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Thermodynamics of Heat Activation of Single Capsaicin Ion Channels VR1
Temperature affects functions of all ion channels, but few of them can be gated directly. The vanilloid receptor VR1 provides one exception. As a pain receptor, it is activated by heat >42°C in addition to other noxious stimuli, e.g. acids and vanilloids. Although it is understood how ligand- and...
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Published in: | Biophysical journal 2003-11, Vol.85 (5), p.2988-3006 |
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description | Temperature affects functions of all ion channels, but few of them can be gated directly. The vanilloid receptor VR1 provides one exception. As a pain receptor, it is activated by heat >42°C in addition to other noxious stimuli, e.g. acids and vanilloids. Although it is understood how ligand- and voltage-gated channels might detect their stimuli, little is known on how heat could be sensed and activate a channel. In this study, we characterized the heat-induced single-channel activity of VR1, in an attempt to localize the temperature-dependent components involved in the activation of the channel. At |
doi_str_mv | 10.1016/S0006-3495(03)74719-5 |
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Q
10 ≈ 27), the unitary current, the open dwell-times, and the intraburst closures were all only weakly temperature dependent (
Q
10
<
2). Instead, heat had a localized effect on the reduction of long closures between bursts (
Q
10 ≈ 7) and the elongation of burst durations (
Q
10 ≈ 32). Both membrane lipids and solution ionic strength affected the temperature threshold of the activation, but neither diminished the response. The thermodynamic basis of heat activation is discussed, to elucidate what makes a thermal-sensitive channel unique.</description><identifier>ISSN: 0006-3495</identifier><identifier>EISSN: 1542-0086</identifier><identifier>DOI: 10.1016/S0006-3495(03)74719-5</identifier><identifier>PMID: 14581201</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Cell Line ; Channels, Receptors, and Transporters ; Cholesterol - metabolism ; Computer Simulation ; Heat ; Hot Temperature ; Humans ; Ion Channel Gating - physiology ; Ion Channel Gating - radiation effects ; Ions ; Kidney - embryology ; Kidney - physiology ; Kidney - radiation effects ; Membrane Potentials - physiology ; Membrane Potentials - radiation effects ; Models, Biological ; Oocytes - physiology ; Oocytes - radiation effects ; Rats ; Receptors, Drug - drug effects ; Receptors, Drug - physiology ; Species Specificity ; Temperature ; Thermodynamics ; Xenopus laevis</subject><ispartof>Biophysical journal, 2003-11, Vol.85 (5), p.2988-3006</ispartof><rights>2003 The Biophysical Society</rights><rights>Copyright Biophysical Society Nov 2003</rights><rights>Copyright © 2003, Biophysical Society 2003</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c556t-474546053c34c8ffa84fc52f4c84139dc36b465f7d959e7e79efb80d7feba4023</citedby><cites>FETCH-LOGICAL-c556t-474546053c34c8ffa84fc52f4c84139dc36b465f7d959e7e79efb80d7feba4023</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/PMC1303577/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC1303577/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27923,27924,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/14581201$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Beiying</creatorcontrib><creatorcontrib>Hui, Kwokyin</creatorcontrib><creatorcontrib>Qin, Feng</creatorcontrib><title>Thermodynamics of Heat Activation of Single Capsaicin Ion Channels VR1</title><title>Biophysical journal</title><addtitle>Biophys J</addtitle><description>Temperature affects functions of all ion channels, but few of them can be gated directly. The vanilloid receptor VR1 provides one exception. As a pain receptor, it is activated by heat >42°C in addition to other noxious stimuli, e.g. acids and vanilloids. Although it is understood how ligand- and voltage-gated channels might detect their stimuli, little is known on how heat could be sensed and activate a channel. In this study, we characterized the heat-induced single-channel activity of VR1, in an attempt to localize the temperature-dependent components involved in the activation of the channel. At <42°C, openings were few and brief. Raising the ambient temperature rapidly increased the frequency of openings. Despite the large temperature coefficient of the apparent activity (
Q
10 ≈ 27), the unitary current, the open dwell-times, and the intraburst closures were all only weakly temperature dependent (
Q
10
<
2). Instead, heat had a localized effect on the reduction of long closures between bursts (
Q
10 ≈ 7) and the elongation of burst durations (
Q
10 ≈ 32). Both membrane lipids and solution ionic strength affected the temperature threshold of the activation, but neither diminished the response. The thermodynamic basis of heat activation is discussed, to elucidate what makes a thermal-sensitive channel unique.</description><subject>Animals</subject><subject>Cell Line</subject><subject>Channels, Receptors, and Transporters</subject><subject>Cholesterol - metabolism</subject><subject>Computer Simulation</subject><subject>Heat</subject><subject>Hot Temperature</subject><subject>Humans</subject><subject>Ion Channel Gating - physiology</subject><subject>Ion Channel Gating - radiation effects</subject><subject>Ions</subject><subject>Kidney - embryology</subject><subject>Kidney - physiology</subject><subject>Kidney - radiation effects</subject><subject>Membrane Potentials - physiology</subject><subject>Membrane Potentials - radiation effects</subject><subject>Models, Biological</subject><subject>Oocytes - physiology</subject><subject>Oocytes - radiation effects</subject><subject>Rats</subject><subject>Receptors, Drug - drug effects</subject><subject>Receptors, Drug - physiology</subject><subject>Species Specificity</subject><subject>Temperature</subject><subject>Thermodynamics</subject><subject>Xenopus laevis</subject><issn>0006-3495</issn><issn>1542-0086</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2003</creationdate><recordtype>article</recordtype><recordid>eNqFkcFu1DAQhi0EotvCI4AiDhUcAuPYEycXqmrV0kqVkGjhanmdcddVYi92dqW-Pdnuqi1cOFkef_Pb44-xdxw-c-D1l2sAqEshW_wI4pOSirclvmAzjrIqAZr6JZs9IgfsMOc7AF4h8NfsgEtseAV8xs5vlpSG2N0HM3ibi-iKCzJjcWpHvzGjj2FbuvbhtqdiblbZeOtDcTnV50sTAvW5-PWDv2GvnOkzvd2vR-zn-dnN_KK8-v7tcn56VVrEeiylkihrQGGFtI1zppHOYuWmjeSi7ayoF7JGp7oWW1KkWnKLBjrlaGEkVOKIfd3lrtaLgTpLYUym16vkB5PudTRe_30S_FLfxo3mAgQqNQUc7wNS_L2mPOrBZ0t9bwLFddZqApVAmMAP_4B3cZ3CNJyuOCqOUG3TcAfZFHNO5B5fwkFvNekHTXrrQIPQD5o0Tn3vn4_x1LX3MgEnO2D6X9p4SjpbT8FS5xPZUXfR_-eKP9oooVo</recordid><startdate>20031101</startdate><enddate>20031101</enddate><creator>Liu, Beiying</creator><creator>Hui, Kwokyin</creator><creator>Qin, Feng</creator><general>Elsevier Inc</general><general>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>3V.</scope><scope>7QO</scope><scope>7QP</scope><scope>7TK</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88I</scope><scope>8AF</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M2P</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>S0X</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20031101</creationdate><title>Thermodynamics of Heat Activation of Single Capsaicin Ion Channels VR1</title><author>Liu, Beiying ; Hui, Kwokyin ; Qin, Feng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c556t-474546053c34c8ffa84fc52f4c84139dc36b465f7d959e7e79efb80d7feba4023</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2003</creationdate><topic>Animals</topic><topic>Cell Line</topic><topic>Channels, Receptors, and Transporters</topic><topic>Cholesterol - metabolism</topic><topic>Computer Simulation</topic><topic>Heat</topic><topic>Hot Temperature</topic><topic>Humans</topic><topic>Ion Channel Gating - physiology</topic><topic>Ion Channel Gating - radiation effects</topic><topic>Ions</topic><topic>Kidney - embryology</topic><topic>Kidney - physiology</topic><topic>Kidney - radiation effects</topic><topic>Membrane Potentials - physiology</topic><topic>Membrane Potentials - radiation effects</topic><topic>Models, Biological</topic><topic>Oocytes - physiology</topic><topic>Oocytes - radiation effects</topic><topic>Rats</topic><topic>Receptors, Drug - drug effects</topic><topic>Receptors, Drug - physiology</topic><topic>Species Specificity</topic><topic>Temperature</topic><topic>Thermodynamics</topic><topic>Xenopus laevis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Beiying</creatorcontrib><creatorcontrib>Hui, Kwokyin</creatorcontrib><creatorcontrib>Qin, Feng</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>ProQuest Central (Corporate)</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>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>STEM Database</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>AUTh Library subscriptions: ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection (Proquest) (PQ_SDU_P3)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Agriculture Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>SIRS Editorial</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>Liu, Beiying</au><au>Hui, Kwokyin</au><au>Qin, Feng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Thermodynamics of Heat Activation of Single Capsaicin Ion Channels VR1</atitle><jtitle>Biophysical journal</jtitle><addtitle>Biophys J</addtitle><date>2003-11-01</date><risdate>2003</risdate><volume>85</volume><issue>5</issue><spage>2988</spage><epage>3006</epage><pages>2988-3006</pages><issn>0006-3495</issn><eissn>1542-0086</eissn><abstract>Temperature affects functions of all ion channels, but few of them can be gated directly. The vanilloid receptor VR1 provides one exception. As a pain receptor, it is activated by heat >42°C in addition to other noxious stimuli, e.g. acids and vanilloids. Although it is understood how ligand- and voltage-gated channels might detect their stimuli, little is known on how heat could be sensed and activate a channel. In this study, we characterized the heat-induced single-channel activity of VR1, in an attempt to localize the temperature-dependent components involved in the activation of the channel. At <42°C, openings were few and brief. Raising the ambient temperature rapidly increased the frequency of openings. Despite the large temperature coefficient of the apparent activity (
Q
10 ≈ 27), the unitary current, the open dwell-times, and the intraburst closures were all only weakly temperature dependent (
Q
10
<
2). Instead, heat had a localized effect on the reduction of long closures between bursts (
Q
10 ≈ 7) and the elongation of burst durations (
Q
10 ≈ 32). Both membrane lipids and solution ionic strength affected the temperature threshold of the activation, but neither diminished the response. The thermodynamic basis of heat activation is discussed, to elucidate what makes a thermal-sensitive channel unique.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>14581201</pmid><doi>10.1016/S0006-3495(03)74719-5</doi><tpages>19</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Cell Line Channels, Receptors, and Transporters Cholesterol - metabolism Computer Simulation Heat Hot Temperature Humans Ion Channel Gating - physiology Ion Channel Gating - radiation effects Ions Kidney - embryology Kidney - physiology Kidney - radiation effects Membrane Potentials - physiology Membrane Potentials - radiation effects Models, Biological Oocytes - physiology Oocytes - radiation effects Rats Receptors, Drug - drug effects Receptors, Drug - physiology Species Specificity Temperature Thermodynamics Xenopus laevis |
title | Thermodynamics of Heat Activation of Single Capsaicin Ion Channels VR1 |
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