{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,5,20]],"date-time":"2026-05-20T15:32:44Z","timestamp":1779291164680,"version":"3.51.4"},"reference-count":52,"publisher":"Frontiers Media SA","funder":[{"DOI":"10.13039\/501100006769","name":"Russian Science Foundation","doi-asserted-by":"publisher","award":["14-15-000618"],"award-info":[{"award-number":["14-15-000618"]}],"id":[{"id":"10.13039\/501100006769","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Neurosci."],"DOI":"10.3389\/fncel.2017.00226","type":"journal-article","created":{"date-parts":[[2017,7,27]],"date-time":"2017-07-27T03:45:40Z","timestamp":1501127140000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":30,"title":["Receptor Mechanisms Mediating the Pro-Nociceptive Action of Hydrogen Sulfide in Rat Trigeminal Neurons and Meningeal Afferents"],"prefix":"10.3389","volume":"11","author":[{"given":"Kseniya","family":"Koroleva","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alsu","family":"Mustafina","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Aleksey","family":"Yakovlev","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Anton","family":"Hermann","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Rashid","family":"Giniatullin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Guzel","family":"Sitdikova","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2017,7,27]]},"reference":[{"key":"B1","doi-asserted-by":"crossref","first-page":"1066","DOI":"10.1523\/JNEUROSCI.16-03-01066.1996","article-title":"The possible role of hydrogen sulfide as an endogenous neuromodulator","volume":"16","author":"Abe","year":"1996","journal-title":"J. Neurosci."},{"key":"B2","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1113\/jphysiol.2007.133231","article-title":"Transient receptor potential TRPA1 channel desensitization in sensory neurons is agonist dependent and regulated by TRPV1-directed internalization","volume":"583","author":"Akopian","year":"2007","journal-title":"J. Physiol."},{"key":"B3","doi-asserted-by":"publisher","first-page":"e46917","DOI":"10.1371\/journal.pone.0046917","article-title":"TRPA1 has a key role in the somatic pro-nociceptive actions of hydrogen sulfide","volume":"7","author":"Andersson","year":"2012","journal-title":"PLoS One"},{"key":"B4","doi-asserted-by":"publisher","first-page":"2485","DOI":"10.1523\/JNEUROSCI.5369-07.2008","article-title":"Transient receptor potential A1 is a sensory receptor for multiple products of oxidative stress","volume":"28","author":"Andersson","year":"2008","journal-title":"J. Neurosci."},{"key":"B5","doi-asserted-by":"publisher","first-page":"71","DOI":"10.1186\/1129-2377-14-71","article-title":"TRPA1 and other TRP channels in migraine","volume":"14","author":"Benemei","year":"2013","journal-title":"J. Headache Pain"},{"key":"B6","doi-asserted-by":"publisher","first-page":"L896","DOI":"10.1152\/ajplung.00053.2006","article-title":"Role of substance P in hydrogen sulfide-induced pulmonary inflammation in mice","volume":"291","author":"Bhatia","year":"2006","journal-title":"Am. J. Physiol. Lung Cell. Mol. Physiol."},{"key":"B7","doi-asserted-by":"publisher","first-page":"203","DOI":"10.1016\/j.ab.2011.10.016","article-title":"Passive loss of hydrogen sulfide in biological experiments","volume":"421","author":"Deleon","year":"2012","journal-title":"Anal. Biochem."},{"key":"B8","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1124\/jpet.105.091595","article-title":"Evidence that hydrogen sulfide exerts antinociceptive effects in the gastrointestinal tract by activating KATP channels","volume":"316","author":"Distrutti","year":"2006","journal-title":"J. Pharmacol. Exp. Ther."},{"key":"B9","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1186\/1744-8069-9-4","article-title":"Hydrogen sulfide increases excitability through suppression of sustained potassium channel currents of rat trigeminal ganglion neurons","volume":"9","author":"Feng","year":"2013","journal-title":"Mol. Pain"},{"key":"B11","doi-asserted-by":"publisher","first-page":"20283","DOI":"10.1074\/jbc.M312577200","article-title":"Molecular determinants of vanilloid sensitivity in TRPV1","volume":"279","author":"Gavva","year":"2004","journal-title":"J. Biol. Chem."},{"key":"B13","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1016\/j.neuroscience.2015.07.036","article-title":"Mechanisms of hydrogen sulfide (H2S) action on synaptic transmission at the mouse neuromuscular junction","volume":"303","author":"Gerasimova","year":"2015","journal-title":"Neuroscience"},{"key":"B12","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1007\/s10517-013-2067-7","article-title":"Role of ryanodine receptors in the effects of hydrogen sulfide on transmitter release from the frog motor nerve ending","volume":"155","author":"Gerasimova","year":"2013","journal-title":"Bull. Exp. Biol. Med."},{"key":"B14","doi-asserted-by":"publisher","first-page":"83","DOI":"10.1007\/s12035-008-8020-5","article-title":"Molecular mechanisms of sensitization of pain-transducing P2X3 receptors by the migraine mediators CGRP and NGF","volume":"37","author":"Giniatullin","year":"2008","journal-title":"Mol. Neurobiol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"1749","DOI":"10.1089\/ars.2012.5041","article-title":"Polysulfides link H2S to protein thiol oxidation","volume":"19","author":"Greiner","year":"2013","journal-title":"Antioxid. Redox Signal."},{"key":"B16","doi-asserted-by":"publisher","first-page":"157","DOI":"10.1007\/s12031-016-0802-z","article-title":"Capsaicin-sensitive sensory nerves mediate the cellular and microvascular effects of H2S via TRPA1 receptor activation and neuropeptide release","volume":"60","author":"Hajna","year":"2016","journal-title":"J. Mol. Neurosci."},{"key":"B17","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1186\/s12990-015-0023-4","article-title":"Polysulfide evokes acute pain through the activation of nociceptive TRPA1 in mouse sensory neurons","volume":"11","author":"Hatakeyama","year":"2015","journal-title":"Mol. Pain"},{"key":"B18","doi-asserted-by":"publisher","first-page":"66","DOI":"10.1186\/1744-8069-8-66","article-title":"Expression of the transient receptor potential channels TRPV1, TRPA1 and TRPM8 in mouse trigeminal primary afferent neurons innervating the dura","volume":"8","author":"Huang","year":"2012","journal-title":"Mol. Pain"},{"key":"B19","doi-asserted-by":"publisher","first-page":"421","DOI":"10.1016\/s0092-8674(02)00637-2","article-title":"Molecular basis for species-specific sensitivity to \u201chot\u201d chili peppers","volume":"108","author":"Jordt","year":"2002","journal-title":"Cell"},{"key":"B20","doi-asserted-by":"publisher","first-page":"74","DOI":"10.1016\/j.pain.2007.01.026","article-title":"Hydrogen sulfide as a novel nociceptive messenger","volume":"132","author":"Kawabata","year":"2007","journal-title":"Pain"},{"key":"B21","doi-asserted-by":"publisher","first-page":"160","DOI":"10.1016\/j.neuropharm.2016.12.024","article-title":"Serotonergic mechanisms of trigeminal meningeal nociception: implications for migraine pain","volume":"116","author":"Kilic","year":"2017","journal-title":"Neuropharmacology"},{"key":"B22","doi-asserted-by":"publisher","first-page":"1235","DOI":"10.1007\/s00702-016-1600-z","article-title":"Hydrogen polysulfide (H2Sn) signaling along with hydrogen sulfide (H2S) and nitric oxide (NO)","volume":"123","author":"Kimura","year":"2016","journal-title":"J. Neural Transm. (Vienna)"},{"key":"B23","doi-asserted-by":"publisher","first-page":"1534","DOI":"10.1111\/bph.12562","article-title":"H2S modulates duodenal motility in male rats via activating TRPV1 and KATP channels","volume":"171","author":"Lu","year":"2014","journal-title":"Br. J. Pharmacol."},{"key":"B24","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1038\/nature05544","article-title":"Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines","volume":"445","author":"Macpherson","year":"2007","journal-title":"Nature"},{"key":"B25","doi-asserted-by":"publisher","first-page":"272","DOI":"10.3389\/fphys.2017.00272","article-title":"TRPA1 channels modify TRPV1-mediated current responses in dorsal root ganglion neurons","volume":"8","author":"Masuoka","year":"2017","journal-title":"Front. Physiol."},{"key":"B26","doi-asserted-by":"publisher","first-page":"751","DOI":"10.1136\/gut.2007.144543","article-title":"Luminal hydrogen sulfide plays a pronociceptive role in mouse colon","volume":"58","author":"Matsunami","year":"2009","journal-title":"Gut"},{"key":"B27","doi-asserted-by":"publisher","first-page":"9","DOI":"10.1186\/1744-8069-10-9","article-title":"Upregulation of cystathionine-\u03b2-synthetase expression contributes to inflammatory pain in rat temporomandibular joint","volume":"10","author":"Miao","year":"2014","journal-title":"Mol. Pain"},{"key":"B28","doi-asserted-by":"publisher","first-page":"45995","DOI":"10.1038\/srep45995","article-title":"Polysulfides (H2Sn) produced from the interaction of hydrogen sulfide (H2S) and nitric oxide (NO) activate TRPA1 channels","volume":"7","author":"Miyamoto","year":"2017","journal-title":"Sci. Rep."},{"key":"B29","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1016\/j.neulet.2011.05.057","article-title":"Time- and concentration-dependent activation of TRPA1 by hydrogen sulfide in rat DRG neurons","volume":"499","author":"Miyamoto","year":"2011","journal-title":"Neurosci. Lett."},{"key":"B30","doi-asserted-by":"publisher","first-page":"825","DOI":"10.1016\/j.bbrc.2015.08.095","article-title":"Hydrogen sulfide induces hyperpolarization and decreases the exocytosis of secretory granules of rat GH3 pituitary tumor cells","volume":"465","author":"Mustafina","year":"2015","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B31","doi-asserted-by":"publisher","first-page":"335","DOI":"10.1016\/j.neuroscience.2012.05.044","article-title":"H2S functions as a nociceptive messenger through transient receptor potential ankyrin 1 (TRPA1) activation","volume":"218","author":"Ogawa","year":"2012","journal-title":"Neuroscience"},{"key":"B32","doi-asserted-by":"publisher","first-page":"1738","DOI":"10.1111\/j.1476-5381.2012.01886.x","article-title":"Hydrogen sulfide-induced mechanical hyperalgesia and allodynia require activation of both Cav3.2 and TRPA1 channels in mice","volume":"166","author":"Okubo","year":"2012","journal-title":"Br. J. Pharmacol."},{"key":"B33","doi-asserted-by":"publisher","first-page":"398","DOI":"10.2174\/1568026611313030014","article-title":"Endogenous modulators of TRP channels","volume":"13","author":"Palazzo","year":"2013","journal-title":"Curr. Top. Med. Chem."},{"key":"B34","doi-asserted-by":"publisher","first-page":"31","DOI":"10.1038\/sj.bjp.0705764","article-title":"Hydrogen sulfide (H2S) stimulates capsaicin-sensitive primary afferent neurons in the rat urinary bladder","volume":"142","author":"Patacchini","year":"2004","journal-title":"Br. J. Pharmacol."},{"key":"B35","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1007\/978-3-540-34891-7_9","article-title":"Capsaicin receptor: TRPV1 a promiscuous TRP channel","volume":"179","author":"Pingle","year":"2007","journal-title":"Handb. Exp. Pharmacol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1016\/j.ejphar.2012.05.053","article-title":"The role of transient receptor potential ankyrin 1 (TRPA1) receptor activation in hydrogen-sulphide-induced CGRP-release and vasodilation","volume":"689","author":"Pozsgai","year":"2012","journal-title":"Eur. J. Pharmacol."},{"key":"B37","doi-asserted-by":"publisher","first-page":"34","DOI":"10.1016\/j.pain.2012.07.031","article-title":"Promoter demethylation of cystathionine-\u03b2-synthetase gene contributes to inflammatory pain in rats","volume":"154","author":"Qi","year":"2013","journal-title":"Pain"},{"key":"B38","doi-asserted-by":"publisher","first-page":"G763","DOI":"10.1152\/ajpgi.00466.2012","article-title":"Neonatal colonic inflammation sensitizes voltage-gated Na+ channels via upregulation of cystathionine \u03b2-synthetase expression in rat primary sensory neurons","volume":"304","author":"Qu","year":"2013","journal-title":"Am. J. Physiol. Gastrointest. Liver Physiol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"85","DOI":"10.2174\/187152811794776286","article-title":"Hydrogen sulfide generation in mammals: the molecular biology of cystathionine-\u03b2- synthase (CBS) and cystathionine-\u03b3-lyase (CSE)","volume":"10","author":"Renga","year":"2011","journal-title":"Inflamm. Allergy Drug Targets"},{"key":"B40","doi-asserted-by":"publisher","first-page":"1542","DOI":"10.1053\/j.gastro.2006.08.035","article-title":"Hydrogen sulfide is a novel prosecretory neuromodulator in the guinea-pig and human colon","volume":"131","author":"Schicho","year":"2006","journal-title":"Gastroenterology"},{"key":"B41","doi-asserted-by":"publisher","first-page":"341","DOI":"10.1016\/j.neuroscience.2013.09.002","article-title":"Cortical spreading depression induces oxidative stress in the trigeminal nociceptive system","volume":"253","author":"Shatillo","year":"2013","journal-title":"Neuroscience"},{"key":"B42","doi-asserted-by":"publisher","first-page":"431","DOI":"10.3389\/fphys.2014.00431","article-title":"Phosphorylation of BK channels modulates the sensitivity to hydrogen sulfide (H2S)","volume":"5","author":"Sitdikova","year":"2014","journal-title":"Front. Physiol."},{"key":"B43","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1007\/s10517-011-1280-5","article-title":"Role of calcium and potassium channels in effects of hydrogen sulfide on frog myocardial contractility","volume":"151","author":"Sitdikova","year":"2011","journal-title":"Bull. Exp. Biol. Med."},{"key":"B44","doi-asserted-by":"publisher","first-page":"389","DOI":"10.1007\/s00424-009-0737-0","article-title":"Hydrogen sulfide increases calcium-activated potassium (BK) channel activity of rat pituitary tumor cells","volume":"459","author":"Sitdikova","year":"2010","journal-title":"Pflugers Arch."},{"key":"B45","doi-asserted-by":"publisher","first-page":"e0116900","DOI":"10.1371\/journal.pone.0116900","article-title":"Unveiling TRPV1 spatio-temporal organization in live cell membranes","volume":"10","author":"Storti","year":"2015","journal-title":"PLoS One"},{"key":"B46","doi-asserted-by":"publisher","first-page":"383","DOI":"10.1124\/mol.106.023069","article-title":"Reducing and oxidizing agents sensitize heat-activated vanilloid receptor (TRPV1) current","volume":"70","author":"Susankova","year":"2006","journal-title":"Mol. Pharmacol."},{"key":"B47","doi-asserted-by":"publisher","first-page":"1757","DOI":"10.1124\/mol.105.017467","article-title":"Direct stimulation of K(ATP) channels by exogenous and endogenous hydrogen sulfide in vascular smooth muscle cells","volume":"68","author":"Tang","year":"2005","journal-title":"Mol. Pharmacol."},{"key":"B48","doi-asserted-by":"publisher","first-page":"1123","DOI":"10.1038\/sj.bjp.0706277","article-title":"Hydrogen sulfide causes vanilloid receptor 1-mediated neurogenic inflammation in the airways","volume":"145","author":"Trevisani","year":"2005","journal-title":"Br. J. Pharmacol."},{"key":"B49","doi-asserted-by":"publisher","first-page":"44","DOI":"10.1186\/1744-8069-5-44","article-title":"The endogenous hydrogen sulfide producing enzyme cystathionine-\u03b2 synthase contributes to visceral hypersensitivity in a rat model of irritable bowel syndrome","volume":"5","author":"Xu","year":"2009","journal-title":"Mol. Pain"},{"key":"B50","doi-asserted-by":"publisher","first-page":"153","DOI":"10.1016\/j.neuroscience.2016.10.051","article-title":"Hydrogen sulfide inhibits giant depolarizing potentials and abolishes epileptiform activity of neonatal rat hippocampal slices","volume":"340","author":"Yakovlev","year":"2017","journal-title":"Neuroscience"},{"key":"B51","doi-asserted-by":"publisher","first-page":"287","DOI":"10.3389\/fncel.2015.00287","article-title":"Hunting for origins of migraine pain: cluster analysis of spontaneous and capsaicin-induced firing in meningeal trigeminal nerve fibers","volume":"9","author":"Zakharov","year":"2015","journal-title":"Front. Cell. Neurosci."},{"key":"B52","doi-asserted-by":"publisher","first-page":"9028","DOI":"10.1523\/JNEUROSCI.1068-13.2013","article-title":"Promoted interaction of nuclear factor-\u03baB with demethylated cystathionine-\u03b2-synthetase gene contributes to gastric hypersensitivity in diabetic rats","volume":"33","author":"Zhang","year":"2013","journal-title":"J. Neurosci."},{"key":"B53","doi-asserted-by":"publisher","first-page":"16109","DOI":"10.1038\/srep16109","article-title":"Adrenergic stimulation sensitizes TRPV1 through upregulation of cystathionine \u03b2-synthetase in a rat model of visceral hypersensitivity","volume":"5","author":"Zhu","year":"2015","journal-title":"Sci. Rep."}],"container-title":["Frontiers in Cellular Neuroscience"],"original-title":[],"link":[{"URL":"http:\/\/journal.frontiersin.org\/article\/10.3389\/fncel.2017.00226\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2019,10,1]],"date-time":"2019-10-01T17:25:55Z","timestamp":1569950755000},"score":1,"resource":{"primary":{"URL":"http:\/\/journal.frontiersin.org\/article\/10.3389\/fncel.2017.00226\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,7,27]]},"references-count":52,"alternative-id":["10.3389\/fncel.2017.00226"],"URL":"https:\/\/doi.org\/10.3389\/fncel.2017.00226","relation":{},"ISSN":["1662-5102"],"issn-type":[{"value":"1662-5102","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,7,27]]},"article-number":"226"}}