Abstract
Ion channels allow for rapid ion diffusion through the plasma membrane. In some conditions, ion channels induce changes in the critical plasma membrane permeability that permit 900-Da solutes to enter cells. This process is known as the pore phenomenon. Some transient receptor potential (TRP) channel subtypes have been highlighted such as the P2X7 receptor, plasma membrane VDAC-1 channel, and pannexin hemichannels. The TRP ion channels are considered multimodal transducers that respond to several kinds of stimuli. In addition, many TRP channel subtypes are involved in physiological and pathophysiological processes such as inflammation, pain, and cancer. The TRPA1, TRPM8, and TRPV1-4 subtypes have been shown to promote large-molecular-weight solute uptake, including impermeable fluorescent dyes, QX-314 hydrophilic lidocaine derivative, gabapentin, and antineoplastic drugs. This review discusses the current knowledge of TRP-associated pores and encourages scientists to study their features and explore them as novel therapeutic tools.
Similar content being viewed by others
References
Ahluwalia J, Rang H, Nagy I (2002) The putative role of vanilloid receptor-like protein-1 in mediating high threshold noxious heat-sensitivity in rat cultured primary sensory neurons. Eur J Neurosci 16:1483–1489. doi:10.1046/j.1460-9568.2002.02231.x
Alberto AV, Faria RX, Couto CGC et al (2013) Is pannexin the pore associated with the P2X7 receptor? Naunyn Schmiedebergs Arch Pharmacol 386:775–787. doi:10.1007/s00210-013-0868-x
Alessandri-Haber N, Dina OA, Chen X, Levine JD (2009) TRPC1 and TRPC6 channels cooperate with TRPV4 to mediate mechanical hyperalgesia and nociceptor sensitization. J Neurosci 29:6217–6228. doi:10.1523/JNEUROSCI.0893-09.2009
Alves LA, De Melo Reis RA, De Souza CAM et al (2014) The P2X7 receptor: shifting from a low- to a high-conductance channel—an enigmatic phenomenon? Biochim Biophys Acta Biomembr 1838:2578–2587. doi:10.1016/j.bbamem.2014.05.015
Amantini C, Mosca M, Lucciarini R et al (2004) Distinct thymocyte subsets express the vanilloid receptor VR1 that mediates capsaicin-induced apoptotic cell death. Cell Death Differ 11:1342–1356. doi:10.1038/sj.cdd.4401506
Andersson DA, Chase HWN, Bevan S (2004) TRPM8 activation by menthol, icilin, and cold is differentially modulated by intracellular pH. J Neurosci 24:5364–5369. doi:10.1523/JNEUROSCI.0890-04.2004
Andreev YA, Vassilevski AA, Kozlov SA (2012) Molecules to selectively target receptors for treatment of pain and neurogenic inflammation. Recent Patents Inflamm Allergy Drug Discov 6:35–45. doi:10.2174/187221312798889266
Aoyagi K, Ohara-Imaizumi M, Nishiwaki C et al (2010) Insulin/phosphoinositide 3-kinase pathway accelerates the glucose-induced first-phase insulin secretion through TrpV2 recruitment in pancreatic β-cells. Biochem J 432:375–386. doi:10.1042/BJ20100864
Arniges M, Vázquez E, Fernández-Fernández JM, Valverde MA (2004) Swelling-activated Ca2+ entry via TRPV4 channel is defective in cystic fibrosis airway epithelia. J Biol Chem 279:54062–54068. doi:10.1074/jbc.M409708200
Bandell M, Story GM, Hwang SW et al (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849–857. doi:10.1016/S0896-6273(04)00150-3
Bang S, Kim KY, Yoo S et al (2007) Transient receptor potential V2 expressed in sensory neurons is activated by probenecid. Neurosci Lett 425:120–125. doi:10.1016/j.neulet.2007.08.035
Banke T (2011) The dilated TRPA1 channel pore state is blocked by amiloride and analogues. Brain Res 1381:21–30. doi:10.1016/j.brainres.2011.01.021
Banke TG, Chaplan SR, Wickenden AD (2010) Dynamic changes in the TRPA1 selectivity filter lead to progressive but reversible pore dilation. Am J Physiol Cell Physiol 298:C1457–C1468. doi:10.1152/ajpcell.00489.2009
Bao L, Locovei S, Dahl G (2004) Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett 572:65–68. doi:10.1016/j.febslet.2004.07.009
Bautista D, Julius D (2008) Fire in the hole: pore dilation of the capsaicin receptor TRPV1. Nat Neurosci 11:528–529. doi:10.1038/nn0508-528
Bautista DM, Siemens J, Glazer JM et al (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204–208. doi:10.1038/nature05910
Behrendt H-J, Germann T, Gillen C et al (2004) Characterization of the mouse cold-menthol receptor TRPM8 and vanilloid receptor type-1 VR1 using a fluorometric imaging plate reader (FLIPR) assay. Br J Pharmacol 141:737–745. doi:10.1038/sj.bjp.0705652
Bellono NW, Kammel LG, Zimmerman AL, Oancea E (2013) UV light phototransduction activates transient receptor potential A1 ion channels in human melanocytes. Proc Natl Acad Sci U S A 110:2383–2388. doi:10.1073/pnas.1215555110
Berg KA, Patwardhan AM, Akopian AN (2012) Receptor and channel heteromers as pain targets. Pharmaceuticals 5:249–278. doi:10.3390/ph5030249
Beyer K, Nickel R, Freidhoff L et al (2000) Association and linkage of atopic dermatitis with chromosome 13q12-14 and 5q31-33 markers. J Investig Dermatol 115:906–908. doi:10.1046/j.1523-1747.2000.00096.x
Biggs JE, Stemkowski PL, Knaus EE, et al (2014) Suppression of network activity in dorsal horn by gabapentin permeation of TRPV1 channels: implications for drug access to cytoplasmic targets. Neurosci Lett
Blanton SH, Liang CY, Cai MW et al (2002) A novel locus for autosomal dominant non-syndromic deafness (DFNA41) maps to chromosome 12q24-qter. J Med Genet 39:567–570. doi:10.1136/jmg.39.8.567
Brauchi S, Orio P, Latorre R (2004) Clues to understanding cold sensation: thermodynamics and electrophysiological analysis of the cold receptor TRPM8. Proc Natl Acad Sci U S A 101:15494–15499. doi:10.1073/pnas.0406773101
Cankurtaran-sayar S, Sayar K, Ugur M (2009) P2X7 receptor activates multiple selective dye-permeation pathways in RAW 264.7 and human embryonic kidney 293 cells. Mol Pharmacol 76:1323–1332. doi:10.1124/mol.109.059923
Cao D-S, Zhong L, Hsieh T et al (2012) Expression of Transient Receptor Potential Ankyrin 1 (TRPA1) and its role in insulin release from rat pancreatic beta cells. PLoS One 7, e38005. doi:10.1371/journal.pone.0038005
Caterina MJ, Schumacher MA, Tominaga M et al (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824. doi:10.1038/39807
Caterina MJ, Rosen TA, Tominaga M et al (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436–441. doi:10.1038/18906
Chen J, Kim D, Bianchi BR et al (2009) Pore dilation occurs in TRPA1 but not in TRPM8 channels. Mol Pain 5:3. doi:10.1186/1744-8069-5-3
Chen C-L, Li H, Xing X-H et al (2015) Effect of TRPV1 gene mutation on bronchial asthma in children before and after treatment. Allergy Asthma Proc 36:29–36. doi:10.2500/aap.2015.36.3828
Cheng W, Sun C, Zheng J (2010) Heteromerization of TRP channel subunits: extending functional diversity. Protein Cell 1:802–810
Chou MZ, Mtui T, Gao YD et al (2004) Resiniferatoxin binds to the capsaicin receptor (TRPV1) near the extracellular side of the S4 transmembrane domain. Biochemistry 43:2501–2511. doi:10.1021/bi035981h
Chung M-K, Lee H, Mizuno A et al (2004) 2-aminoethoxydiphenyl borate activates and sensitizes the heat-gated ion channel TRPV3. J Neurosci 24:5177–5182. doi:10.1523/JNEUROSCI.0934-04.2004
Chung MK, Güler AD, Caterina MJ (2005) Biphasic currents evoked by chemical or thermal activation of the heat-gated ion channel, TRPV3. J Biol Chem 280:15928–15941. doi:10.1074/jbc.M500596200
Chung M-K, Güler AD, Caterina MJ (2008) TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat Neurosci 11:555–564. doi:10.1038/nn.2102
Chung G, Im ST, Kim YH et al (2014) Activation of transient receptor potential ankyrin 1 by eugenol. Neuroscience 261:153–160. doi:10.1016/j.neuroscience.2013.12.047
Clapham DE (2003) TRP channels as cellular sensors. Nature 426:517–524. doi:10.1038/nature02196
Compan V, Baroja-Mazo A, López-Castejón G et al (2012) Cell volume regulation modulates NLRP3 inflammasome activation. Immunity 37:487–500. doi:10.1016/j.immuni.2012.06.013
Correll CC, Phelps PT, Anthes JC et al (2004) Cloning and pharmacological characterization of mouse TRPV1. Neurosci Lett 370:55–60. doi:10.1016/j.neulet.2004.07.058
Cosens DJ, Manning A (1969) Abnormal electroretinogram from a Drosophila mutant. Nature 224:285–287. doi:10.1038/224285a0
Cross JL, Meloni BP, Bakker AJ et al (2010) Modes of neuronal calcium entry and homeostasis following cerebral ischemia. Stroke Res Treat 2010:316862. doi:10.4061/2010/316862
Dahlquist R, Diamant B, Krüger PG (1974) Increased permeability of the rat mast cell membrane to sodium and potassium caused by extracellular ATP and its relationship to histamine release. Int Arch Allergy Appl Immunol 46:655–675. doi:10.1159/000231167
De Schepper HU, De Man JG, Ruyssers NE et al (2008) TRPV1 receptor signaling mediates afferent nerve sensitization during colitis-induced motility disorders in rats. Am J Physiol Gastrointest Liver Physiol 294:G245–G253. doi:10.1152/ajpgi.00351.2007
Dhaka A, Murray AN, Mathur J et al (2007) TRPM8 is required for cold sensation in mice. Neuron 54:371–378. doi:10.1016/j.neuron.2007.02.024
Doly S, Fischer J, Salio C, Conrath M (2004) The vanilloid receptor-1 is expressed in rat spinal dorsal horn astrocytes. Neurosci Lett 357:123–126. doi:10.1016/j.neulet.2003.12.051
Drew LJ, Wood JN (2007) FM1-43 is a permeant blocker of mechanosensitive ion channels in sensory neurons and inhibits behavioural responses to mechanical stimuli. Mol Pain 3:1. doi:10.1186/1744-8069-3-1
Duchatelet S, Pruvost S, de Veer S et al (2014) A new TRPV3 missense mutation in a patient with Olmsted syndrome and erythromelalgia. JAMA Dermatol 150:303–306. doi:10.1001/jamadermatol.2013.8709
Dutta AK, Sabirov RZ, Uramoto H, Okada Y (2004) Role of ATP-conductive anion channel in ATP release from neonatal rat cardiomyocytes in ischaemic or hypoxic conditions. J Physiol 559:799–812. doi:10.1113/jphysiol.2004.069245
Eijkelkamp N, Quick K, Wood JN (2013) Transient receptor potential channels and mechanosensation. Annu Rev Neurosci 36:519–546. doi:10.1146/annurev-neuro-062012-170412
El Karim IA, Linden GJ, Curtis TM et al (2011a) Human odontoblasts express functional thermo-sensitive TRP channels: implications for dentin sensitivity. Pain 152:2211–2223. doi:10.1016/j.pain.2010.10.016
El Karim IA, Linden GJ, Curtis TM et al (2011b) Human dental pulp fibroblasts express the “cold-sensing” transient receptor potential channels TRPA1 and TRPM8. J Endod 37:473–478. doi:10.1016/j.joen.2010.12.017
Faria RX, Defarias FP, Alves LA (2005) Are second messengers crucial for opening the pore associated with P2X7 receptor? Am J Physiol Cell Physiol 288:C260–C271. doi:10.1152/ajpcell.00215.2004
Faria RX, Reis RAM, Casabulho CM et al (2009) Pharmacological properties of a pore induced by raising intracellular Ca2+. Am J Physiol Cell Physiol 297:C28–C42. doi:10.1152/ajpcell.00476.2008
Faria RX, Cascabulho CM, Reis RAM, Alves LA (2010a) Large-conductance channel formation mediated by P2X7 receptor activation is regulated through distinct intracellular signaling pathways in peritoneal macrophages and 2BH4 cells. Naunyn Schmiedebergs Arch Pharmacol 382:73–87. doi:10.1007/s00210-010-0523-8
Faria RX, Ferreira LG, Alves L (2010b) The mystery of P2X7 ionotropic receptor: from a small conductance channel to a large conductance channel. cdn.intechopen.com
Fernandes ES, Fernandes MA, Keeble JE (2012) The functions of TRPA1 and TRPV1: moving away from sensory nerves. Br J Pharmacol 166:510–521. doi:10.1111/j.1476-5381.2012.01851.x
Ferreira LG, Reis RA, Alves L, Faria RX (2012) Intracellular signaling pathways integrating the pore associated with P2X7R receptor with other large pores. In: PFSK (ed) Patch clamp technique. InTech
Ferreira LG, Pereira L, Faria R (2015) Fluorescent dyes as a reliable tool in P2X7 receptor-associated pore studies. J Bioenerg Biomembr. doi:10.1007/s10863-015-9613-0
Ferrer-Montiel A, Fernández-Carvajal A, Planells-Cases R et al (2012) Advances in modulating thermosensory TRP channels. Expert Opin Ther Pat 22:999–1017. doi:10.1517/13543776.2012.711320
Ficai A, Marques C, Ferreira JMF, et al (2014) Multifunctional materials for bone cancer treatment. Int J Nanomedicine 2713. doi:10.2147/IJN.S55943
Frank JA, Moroni M, Moshourab R et al (2015) Photoswitchable fatty acids enable optical control of TRPV1. Nat Commun 6:7118. doi:10.1038/ncomms8118
Garami A, Shimansky YP, Pakai E et al (2010) Contributions of different modes of TRPV1 activation to TRPV1 antagonist-induced hyperthermia. J Neurosci 30:1435–1440. doi:10.1523/JNEUROSCI.5150-09.2010
Gaudet R (2008) A primer on ankyrin repeat function in TRP channels and beyond. Mol Biosyst 4:372–379. doi:10.1039/b801481g
Gavva NR, Bannon AW, Hovland DN et al (2007a) Repeated administration of vanilloid receptor TRPV1 antagonists attenuates hyperthermia elicited by TRPV1 blockade. J Pharmacol Exp Ther 323:128–137. doi:10.1124/jpet.107.125674
Gavva NR, Bannon AW, Surapaneni S et al (2007b) The vanilloid receptor TRPV1 is tonically activated in vivo and involved in body temperature regulation. J Neurosci 27:3366–3374. doi:10.1523/JNEUROSCI.4833-06.2007
Gavva NR, Treanor JJS, Garami A et al (2008) Pharmacological blockade of the vanilloid receptor TRPV1 elicits marked hyperthermia in humans. Pain 136:202–210. doi:10.1016/j.pain.2008.01.024
Gradilone SA, Masyuk AI, Splinter PL et al (2007) Cholangiocyte cilia express TRPV4 and detect changes in luminal tonicity inducing bicarbonate secretion. Proc Natl Acad Sci U S A 104:19138–19143. doi:10.1073/pnas.0705964104
Güler AD, Lee H, Iida T et al (2002) Heat-evoked activation of the ion channel, TRPV4. J Neurosci 22:6408–6414
Guo A, Vulchanova L, Wang J et al (1999) Immunocytochemical localization of the vanilloid receptor 1 (VR1), relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 11:946–958. doi:10.1046/j.1460-9568.1999.00503.x
Guo A, Simone DA, Stone LS et al (2001) Developmental shift of vanilloid receptor 1 (VR1) terminals into deeper regions of the superficial dorsal horn: correlation with a shift from TrkA to Ret expression by dorsal root ganglion neurons. Eur J Neurosci 14:293–304. doi:10.1046/j.0953-816X.2001.01665.x
Hata T, Tazawa S, Ohta S et al (2012) Artepillin C, a major ingredient of Brazilian propolis, induces a pungent taste by activating TRPA1 channels. PLoS One 7, e48072. doi:10.1371/journal.pone.0048072
Hayes P, Meadows HJ, Gunthorpe MJ et al (2000) Cloning and functional expression of a human orthologue of rat vanilloid receptor-1. Pain 88:205–215. doi:10.1016/S0304-3959(00)00353-5
Hellwig N, Albrecht N, Harteneck C et al (2005) Homo- and heteromeric assembly of TRPV channel subunits. J Cell Sci 118:917–928. doi:10.1242/jcs.01675
Hille B (1975) Ionic selectivity of Na and K channels of nerve membranes. Membranes (Basel) 3:255–323
Horvath G, Kekesi G, Nagy E, Benedek G (2008) The role of TRPV1 receptors in the antinociceptive effect of anandamide at spinal level. Pain 134:277–284. doi:10.1016/j.pain.2007.04.032
Hu HZ, Gu Q, Wang C et al (2004) 2-Aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J Biol Chem 279:35741–35748. doi:10.1074/jbc.M404164200
Ichikawa H, Sugimoto T (2003) The co-expression of VR1 and VRL-1 in the rat vagal sensory ganglia. Brain Res 980:293–296. doi:10.1016/S0006-8993(03)02998-6
Islam MR, Uramoto H, Okada T et al (2012) Maxi-anion channel and pannexin 1 hemichannel constitute separate pathways for swelling-induced ATP release in murine L929 fibrosarcoma cells. AJP Cell Physiol 303:C924–C935. doi:10.1152/ajpcell.00459.2011
Jansson ET, Boström CL, Ahemaiti A et al (2012) Effect of cholesterol on the pore dilation of TRPV1. Biophys J 102:342a. doi:10.1016/j.bpj.2011.11.1873
Jansson ET, Trkulja CL, Ahemaiti A et al (2013) Effect of cholesterol depletion on the pore dilation of TRPV1. Mol Pain 9:1. doi:10.1186/1744-8069-9-1
Jaquemar D, Schenker T, Trueb B (1999) An ankyrin-like protein with transmembrane domains is specifically lost after oncogenic transformation of human fibroblasts * lacking in SV40 transformed cells as well as in many. Biochemistry 274:7325–7333. doi:10.1074/jbc.274.11.7325
Jordt S-E, Bautista DM, Chuang H-H et al (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260–265. doi:10.1038/nature02282
Juvin V, Penna A, Chemin J et al (2007) Pharmacological characterization and molecular determinants of the activation of transient receptor potential V2 channel orthologs by 2-aminoethoxydiphenyl borate. Mol Pharmacol 72:1258–1268. doi:10.1124/mol.107.037044
Kang J, Kang N, Lovatt D et al (2008) Connexin 43 hemichannels are permeable to ATP. J Neurosci 28:4702–4711. doi:10.1523/JNEUROSCI.5048-07.2008
Kanzaki M, Zhang YQ, Mashima H et al (1999) Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nat Cell Biol 1:165–170. doi:10.1038/11086
Karasawa T, Wang Q, Fu Y et al (2008) TRPV4 enhances the cellular uptake of aminoglycoside antibiotics. J Cell Sci 121:2871–2879. doi:10.1242/jcs.023705
Karashima Y, Prenen J, Talavera K et al (2010) Agonist-induced changes in Ca(2+) permeation through the nociceptor cation channel TRPA1. Biophys J 98:773–783. doi:10.1016/j.bpj.2009.11.007
Kimball C, Luo J, Yin S et al (2015) The pore loop domain of TRPV1 is required for its activation by the volatile anesthetics chloroform and isoflurane. Mol Pharmacol. doi:10.1124/mol.115.098277
Kissin I, Szallasi A (2011) Therapeutic targeting of TRPV1 by resiniferatoxin, from preclinical studies to clinical trials. Curr Top Med Chem 11:2159–2170. doi:10.2174/156802611796904924
Koch SE, Gao X, Haar L et al (2012) Probenecid: novel use as a non-injurious positive inotrope acting via cardiac TRPV2 stimulation. J Mol Cell Cardiol 53:134–144. doi:10.1016/j.yjmcc.2012.04.011
Kress M, Zeilhofer HU (1999) Capsaicin, protons and heat: new excitement about nociceptors. Trends Pharmacol Sci 20:112–118
Kwon S-G, Roh D-H, Yoon S-Y et al (2014) Acid evoked thermal hyperalgesia involves peripheral P2Y1 receptor mediated TRPV1 phosphorylation in a rodent model of thrombus induced ischemic pain. Mol Pain 10:2. doi:10.1186/1744-8069-10-2
Laing RJ, Dhaka A (2015) ThermoTRPs and pain. Neuroscience. doi:10.1177/1073858414567884
Landouré G, Zdebik AA, Martinez TL et al (2010) Mutations in TRPV4 cause Charcot-Marie-Tooth disease type 2C. Nat Genet 42:170–174. doi:10.1038/ng.512
Läuger P (1973) Ion transport through pores: a rate-theory analysis. Biochim Biophys Acta 311:423–441. doi:10.1016/0005-2736(73)90323-4
Lee J-H, Park C, Kim S-J et al (2013) Different uptake of gentamicin through TRPV1 and TRPV4 channels determines cochlear hair cell vulnerability. Exp Mol Med 45, e12. doi:10.1038/emm.2013.25
Lieben L, Carmeliet G (2012) The involvement of TRP channels in bone homeostasis. Front Endocrinol (Lausanne) 3
Liedtke W, Choe Y, Martí-Renom MA et al (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103:525–535. doi:10.1016/S0092-8674(00)00143-4
Lin Z, Chen Q, Lee M et al (2012) Exome sequencing reveals mutations in TRPV3 as a cause of Olmsted syndrome. Am J Hum Genet 90:558–564. doi:10.1016/j.ajhg.2012.02.006
Link TM, Park U, Vonakis BM et al (2010) TRPV2 has a pivotal role in macrophage particle binding and phagocytosis. Nat Immunol 11:232–239. doi:10.1038/ni.1842
Liu HT, Tashmukhamedov BA, Inoue H et al (2006) Roles of two types of anion channels in glutamate release from mouse astrocytes under ischemic or osmotic stress. Glia 54:343–357. doi:10.1002/glia.20400
Liu H, Zhang H-X, Hou H-Y et al (2011) Acid solution is a suitable medium for introducing QX-314 into nociceptors through TRPV1 channels to produce sensory-specific analgesic effects. PLoS One 6, e29395. doi:10.1371/journal.pone.0029395
Ma Z, Siebert AP, Cheung K-HK-H et al (2012) PNAS plus: calcium homeostasis modulator 1 (CALHM1) is the pore-forming subunit of an ion channel that mediates extracellular Ca2+ regulation of neuronal excitability. Proc Natl Acad Sci 109:E1963–E1971. doi:10.1073/pnas.1204023109
Mandadi S, Roufogalis BD (2008) ThermoTRP channels in nociceptors: taking a lead from capsaicin receptor TRPV1. Curr Neuropharmacol 6:21–38. doi:10.2174/157015908783769680
McKemy DD, Neuhausser WM, Julius D (2002) Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:52–58. doi:10.1038/nature719
McLeod RL, Correll CC, Jia Y, Anthes JC (2008) TRPV1 antagonists as potential antitussive agents. Lung
Meyers JR, MacDonald RB, Duggan A et al (2003) Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J Neurosci 23:4054–4065
Mienville JM, Clay JR (1997) Ion conductance of the Ca(2+)-activated maxi-K+ channel from the embryonic rat brain. Biophys J 72:188–192. doi:10.1016/S0006-3495(97)78657-0
Minke B (2010) The history of the Drosophila TRP channel: the birth of a new channel superfamily. J Neurogenet 24:216–233. doi:10.3109/01677063.2010.514369
Misak A, Grman M, Malekova L et al (2013) Mitochondrial chloride channels: electrophysiological characterization and pH induction of channel pore dilation. Eur Biophys J 42:709–720. doi:10.1007/s00249-013-0920-2
Montell C (2001) Physiology, phylogeny, and functions of the TRP superfamily of cation channels. Sci STKE 2001:re1. doi:10.1126/stke.2001.90.re1
Morelli MB, Offidani M, Alesiani F et al (2014) The effects of cannabidiol and its synergism with bortezomib in multiple myeloma cell lines. A role for transient receptor potential vanilloid type-2. Int J Cancer 134:2534–2546. doi:10.1002/ijc.28591
Mukhopadhyay I, Gomes P, Aranake S et al (2011) Expression of functional TRPA1 receptor on human lung fibroblast and epithelial cells. J Recept Signal Transduct 31:350–358. doi:10.3109/10799893.2011.602413
Munns CH, Chung M-K, Sanchez YE, et al (2015) Role of the outer pore domain in transient receptor potential vanilloid 1 dynamic permeability to large cations. J Biol Chem 290. doi:10.1074/jbc.M114.597435
Myrdal SE, Steyger PS (2005) TRPV1 regulators mediate gentamicin penetration of cultured kidney cells. Hear Res 204:170–182. doi:10.1016/j.heares.2005.02.005
Nabissi M, Morelli MB, Santoni M, Santoni G (2013) Triggering of the TRPV2 channel by cannabidiol sensitizes glioblastoma cells to cytotoxic chemotherapeutic agents. Carcinogenesis 34:48–57. doi:10.1093/carcin/bgs328
Nagasawa M, Kojima I (2015) Translocation of TRPV2 channel induced by focal administration of mechanical stress. Physiol Rep 3:e12296. doi:10.14814/phy2.12296
Nagata K, Duggan A, Kumar G, García-Añoveros J (2005) Nociceptor and hair cell transducer properties of TRPA1, a channel for pain and hearing. J Neurosci 25:4052–4061. doi:10.1523/JNEUROSCI.0013-05.2005
Nakagawa H, Hiura A (2013) Comparison of the transport of QX-314 through TRPA1, TRPM8, and TRPV1 channels. J Pain Res 6:223–230. doi:10.2147/JPR.S41614
Nealen ML, Gold MS, Thut PD, Caterina MJ (2003) TRPM8 mRNA is expressed in a subset of cold-responsive trigeminal neurons from rat. J Neurophysiol 90:515–520. doi:10.1152/jn.00843.2002
Neeper MP, Liu Y, Hutchinson TL et al (2007) Activation properties of heterologously expressed mammalian TRPV2: evidence for species dependence. J Biol Chem 282:15894–15902. doi:10.1074/jbc.M608287200
Nilius B, Appendino G, Owsianik G (2012) The transient receptor potential channel TRPA1: from gene to pathophysiology. Pflugers Arch Eur J Physiol 464:425–458. doi:10.1007/s00424-012-1158-z
Nishida M, Hara Y, Yoshida T et al (2006) TRP channels: molecular diversity and physiological function. Microcirculation 13:535–550. doi:10.1080/10739680600885111
North RA (2002) Molecular physiology of P2X receptors. Physiol Rev 82:1013–1067. doi:10.1152/physrev.00015.2002
Nuttle LC, El-Moatassim C, Dubyak GR (1993) Expression of the pore-forming P2Z purinoreceptor in Xenopus oocytes injected with poly(A)+RNA from murine macrophages. Mol Pharmacol 44:93–101
Oh M-H, Oh SY, Lu J et al (2013) TRPA1-dependent pruritus in IL-13-induced chronic atopic dermatitis. J Immunol 191:5371–5382. doi:10.4049/jimmunol.1300300
Othman AA, Nothaft W, Awni WM, Dutta S (2013) Effects of the TRPV1 antagonist ABT-102 on body temperature in healthy volunteers: pharmacokinetic/ pharmacodynamic analysis of three phase 1 trials. Br J Clin Pharmacol 75:1029–1040. doi:10.1111/j.1365-2125.2012.04405.x
Pabbidi RM, Yu S-Q, Peng S et al (2008) Influence of TRPV1 on diabetes-induced alterations in thermal pain sensitivity. Mol Pain 4:9. doi:10.1186/1744-8069-4-9
Patapoutian A, Macpherson L (2006) Channeling pain. Nat Med 12:506–507
Patterson LM, Zheng H, Ward SM, Berthoud H-R (2003) Vanilloid receptor (VR1) expression in vagal afferent neurons innervating the gastrointestinal tract. Cell Tissue Res 311:277–287. doi:10.1007/s00441-002-0682-0
Pedersen SF, Owsianik G, Nilius B (2005) TRP channels: an overview. Cell Calcium 38:233–252. doi:10.1016/j.ceca.2005.06.028
Pedretti A, Marconi C, Bettinelli I, Vistoli G (2009) Comparative modeling of the quaternary structure for the human TRPM8 channel and analysis of its binding features. Biochim Biophys Acta Biomembr 1788:973–982. doi:10.1016/j.bbamem.2009.02.007
Peier AM, Moqrich A, Hergarden AC et al (2002a) A TRP channel that senses cold stimuli and menthol. Cell 108:705–715
Peier AM, Reeve AJ, Andersson DA et al (2002b) A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046–2049. doi:10.1126/science.1073140
Pelegrín P (2011) Many ways to dilate the P2X7 receptor pore. Br J Pharmacol 163:908–911. doi:10.1111/j.1476-5381.2011.01325.x
Puopolo M, Binshtok AM, Yao G-L et al (2013) Permeation and block of TRPV1 channels by the cationic lidocaine derivative QX-314. J Neurophysiol 109:1704–1712. doi:10.1152/jn.00012.2013
Qin N, Neeper MP, Liu Y et al (2008) TRPV2 is activated by cannabidiol and mediates CGRP release in cultured rat dorsal root ganglion neurons. J Neurosci 28:6231–6238. doi:10.1523/JNEUROSCI.0504-08.2008
Roberts LA, Connor M (2006) TRPV1 antagonists as a potential treatment for hyperalgesia. Recent Pat CNS Drug Discov 1:65–76. doi:10.2174/1574889810601010065
Romanenko V, Nakamoto T, Srivastava A et al (2006) Molecular identification and physiological roles of parotid acinar cell maxi-K channels. J Biol Chem 281:27964–27972. doi:10.1074/jbc.M603871200
Sabirov RZ, Okada Y (2005) ATP release via anion channels. Purinergic Signal 1:311–328. doi:10.1007/s11302-005-1557-0
Schaefer M (2005) Homo- and heteromeric assembly of TRP channel subunits. Pflugers Arch 451:35–42. doi:10.1007/s00424-005-1467-6
Schilling WP, Sinkins WG, Estacion M (1999a) Maitotoxin activates a nonselective cation channel and a P2Z/P2X(7)-like cytolytic pore in human skin fibroblasts. Am J Physiol 277:C755–C765
Schilling WP, Wasylyna T, Dubyak GR et al (1999b) Maitotoxin and P2Z/P2X(7) purinergic receptor stimulation activate a common cytolytic pore. Am J Physiol 277:C766–C776
Seo HS, Roh DH, Yoon SY et al (2010) Peripheral acid-sensing ion channels and P2X receptors contribute to mechanical allodynia in a rodent thrombus-induced ischemic pain model. J Pain 11:718–727. doi:10.1016/j.jpain.2009.10.010
Seo HS, Roh DH, Kwon SG et al (2011) Acidic pH facilitates peripheral αβmeATP-mediated nociception in rats: Differential roles of P2X, P2Y, ASIC and TRPV1 receptors in ATP-induced mechanical allodynia and thermal hyperalgesia. Neuropharmacology 60:580–586. doi:10.1016/j.neuropharm.2010.12.009
Siebert AP, Ma Z, Grevet JD et al (2013) Structural and functional similarities of calcium homeostasis modulator 1 (CALHM1) ion channel with connexins, pannexins, and innexins. J Biol Chem 288:6140–6153. doi:10.1074/jbc.M112.409789
Smart D, Gunthorpe MJ, Jerman JC et al (2000) The endogenous lipid anandamide is a full agonist at the human vanilloid receptor (hVR1). Br J Pharmacol 129:227–230. doi:10.1038/sj.bjp.0703050
Smith GD, Gunthorpe MJ, Kelsell RE et al (2002) TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418:186–190. doi:10.1038/nature00894
Stepanyan RS, Indzhykulian AA, Catalinavélez-Ortega A et al (2011) TRPA1-mediated accumulation of aminoglycosides in mouse cochlear outer hair cells. JARO - J Assoc Res Otolaryngol 12:729–740. doi:10.1007/s10162-011-0288-x
Steyger PS, Karasawa T (2008) Intra-cochlear trafficking of aminoglycosides. Commun Integr Biol 1:140–142. doi:10.4161/cib.1.2.6888
Story GM, Peier AM, Reeve AJ et al (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–829. doi:10.1016/S0092-8674(03)00158-2
Strotmann R, Harteneck C, Nunnenmacher K et al (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2:695–702. doi:10.1038/35036318
Surprenant A, Rassendren F, Kawashima E et al (1996) The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science 272:735–738. doi:10.1126/science.272.5262.735
Ternesten-Hasséus E, Johansson E-L, Millqvist E (2015) Cough reduction using capsaicin. Respir Med 109:27–37. doi:10.1016/j.rmed.2014.11.001
Tominaga M, Caterina MJ, Malmberg AB et al (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21:531–543
Toychiev AH, Sabirov RZ, Takahashi N et al (2009) Activation of maxi-anion channel by protein tyrosine dephosphorylation. Am J Physiol Cell Physiol 297:C990–C1000. doi:10.1152/ajpcell.00131.2009
Tsavaler L, Shapero MH, Morkowski S, Laus R (2001) Trp-p8, a novel prostate-specific gene, is up-regulated in prostate cancer and other malignancies and shares high homology with transient receptor potential calcium channel proteins. Cancer Res 61:3760–3769
Tsuzuki K, Xing H, Ling J, Gu JG (2004) Menthol-induced Ca2+ release from presynaptic Ca2+ stores potentiates sensory synaptic transmission. J Neurosci 24:762–771. doi:10.1523/JNEUROSCI.4658-03.2004
Valtschanoff JG, Rustioni A, Guo A, Hwang SJ (2001) Vanilloid receptor VR1 is both presynaptic and postsynaptic in the superficial laminae of the rat dorsal horn. J Comp Neurol 436:225–235. doi:10.1002/cne.1063
Veldhuis NA, Lew MJ, Abogadie FC et al (2012) N-glycosylation determines ionic permeability and desensitization of the TRPV1 capsaicin receptor. J Biol Chem 287:21765–21772. doi:10.1074/jbc.M112.342022
Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417. doi:10.1146/annurev.biochem.75.103004.142819
Voets T, Prenen J, Vriens J et al (2002) Molecular determinants of permeation through the cation channel TRPV4. J Biol Chem 277:33704–33710. doi:10.1074/jbc.M204828200
Voets T, Droogmans G, Wissenbach U et al (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430:748–754. doi:10.1038/nature02732
Voets T, Talavera K, Owsianik G, Nilius B (2005) Sensing with TRP channels. Nat Chem Biol 1:85–92. doi:10.1038/nchembio0705-85
Vriens J, Janssens A, Prenen J et al (2004) TRPV channels and modulation by hepatocyte growth factor/scatter factor in human hepatoblastoma (HepG2) cells. Cell Calcium 36:19–28. doi:10.1016/j.ceca.2003.11.006
Watanabe H, Davis JB, Smart D et al (2002) Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem 277:13569–13577. doi:10.1074/jbc.M200062200
Wes PD, Chevesich J, Jeromin A et al (1995) TRPC1, a human homolog of a Drosophila store-operated channel. Proc Natl Acad Sci U S A 92:9652–9656. doi:10.1073/pnas.92.21.9652
Xu H, Ramsey IS, Kotecha SA (2002) TRPV3 is a calcium-permeable temperature-sensitive cation channel. 418:181–186. doi:10.1038/nature00850.1
Xu H, Delling M, Jun JC, Clapham DE (2006) Oregano, thyme and clove-derived flavors and skin sensitizers activate specific TRP channels. 9:628–635. doi:10.1038/nn1692
Yao J, Liu B, Qin F (2011) Modular thermal sensors in temperature-gated transient receptor potential (TRP) channels. Proc Natl Acad Sci U S A 108:11109–11114. doi:10.1073/pnas.1105196108
Yoneda T, Hata K, Nakanishi M et al (2011) Involvement of acidic microenvironment in the pathophysiology of cancer-associated bone pain. Bone 48:100–105. doi:10.1016/j.bone.2010.07.009
Yu S, Gao G, Peterson BZ, Ouyang A (2009) TRPA1 in mast cell activation-induced long-lasting mechanical hypersensitivity of vagal afferent C-fibers in guinea pig esophagus. Am J Physiol Gastrointest Liver Physiol 297:G34–G42. doi:10.1152/ajpgi.00068.2009
Zhang L, Barritt GJ (2004) Evidence that TRPM8 is an androgen-dependent Ca 2 + channel required for the survival of prostate cancer cells evidence that TRPM8 is an androgen-dependent Ca 2 ؉ channel required for the survival of prostate cancer cells. 8365–8373. doi:10.1158/0008-5472.CAN-04-2146
Acknowledgments
We are grateful to Dr. Ricardo Augusto de Melo Reis for the support and collaboration. This work was supported by grants from FAPERJ, CNPq, and Oswaldo Cruz Institute.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Rights and permissions
About this article
Cite this article
Ferreira, L.G.B., Faria, R.X. TRPing on the pore phenomenon: what do we know about transient receptor potential ion channel-related pore dilation up to now?. J Bioenerg Biomembr 48, 1–12 (2016). https://doi.org/10.1007/s10863-015-9634-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10863-015-9634-8