Information de reference pour ce titreAccession Number: | 00006396-201607000-00018.
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Author: | Wang, Sen a; Joseph, John a; Diatchenko, Luda b; Ro, Jin Y. a; Chung, Man-Kyo a,*
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Institution: | (a)The Department of Neural and Pain Sciences, School of Dentistry, Program in Neuroscience, University of Maryland, Baltimore, MD, USA (b)Alan Edwards Centre for Research on Pain, McGill University, Montreal, QC, Canada
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Title: | |
Source: | Pain. 157(7):1515-1524, July 2016.
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Abstract: | Transient receptor potential vanilloid 1 (TRPV1) is a polymodal receptor activated by capsaicin, heat, and acid, which plays critical roles in thermosensation and pain. In addition, TRPV1 also contributes to multiple pathophysiological states in respiratory, cardiovascular, metabolic, and renal systems. These contributions are further supported by evidence that variations in the human TRPV1 (hTRPV1) gene are associated with various physiological and pathological phenotypes. However, it is not well understood how the variations in hTRPV1 affect channel functions. In this study, we examined functional consequences of amino acid variations of hTRPV1 induced by 5 nonsynonymous single-nucleotide polymorphisms (SNPs) that most commonly exist in the human population. Using electrophysiological assays in HEK293 cells, we examined 9 parameters: activation, Ca2+ permeation, and desensitization after activation by capsaicin, acid, and heat. Our results demonstrated that the 5 SNPs differentially affected functional properties of hTRPV1 in an agonist-dependent manner. Based upon the directionality of change of each phenotype and cumulative changes in each SNP, we classified the 5 SNPs into 3 presumptive functional categories: gain of function (hTRPV1 Q85R, P91S, and T469I), loss of function (I585V), and mixed (M315I). These results reveal a spectrum of functional variation among common hTRPV1 polymorphisms in humans and may aid mechanistic interpretation of phenotypes associated with nonsynonymous hTRPV1 SNPs under pathophysiological conditions.
(C) 2016 International Association for the Study of Pain
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Author Keywords: | Transient receptor potential vanilloid 1; Single-nucleotide polymorphisms; Patch clamp electrophysiology; Activation; Permeation; Desensitization; Capsaicin; Heat; Acid.
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References: | [1]. Altomare A, Guarino MP, Cicala M, Drewes AM, Krarup AL, Brock C, Lottrup C, Frokjaer JB, Souza RF, Nardone G, Compare D. Gastrointestinal sensitivity and gastroesophageal reflux disease. Ann N Y Acad Sci 2013;1300:80-95.
[2]. Binder A, May D, Baron R, Maier C, Tolle TR, Treede RD, Berthele A, Faltraco F, Flor H, Gierthmuhlen J, Haenisch S, Huge V, Magerl W, Maihofner C, Richter H, Rolke R, Scherens A, Uceyler N, Ufer M, Wasner G, Zhu J, Cascorbi I. Transient receptor potential channel polymorphisms are associated with the somatosensory function in neuropathic pain patients. PLoS One 2011;6:e17387.
[3]. Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, Watkins S, Caterina MJ. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 2002;5:856-60.
[4]. Cantero-Recasens G, Gonzalez JR, Fandos C, Duran-Tauleria E, Smit LA, Kauffmann F, Anto JM, Valverde MA. Loss of function of transient receptor potential vanilloid 1 (TRPV1) genetic variant is associated with lower risk of active childhood asthma. J Biol Chem 2010;285:27532-5.
[5]. Carreno O, Corominas R, Fernandez-Morales J, Camina M, Sobrido MJ, Fernandez-Fernandez JM, Pozo-Rosich P, Cormand B, Macaya A. SNP variants within the vanilloid TRPV1 and TRPV3 receptor genes are associated with migraine in the Spanish population. Am J Med Genet B Neuropsychiatr Genet 2012;159B:94-103.
[6]. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997;389:816-24.
[7]. Cavanaugh DJ, Chesler AT, Jackson AC, Sigal YM, Yamanaka H, Grant R, O'Donnell D, Nicoll RA, Shah NM, Julius D, Basbaum AI. Trpv1 reporter mice reveal highly restricted brain distribution and functional expression in arteriolar smooth muscle cells. J Neurosci 2011;31:5067-77.
[8]. Chung MK, Guler AD, Caterina MJ. TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat Neurosci 2008;11:555-64.
[9]. Chung MK, Jung SJ, Oh SB. Role of TRP channels in pain sensation. Adv Exp Med Biol 2011;704:615-36.
[10]. Chung MK, Wang S. Cold suppresses agonist-induced activation of TRPV1. J Dent Res 2011;90:1098-102.
[11]. Clapham DE, Miller C. A thermodynamic framework for understanding temperature sensing by transient receptor potential (TRP) channels. Proc Natl Acad Sci U S A 2011;108:19492-7.
[12]. Dias AG, Rousseau D, Duizer L, Cockburn M, Chiu W, Nielsen D, El-Sohemy A. Genetic variation in putative salt taste receptors and salt taste perception in humans. Chem Senses 2013;38:137-45.
[13]. Fehrenbacher JC, Sun XX, Locke EE, Henry MA, Hargreaves KM. Capsaicin-evoked iCGRP release from human dental pulp: a model system for the study of peripheral neuropeptide secretion in normal healthy tissue. Pain 2009;144:253-61.
[14]. Grace MS, Baxter M, Dubuis E, Birrell MA, Belvisi MG. Transient Receptor Potential (TRP) channels in the airway: role in airway disease. Br J Pharmacol 2013;171:2593-607.
[15]. Henrich F, Magerl W, Klein T, Greffrath W, Treede RD. Capsaicin-sensitive C- and A-fibre nociceptors control long-term potentiation-like pain amplification in humans. Brain 2015;138:2505-20.
[16]. Hollis M, Wang DH. Transient receptor potential vanilloid in blood pressure regulation. Curr Opin Nephrol Hypertens 2013;22:170-6.
[17]. Joseph J, Wang S, Lee J, Ro JY, Chung MK. Carboxyl-terminal domain of transient receptor potential vanilloid 1 contains distinct segments differentially involved in capsaicin- and heat-induced desensitization. J Biol Chem 2013;288:35690-702.
[18]. Kim H, Neubert JK, San Miguel A, Xu K, Krishnaraju RK, Iadarola MJ, Goldman D, Dionne RA. Genetic influence on variability in human acute experimental pain sensitivity associated with gender, ethnicity and psychological temperament. Pain 2004;109:488-96.
[19]. Kim MS, Usachev YM. Mitochondrial Ca2+ cycling facilitates activation of the transcription factor NFAT in sensory neurons. J Neurosci 2009;29:12101-14.
[20]. Liao M, Cao E, Julius D, Cheng Y. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 2013;504:107-12.
[21]. Lieu TM, Myers AC, Meeker S, Undem BJ. TRPV1 induction in airway vagal low-threshold mechanosensory neurons by allergen challenge and neurotrophic factors. Am J Physiol Lung Cell Mol Physiol 2012;302:L941-948.
[22]. Lishko PV, Procko E, Jin X, Phelps CB, Gaudet R. The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity. Neuron 2007;54:905-18.
[23]. Lukacs V, Yudin Y, Hammond GR, Sharma E, Fukami K, Rohacs T. Distinctive changes in plasma membrane phosphoinositides underlie differential regulation of TRPV1 in nociceptive neurons. J Neurosci 2013;33:11451-63.
[24]. Lyall V, Heck GL, Vinnikova AK, Ghosh S, Phan TH, Alam RI, Russell OF, Malik SA, Bigbee JW, DeSimone JA. The mammalian amiloride-insensitive non-specific salt taste receptor is a vanilloid receptor-1 variant. J Physiol 2004;558:147-59.
[25]. McGarvey LP, Butler CA, Stokesberry S, Polley L, McQuaid S, Abdullah H, Ashraf S, McGahon MK, Curtis TM, Arron J, Choy D, Warke TJ, Bradding P, Ennis M, Zholos A, Costello RW, Heaney LG. Increased expression of bronchial epithelial transient receptor potential vanilloid 1 channels in patients with severe asthma. J Allergy Clin Immunol 2014;133:704-12.
[26]. Mori F, Ribolsi M, Kusayanagi H, Monteleone F, Mantovani V, Buttari F, Marasco E, Bernardi G, Maccarrone M, Centonze D. TRPV1 channels regulate cortical excitability in humans. J Neurosci 2012;32:873-9.
[27]. Myers BR, Bohlen CJ, Julius D. A yeast genetic screen reveals a critical role for the pore helix domain in TRP channel gating. Neuron 2008;58:362-73.
[28]. Novakova-Tousova K, Vyklicky L, Susankova K, Benedikt J, Samad A, Teisinger J, Vlachova V. Functional changes in the vanilloid receptor subtype 1 channel during and after acute desensitization. Neuroscience 2007;149:144-54.
[29]. Razavi R, Chan Y, Afifiyan FN, Liu XJ, Wan X, Yantha J, Tsui H, Tang L, Tsai S, Santamaria P, Driver JP, Serreze D, Salter MW, Dosch HM. TRPV1+ sensory neurons control beta cell stress and islet inflammation in autoimmune diabetes. Cell 2006;127:1123-35.
[30]. Reilly RM, McDonald HA, Puttfarcken PS, Joshi SK, Lewis L, Pai M, Franklin PH, Segreti JA, Neelands TR, Han P, Chen J, Mantyh PW, Ghilardi JR, Turner TM, Voight EA, Daanen JF, Schmidt RG, Gomtsyan A, Kort ME, Faltynek CR, Kym PR. Pharmacology of modality-specific transient receptor potential vanilloid-1 antagonists that do not alter body temperature. J Pharmacol Exp Ther 2012;342:416-28.
[31]. Sadeh M, Glazer B, Landau Z, Wainstein J, Bezaleli T, Dabby R, Hanukoglu A, Boaz M, Leshinsky-Silver E. Association of the M315I variant in the Transient Receptor Potential Vanilloid Receptor-1 (TRPV1) gene with type 1 diabetes in an Ashkenazi Jewish population. Isr Med Assoc J 2013;15:545-8.
[32]. Schumacher MA, Eilers H. TRPV1 splice variants: structure and function. Front Biosci (Landmark Ed) 2010;15:872-82.
[33]. Smit LA, Kogevinas M, Anto JM, Bouzigon E, Gonzalez JR, Le Moual N, Kromhout H, Carsin AE, Pin I, Jarvis D, Vermeulen R, Janson C, Heinrich J, Gut I, Lathrop M, Valverde MA, Demenais F, Kauffmann F. Transient receptor potential genes, smoking, occupational exposures and cough in adults. Respir Res 2012;13:26.
[34]. Tahara T, Shibata T, Nakamura M, Yamashita H, Yoshioka D, Hirata I, Arisawa T. Homozygous TRPV1 315C influences the susceptibility to functional dyspepsia. J Clin Gastroenterol 2010;44:e1-7.
[35]. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009;25:1105-11.
[36]. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 2012;7:562-78.
[37]. Valdes AM, De Wilde G, Doherty SA, Lories RJ, Vaughn FL, Laslett LL, Maciewicz RA, Soni A, Hart DJ, Zhang W, Muir KR, Dennison EM, Wheeler M, Leaverton P, Cooper C, Spector TD, Cicuttini FM, Chapman V, Jones G, Arden NK, Doherty M. The Ile585Val TRPV1 variant is involved in risk of painful knee osteoarthritis. Ann Rheum Dis 2011;70:1556-61.
[38]. Vlachova V, Teisinger J, Susankova K, Lyfenko A, Ettrich R, Vyklicky L. Functional role of C-terminal cytoplasmic tail of rat vanilloid receptor 1. J Neurosci 2003;23:1340-50.
[39]. Wang S, Lee J, Ro JY, Chung MK. Warmth suppresses and desensitizes damage-sensing ion channel TRPA1. Mol Pain 2012;8:22.
[40]. Woudenberg-Vrenken TE, Bindels RJ, Hoenderop JG. The role of transient receptor potential channels in kidney disease. Nat Rev Nephrol 2009;5:441-9.
[41]. Xu H, Tian W, Fu Y, Oyama TT, Anderson S, Cohen DM. Functional effects of nonsynonymous polymorphisms in the human TRPV1 gene. Am J Physiol Ren Physiol 2007;293:F1865-1876.
[42]. Yao J, Liu B, Qin F. Kinetic and energetic analysis of thermally activated TRPV1 channels. Biophys J 2010;99:1743-53.
[43]. Zsombok A. Vanilloid receptors-do they have a role in whole body metabolism? Evidence from TRPV1. J Diabetes Complications 2013;27:287-92.
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Language: | English.
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Document Type: | Research Paper.
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Journal Subset: | Clinical Medicine.
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ISSN: | 0304-3959
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NLM Journal Code: | opf, 7508686
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DOI Number: | https://dx.doi.org/10.1097/j.pai...- ouverture dans une nouvelle fenêtre
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