Recovery from tachyphylaxis of TRPV1 coincides with recycling to the surface membrane
The transient receptor potential vanilloid-1 (TRPV1) ion channel is essential for sensation of thermal and chemical pain. TRPV1 activation is accompanied by Ca2+-dependent desensitization; acute desensitization reflects rapid reduction in channel activity during stimulation, whereas tachyphylaxis de...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2019-03, Vol.116 (11), p.5170-5175 |
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| creator | Tian, Quan Hu, Juan Xie, Chang Mei, Kaidi Pham, Cuong Mo, Xiaoyi Hepp, Régine Soares, Sylvia Nothias, Fatiha Wang, Yuanyuan Liu, Qiang Cai, Fen Zhong, Bo Li, Dongdong Yao, Jing |
| description | The transient receptor potential vanilloid-1 (TRPV1) ion channel is essential for sensation of thermal and chemical pain. TRPV1 activation is accompanied by Ca2+-dependent desensitization; acute desensitization reflects rapid reduction in channel activity during stimulation, whereas tachyphylaxis denotes the diminution in TRPV1 responses to repetitive stimulation. Acute desensitization has been attributed to conformational changes of the TRPV1 channel; however, the mechanisms underlying the establishment of tachyphylaxis remain to be defined. Here, we report that the degree of whole-cell TRPV1 tachyphylaxis is regulated by the strength of inducing stimulation. Using light-sheet microscopy and pH-sensitive sensor pHluorin to follow TRPV1 endocytosis and exocytosis trafficking, we provide real-time information that tachyphylaxis of different degrees concurs with TRPV1 recycling to the plasma membrane in a proportional manner. This process controls TRPV1 surface expression level thereby the whole-cell nociceptive response. We further show that activity-gated TRPV1 trafficking associates with intracellular Ca2+ signals of distinct kinetics, and recruits recycling routes mediated by synaptotagmin 1 and 7, respectively. These results suggest that activity-dependent TRPV1 recycling contributes to the establishment of tachyphylaxis. |
| doi_str_mv | 10.1073/pnas.1819635116 |
| format | Article |
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TRPV1 activation is accompanied by Ca2+-dependent desensitization; acute desensitization reflects rapid reduction in channel activity during stimulation, whereas tachyphylaxis denotes the diminution in TRPV1 responses to repetitive stimulation. Acute desensitization has been attributed to conformational changes of the TRPV1 channel; however, the mechanisms underlying the establishment of tachyphylaxis remain to be defined. Here, we report that the degree of whole-cell TRPV1 tachyphylaxis is regulated by the strength of inducing stimulation. Using light-sheet microscopy and pH-sensitive sensor pHluorin to follow TRPV1 endocytosis and exocytosis trafficking, we provide real-time information that tachyphylaxis of different degrees concurs with TRPV1 recycling to the plasma membrane in a proportional manner. This process controls TRPV1 surface expression level thereby the whole-cell nociceptive response. We further show that activity-gated TRPV1 trafficking associates with intracellular Ca2+ signals of distinct kinetics, and recruits recycling routes mediated by synaptotagmin 1 and 7, respectively. These results suggest that activity-dependent TRPV1 recycling contributes to the establishment of tachyphylaxis.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1819635116</identifier><identifier>PMID: 30804201</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Biological Sciences ; Calcium (intracellular) ; Calcium ions ; Calcium Signaling ; Calcium signalling ; Capsaicin receptors ; Cell Membrane - metabolism ; Channel gating ; Desensitization ; Endocytosis ; Exocytosis ; HEK293 Cells ; Humans ; Ion channels ; Kinetics ; Life Sciences ; Light ; Organic chemistry ; Pain ; Pain perception ; pH effects ; Process control ; Process controls ; Protein Transport ; Protein turnover ; Rats ; Stimulation ; Synaptotagmin ; Synaptotagmins - metabolism ; Tachyphylaxis ; Transient receptor potential proteins ; TRPV Cation Channels - metabolism</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2019-03, Vol.116 (11), p.5170-5175</ispartof><rights>Copyright National Academy of Sciences Mar 12, 2019</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2019</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c477t-b38430c235e61f66061590e3f06ff809cb61b8efce02f0e2795192420edd94343</citedby><cites>FETCH-LOGICAL-c477t-b38430c235e61f66061590e3f06ff809cb61b8efce02f0e2795192420edd94343</cites><orcidid>0000-0002-7683-7451 ; 0000-0003-2459-6956 ; 0000-0002-6731-4771 ; 0000-0003-1301-9758 ; 0000-0002-2497-2096</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26672219$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26672219$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,723,776,780,799,881,27901,27902,53766,53768,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30804201$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02417704$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Tian, Quan</creatorcontrib><creatorcontrib>Hu, Juan</creatorcontrib><creatorcontrib>Xie, Chang</creatorcontrib><creatorcontrib>Mei, Kaidi</creatorcontrib><creatorcontrib>Pham, Cuong</creatorcontrib><creatorcontrib>Mo, Xiaoyi</creatorcontrib><creatorcontrib>Hepp, Régine</creatorcontrib><creatorcontrib>Soares, Sylvia</creatorcontrib><creatorcontrib>Nothias, Fatiha</creatorcontrib><creatorcontrib>Wang, Yuanyuan</creatorcontrib><creatorcontrib>Liu, Qiang</creatorcontrib><creatorcontrib>Cai, Fen</creatorcontrib><creatorcontrib>Zhong, Bo</creatorcontrib><creatorcontrib>Li, Dongdong</creatorcontrib><creatorcontrib>Yao, Jing</creatorcontrib><title>Recovery from tachyphylaxis of TRPV1 coincides with recycling to the surface membrane</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>The transient receptor potential vanilloid-1 (TRPV1) ion channel is essential for sensation of thermal and chemical pain. TRPV1 activation is accompanied by Ca2+-dependent desensitization; acute desensitization reflects rapid reduction in channel activity during stimulation, whereas tachyphylaxis denotes the diminution in TRPV1 responses to repetitive stimulation. Acute desensitization has been attributed to conformational changes of the TRPV1 channel; however, the mechanisms underlying the establishment of tachyphylaxis remain to be defined. Here, we report that the degree of whole-cell TRPV1 tachyphylaxis is regulated by the strength of inducing stimulation. Using light-sheet microscopy and pH-sensitive sensor pHluorin to follow TRPV1 endocytosis and exocytosis trafficking, we provide real-time information that tachyphylaxis of different degrees concurs with TRPV1 recycling to the plasma membrane in a proportional manner. This process controls TRPV1 surface expression level thereby the whole-cell nociceptive response. We further show that activity-gated TRPV1 trafficking associates with intracellular Ca2+ signals of distinct kinetics, and recruits recycling routes mediated by synaptotagmin 1 and 7, respectively. These results suggest that activity-dependent TRPV1 recycling contributes to the establishment of tachyphylaxis.</description><subject>Animals</subject><subject>Biological Sciences</subject><subject>Calcium (intracellular)</subject><subject>Calcium ions</subject><subject>Calcium Signaling</subject><subject>Calcium signalling</subject><subject>Capsaicin receptors</subject><subject>Cell Membrane - metabolism</subject><subject>Channel gating</subject><subject>Desensitization</subject><subject>Endocytosis</subject><subject>Exocytosis</subject><subject>HEK293 Cells</subject><subject>Humans</subject><subject>Ion channels</subject><subject>Kinetics</subject><subject>Life Sciences</subject><subject>Light</subject><subject>Organic chemistry</subject><subject>Pain</subject><subject>Pain perception</subject><subject>pH effects</subject><subject>Process control</subject><subject>Process controls</subject><subject>Protein Transport</subject><subject>Protein turnover</subject><subject>Rats</subject><subject>Stimulation</subject><subject>Synaptotagmin</subject><subject>Synaptotagmins - metabolism</subject><subject>Tachyphylaxis</subject><subject>Transient receptor potential proteins</subject><subject>TRPV Cation Channels - metabolism</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkU1v1DAQhi0EokvhzAlkiQsc0s7YjhNfKlUVUKSVQFXL1Uq84yarJF7s7EL-PVltWaCnkWaeeefjZew1whlCIc83Q5XOsESjZY6on7AFgsFMKwNP2QJAFFmphDphL1JaA4DJS3jOTiSUoATggt3dkAs7ihP3MfR8rFwzbZqpq361iQfPb2--fUfuQju4dkWJ_2zHhkdyk-va4Z6PgY8N8bSNvnLEe-rrWA30kj3zVZfo1UM8ZXefPt5eXWfLr5-_XF0uM6eKYsxqWSoJTsicNHqtQWNugKQH7X0JxtUa65K8IxAeSBQmRyPmxWm1MkoqecouDrqbbd3TytEwxqqzm9j2VZxsqFr7f2VoG3sfdlYrgUrDLPDhINA8aru-XNp9DoTCogC1w5l9_zAshh9bSqPt2-So6-aDwzZZgaVGVaDeo-8eoeuwjcP8ipkyCoXORT5T5wfKxZBSJH_cAMHu7bV7e-1fe-eOt__ee-T_-DkDbw7AOo0hHutC60LMk-VvtvmpcQ</recordid><startdate>20190312</startdate><enddate>20190312</enddate><creator>Tian, Quan</creator><creator>Hu, Juan</creator><creator>Xie, Chang</creator><creator>Mei, Kaidi</creator><creator>Pham, Cuong</creator><creator>Mo, Xiaoyi</creator><creator>Hepp, Régine</creator><creator>Soares, Sylvia</creator><creator>Nothias, Fatiha</creator><creator>Wang, Yuanyuan</creator><creator>Liu, Qiang</creator><creator>Cai, Fen</creator><creator>Zhong, Bo</creator><creator>Li, Dongdong</creator><creator>Yao, Jing</creator><general>National Academy of Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-7683-7451</orcidid><orcidid>https://orcid.org/0000-0003-2459-6956</orcidid><orcidid>https://orcid.org/0000-0002-6731-4771</orcidid><orcidid>https://orcid.org/0000-0003-1301-9758</orcidid><orcidid>https://orcid.org/0000-0002-2497-2096</orcidid></search><sort><creationdate>20190312</creationdate><title>Recovery from tachyphylaxis of TRPV1 coincides with recycling to the surface membrane</title><author>Tian, Quan ; 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TRPV1 activation is accompanied by Ca2+-dependent desensitization; acute desensitization reflects rapid reduction in channel activity during stimulation, whereas tachyphylaxis denotes the diminution in TRPV1 responses to repetitive stimulation. Acute desensitization has been attributed to conformational changes of the TRPV1 channel; however, the mechanisms underlying the establishment of tachyphylaxis remain to be defined. Here, we report that the degree of whole-cell TRPV1 tachyphylaxis is regulated by the strength of inducing stimulation. Using light-sheet microscopy and pH-sensitive sensor pHluorin to follow TRPV1 endocytosis and exocytosis trafficking, we provide real-time information that tachyphylaxis of different degrees concurs with TRPV1 recycling to the plasma membrane in a proportional manner. This process controls TRPV1 surface expression level thereby the whole-cell nociceptive response. We further show that activity-gated TRPV1 trafficking associates with intracellular Ca2+ signals of distinct kinetics, and recruits recycling routes mediated by synaptotagmin 1 and 7, respectively. These results suggest that activity-dependent TRPV1 recycling contributes to the establishment of tachyphylaxis.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>30804201</pmid><doi>10.1073/pnas.1819635116</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0002-7683-7451</orcidid><orcidid>https://orcid.org/0000-0003-2459-6956</orcidid><orcidid>https://orcid.org/0000-0002-6731-4771</orcidid><orcidid>https://orcid.org/0000-0003-1301-9758</orcidid><orcidid>https://orcid.org/0000-0002-2497-2096</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Animals Biological Sciences Calcium (intracellular) Calcium ions Calcium Signaling Calcium signalling Capsaicin receptors Cell Membrane - metabolism Channel gating Desensitization Endocytosis Exocytosis HEK293 Cells Humans Ion channels Kinetics Life Sciences Light Organic chemistry Pain Pain perception pH effects Process control Process controls Protein Transport Protein turnover Rats Stimulation Synaptotagmin Synaptotagmins - metabolism Tachyphylaxis Transient receptor potential proteins TRPV Cation Channels - metabolism |
| title | Recovery from tachyphylaxis of TRPV1 coincides with recycling to the surface membrane |
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