH heterogeneities can induce local dynamical membrane deformations.•Mitochondrial cristae formation has been mimicked using lipid-only systems.</description><subject>Alzheimer's disease</subject><subject>Biological Physics</subject><subject>Giant unilamellar vesicle</subject><subject>Lipid membrane dynamics</subject><subject>Local chemical gradient</subject><subject>Local chemical modification</subject><subject>Mitochondria</subject><subject>Physics</subject><issn>0005-2736</issn><issn>1879-2642</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp9kU9rGzEQxUVpaNy036AUHVvIuiOtVl71EAghrQuGXNKz0L9NZHalrbQ2uPd878jeNMfCgDTD770HMwh9IrAkQPi37VJrNbhhSYG0S6Cl-Bu0IO1KVJQz-hYtAKCp6Krm5-h9zlsoMkabd-iciqb8gSzQ07jG2YXswwPWB9z70duMfcDFWScVXP6O7x8d7nbBlrQwqT7j2OFxXdnk966A_iGpycdwicfYq-T_njqsgsXWdTENp_6kOtlj7Xt1cAmrnEtI713-gM66Yuw-vrwX6PeP2_ubdbW5-_nr5npTGcboVInaGrICbVjHuroFrTtiODAQRvNWC9ZwxbnVhKvGCmUVWxGrWkMYEcoIUl-gr7Pvo-rlmPyg0kFG5eX6eiOPMyACCGV8f2S_zOyY4p-dy5McfDau78tS4i7LsnZoWQ0gCspm1KSYc3LdqzcBeTyW3Mr5WEdVK4GW4kX2-SVhpwdnX0X_rlOAqxlwZSd775LMxrtgnPXJmUna6P-f8Ax2tKiH</recordid><startdate>20181001</startdate><enddate>20181001</enddate><creator>Angelova, Miglena I.</creator><creator>Bitbol, Anne-Florence</creator><creator>Seigneuret, Michel</creator><creator>Staneva, Galya</creator><creator>Kodama, Atsuji</creator><creator>Sakuma, Yuka</creator><creator>Kawakatsu, Toshihiro</creator><creator>Imai, Masayuki</creator><creator>Puff, Nicolas</creator><general>Elsevier B.V</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0003-1020-494X</orcidid><orcidid>https://orcid.org/0000-0002-4460-133X</orcidid><orcidid>https://orcid.org/0000-0001-8501-6893</orcidid></search><sort><creationdate>20181001</creationdate><title>pH sensing by lipids in membranes: The fundamentals of pH-driven migration, polarization and deformations of lipid bilayer assemblies</title><author>Angelova, Miglena I. ; Bitbol, Anne-Florence ; Seigneuret, Michel ; Staneva, Galya ; Kodama, Atsuji ; Sakuma, Yuka ; Kawakatsu, Toshihiro ; Imai, Masayuki ; Puff, Nicolas</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-93dc170bc4f4f380bbf1c60409cb68b9456a66db16a5d9ada471da8c1419ac913</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Alzheimer's disease</topic><topic>Biological Physics</topic><topic>Giant unilamellar vesicle</topic><topic>Lipid membrane dynamics</topic><topic>Local chemical gradient</topic><topic>Local chemical modification</topic><topic>Mitochondria</topic><topic>Physics</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Angelova, Miglena I.</creatorcontrib><creatorcontrib>Bitbol, Anne-Florence</creatorcontrib><creatorcontrib>Seigneuret, Michel</creatorcontrib><creatorcontrib>Staneva, Galya</creatorcontrib><creatorcontrib>Kodama, Atsuji</creatorcontrib><creatorcontrib>Sakuma, Yuka</creatorcontrib><creatorcontrib>Kawakatsu, Toshihiro</creatorcontrib><creatorcontrib>Imai, Masayuki</creatorcontrib><creatorcontrib>Puff, Nicolas</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><jtitle>Biochimica et biophysica acta. Biomembranes</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Angelova, Miglena I.</au><au>Bitbol, Anne-Florence</au><au>Seigneuret, Michel</au><au>Staneva, Galya</au><au>Kodama, Atsuji</au><au>Sakuma, Yuka</au><au>Kawakatsu, Toshihiro</au><au>Imai, Masayuki</au><au>Puff, Nicolas</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>pH sensing by lipids in membranes: The fundamentals of pH-driven migration, polarization and deformations of lipid bilayer assemblies</atitle><jtitle>Biochimica et biophysica acta. Biomembranes</jtitle><addtitle>Biochim Biophys Acta Biomembr</addtitle><date>2018-10-01</date><risdate>2018</risdate><volume>1860</volume><issue>10</issue><spage>2042</spage><epage>2063</epage><pages>2042-2063</pages><issn>0005-2736</issn><eissn>1879-2642</eissn><abstract>Most biological molecules contain acido-basic groups that modulate their structure and interactions. A consequence is that pH gradients, local heterogeneities and dynamic variations are used by cells and organisms to drive or regulate specific biological functions including energetic metabolism, vesicular traffic, migration and spatial patterning of tissues in development. While the direct or regulatory role of pH in protein function is well documented, the role of hydrogen and hydroxyl ions in modulating the properties of lipid assemblies such as bilayer membranes is only beginning to be understood. Here, we review approaches using artificial lipid vesicles that have been instrumental in providing an understanding of the influence of pH gradients and local variations on membrane vectorial motional processes: migration, membrane curvature effects promoting global or local deformations, crowding generation by segregative polarization processes. In the case of pH induced local deformations, an extensive theoretical framework is given and an application to a specific biological issue, namely the structure and stability of mitochondrial cristae, is described. This article is part of a Special Issue entitled: Emergence of Complex Behavior in Biomembranes edited by Marjorie Longo.
[Display omitted]
•Membrane lipids are directly affected by pH, due to their acido-basic properties.•pH change can induce lipid vesicle migration and global deformation.•pH change can cause polarization in phase-separated membrane of GUVs.•Localized pH heterogeneities can induce local dynamical membrane deformations.•Mitochondrial cristae formation has been mimicked using lipid-only systems.</abstract><cop>Netherlands</cop><pub>Elsevier B.V</pub><pmid>29501601</pmid><doi>10.1016/j.bbamem.2018.02.026</doi><tpages>22</tpages><orcidid>https://orcid.org/0000-0003-1020-494X</orcidid><orcidid>https://orcid.org/0000-0002-4460-133X</orcidid><orcidid>https://orcid.org/0000-0001-8501-6893</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Alzheimer's disease Biological Physics Giant unilamellar vesicle Lipid membrane dynamics Local chemical gradient Local chemical modification Mitochondria Physics |
title | pH sensing by lipids in membranes: The fundamentals of pH-driven migration, polarization and deformations of lipid bilayer assemblies |
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