Charge as a selection criterion for translocation through the nuclear pore complex
Nuclear pore complexes (NPCs) are highly selective filters that control the exchange of material between nucleus and cytoplasm. The principles that govern selective filtering by NPCs are not fully understood. Previous studies find that cellular proteins capable of fast translocation through NPCs (tr...
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description | Nuclear pore complexes (NPCs) are highly selective filters that control the exchange of material between nucleus and cytoplasm. The principles that govern selective filtering by NPCs are not fully understood. Previous studies find that cellular proteins capable of fast translocation through NPCs (transport receptors) are characterized by a high proportion of hydrophobic surface regions. Our analysis finds that transport receptors and their complexes are also highly negatively charged. Moreover, NPC components that constitute the permeability barrier are positively charged. We estimate that electrostatic interactions between a transport receptor and the NPC result in an energy gain of several k(B)T, which would enable significantly increased translocation rates of transport receptors relative to other cellular proteins. We suggest that negative charge is an essential criterion for selective passage through the NPC. |
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The principles that govern selective filtering by NPCs are not fully understood. Previous studies find that cellular proteins capable of fast translocation through NPCs (transport receptors) are characterized by a high proportion of hydrophobic surface regions. Our analysis finds that transport receptors and their complexes are also highly negatively charged. Moreover, NPC components that constitute the permeability barrier are positively charged. We estimate that electrostatic interactions between a transport receptor and the NPC result in an energy gain of several k(B)T, which would enable significantly increased translocation rates of transport receptors relative to other cellular proteins. We suggest that negative charge is an essential criterion for selective passage through the NPC.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1000747</identifier><identifier>PMID: 20421988</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino Acid Sequence ; Biological transport ; Biophysics/Macromolecular Assemblies and Machines ; Cell Biology ; Cluster Analysis ; Computational Biology/Systems Biology ; Crystal structure ; Cytoplasm ; Fungal Proteins - metabolism ; Genetic aspects ; Humans ; Hydrophobic and Hydrophilic Interactions ; Hydrophobicity ; Identification and classification ; Measurement ; Models, Biological ; Molecular Sequence Data ; Nuclear Pore - chemistry ; Nuclear Pore - metabolism ; Nuclear Pore - physiology ; Nuclear Pore Complex Proteins - metabolism ; Physics/Condensed Matter ; Protein Binding ; Protein Transport - physiology ; Protein-protein interactions ; Proteins ; Saccharomyces cerevisiae ; Standard deviation ; Static Electricity ; Thermodynamics ; Translocation (Genetics)</subject><ispartof>PLoS computational biology, 2010-04, Vol.6 (4), p.e1000747-e1000747</ispartof><rights>COPYRIGHT 2010 Public Library of Science</rights><rights>Colwell et al. 2010</rights><rights>2010 Colwell et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Colwell LJ, Brenner MP, Ribbeck K (2010) Charge as a Selection Criterion for Translocation through the Nuclear Pore Complex. PLoS Comput Biol 6(4): e1000747. doi:10.1371/journal.pcbi.1000747</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c670t-1ffde106e53b0e132b056b18697cbc70e9076c8bcb5cd345eb377648855075033</citedby><cites>FETCH-LOGICAL-c670t-1ffde106e53b0e132b056b18697cbc70e9076c8bcb5cd345eb377648855075033</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/PMC2858669/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2858669/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/20421988$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Gilson, Michael</contributor><creatorcontrib>Colwell, Lucy J</creatorcontrib><creatorcontrib>Brenner, Michael P</creatorcontrib><creatorcontrib>Ribbeck, Katharina</creatorcontrib><title>Charge as a selection criterion for translocation through the nuclear pore complex</title><title>PLoS computational biology</title><addtitle>PLoS Comput Biol</addtitle><description>Nuclear pore complexes (NPCs) are highly selective filters that control the exchange of material between nucleus and cytoplasm. The principles that govern selective filtering by NPCs are not fully understood. Previous studies find that cellular proteins capable of fast translocation through NPCs (transport receptors) are characterized by a high proportion of hydrophobic surface regions. Our analysis finds that transport receptors and their complexes are also highly negatively charged. Moreover, NPC components that constitute the permeability barrier are positively charged. We estimate that electrostatic interactions between a transport receptor and the NPC result in an energy gain of several k(B)T, which would enable significantly increased translocation rates of transport receptors relative to other cellular proteins. We suggest that negative charge is an essential criterion for selective passage through the NPC.</description><subject>Amino Acid Sequence</subject><subject>Biological transport</subject><subject>Biophysics/Macromolecular Assemblies and Machines</subject><subject>Cell Biology</subject><subject>Cluster Analysis</subject><subject>Computational Biology/Systems Biology</subject><subject>Crystal structure</subject><subject>Cytoplasm</subject><subject>Fungal Proteins - metabolism</subject><subject>Genetic aspects</subject><subject>Humans</subject><subject>Hydrophobic and Hydrophilic Interactions</subject><subject>Hydrophobicity</subject><subject>Identification and classification</subject><subject>Measurement</subject><subject>Models, Biological</subject><subject>Molecular Sequence Data</subject><subject>Nuclear Pore - chemistry</subject><subject>Nuclear Pore - metabolism</subject><subject>Nuclear Pore - physiology</subject><subject>Nuclear Pore Complex Proteins - metabolism</subject><subject>Physics/Condensed Matter</subject><subject>Protein Binding</subject><subject>Protein Transport - physiology</subject><subject>Protein-protein interactions</subject><subject>Proteins</subject><subject>Saccharomyces cerevisiae</subject><subject>Standard deviation</subject><subject>Static Electricity</subject><subject>Thermodynamics</subject><subject>Translocation (Genetics)</subject><issn>1553-7358</issn><issn>1553-734X</issn><issn>1553-7358</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2010</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVUk1v1DAQjRCIlsI_QJAb4rCLHX_mglStKKxUgVTgbNnOJOuVEwc7QeXf19tNq-4RzWFGM2-ePU-vKN5itMZE4E_7MMdB-_VojVtjhJCg4llxjhkjK0GYfP6kPitepbRHKJc1f1mcVYhWuJbyvLjZ7HTsoNSp1GUCD3ZyYShtdBPEQ9WGWE5RD8kHq-9n0y6GudvlDOUwWw86lmOIUNrQjx5uXxcvWu0TvFnyRfH76suvzbfV9Y-v283l9cpygaYVbtsGMOLAiEGASWUQ4wZLXgtrrEBQI8GtNNYw2xDKwBAhOJWSMSQYIuSieH_kHX1IapEjKUxyiKqmMiO2R0QT9F6N0fU6_lNBO3XfCLFTOk4un6BY2xjCSBas1pRiqFmDa902GlVSagaZ6_Py2mx6aCwMWRV_Qno6GdxOdeGvqiSTnNeZ4MNCEMOfGdKkepcseK8HCHNSghBOESWHw9ZHZKfzz9zQhkxoczTQOxsGaF3uX1YVq7MkkueFjycLGTPB7dTpOSW1_XnzH9jvp1h6xNoYUorQPp6LkTqY8EF1dTChWkyY1949lepx6cF15A7DUdld</recordid><startdate>20100401</startdate><enddate>20100401</enddate><creator>Colwell, Lucy J</creator><creator>Brenner, Michael P</creator><creator>Ribbeck, Katharina</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20100401</creationdate><title>Charge as a selection criterion for translocation through the nuclear pore complex</title><author>Colwell, Lucy J ; Brenner, Michael P ; Ribbeck, Katharina</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c670t-1ffde106e53b0e132b056b18697cbc70e9076c8bcb5cd345eb377648855075033</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2010</creationdate><topic>Amino Acid Sequence</topic><topic>Biological transport</topic><topic>Biophysics/Macromolecular Assemblies and Machines</topic><topic>Cell Biology</topic><topic>Cluster Analysis</topic><topic>Computational Biology/Systems Biology</topic><topic>Crystal structure</topic><topic>Cytoplasm</topic><topic>Fungal Proteins - metabolism</topic><topic>Genetic aspects</topic><topic>Humans</topic><topic>Hydrophobic and Hydrophilic Interactions</topic><topic>Hydrophobicity</topic><topic>Identification and classification</topic><topic>Measurement</topic><topic>Models, Biological</topic><topic>Molecular Sequence Data</topic><topic>Nuclear Pore - chemistry</topic><topic>Nuclear Pore - metabolism</topic><topic>Nuclear Pore - physiology</topic><topic>Nuclear Pore Complex Proteins - metabolism</topic><topic>Physics/Condensed Matter</topic><topic>Protein Binding</topic><topic>Protein Transport - physiology</topic><topic>Protein-protein interactions</topic><topic>Proteins</topic><topic>Saccharomyces cerevisiae</topic><topic>Standard deviation</topic><topic>Static Electricity</topic><topic>Thermodynamics</topic><topic>Translocation (Genetics)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Colwell, Lucy J</creatorcontrib><creatorcontrib>Brenner, Michael P</creatorcontrib><creatorcontrib>Ribbeck, Katharina</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Colwell, Lucy J</au><au>Brenner, Michael P</au><au>Ribbeck, Katharina</au><au>Gilson, Michael</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Charge as a selection criterion for translocation through the nuclear pore complex</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2010-04-01</date><risdate>2010</risdate><volume>6</volume><issue>4</issue><spage>e1000747</spage><epage>e1000747</epage><pages>e1000747-e1000747</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>Nuclear pore complexes (NPCs) are highly selective filters that control the exchange of material between nucleus and cytoplasm. The principles that govern selective filtering by NPCs are not fully understood. Previous studies find that cellular proteins capable of fast translocation through NPCs (transport receptors) are characterized by a high proportion of hydrophobic surface regions. Our analysis finds that transport receptors and their complexes are also highly negatively charged. Moreover, NPC components that constitute the permeability barrier are positively charged. We estimate that electrostatic interactions between a transport receptor and the NPC result in an energy gain of several k(B)T, which would enable significantly increased translocation rates of transport receptors relative to other cellular proteins. We suggest that negative charge is an essential criterion for selective passage through the NPC.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>20421988</pmid><doi>10.1371/journal.pcbi.1000747</doi><oa>free_for_read</oa></addata></record> |
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subjects | Amino Acid Sequence Biological transport Biophysics/Macromolecular Assemblies and Machines Cell Biology Cluster Analysis Computational Biology/Systems Biology Crystal structure Cytoplasm Fungal Proteins - metabolism Genetic aspects Humans Hydrophobic and Hydrophilic Interactions Hydrophobicity Identification and classification Measurement Models, Biological Molecular Sequence Data Nuclear Pore - chemistry Nuclear Pore - metabolism Nuclear Pore - physiology Nuclear Pore Complex Proteins - metabolism Physics/Condensed Matter Protein Binding Protein Transport - physiology Protein-protein interactions Proteins Saccharomyces cerevisiae Standard deviation Static Electricity Thermodynamics Translocation (Genetics) |
title | Charge as a selection criterion for translocation through the nuclear pore complex |
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