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TRP Channels in Sensory Transduction pp 1–39Cite as

Biophysical and Molecular Features of Thermosensitive TRP Channels Involved in Sensory Transduction

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Abstract

Temperature is one of the physical variables that cells and biological organisms constantly monitor to achieve homeostasis and maintain chemical reactions at a suitable speed for the living environment to which they are adapted. In order to monitor and maintain temperature on a constant basis, thermosensitive molecules were selected during evolution. One of the most remarkable sets of molecules acting as sensors is constituted by thermosensitive transient receptor potential channels (thermoTRP channels). TRP channels are a superfamily of non-selective tetrameric cation channels closely related to the classic superfamily of voltage-gated channels, having a set of distinctive sequence elements in common, while acting as polymodal receptors. This latter ability is what makes them suitable for integrating many kinds of signals in different cells, ranging from chemical to physical stimulation (i.e.: temperature-, mechano- and chemo-sensitivity). These channels act as allosteric proteins modifying sensitivity to one stimulus in the presence of another, and thus allowing the integration of many different signaling processes that are critical for sensing the extracellular and intracellular environment and for maintaining homeostasis. This ability has made them vital for life support. Several subfamilies of TRP channels have been described. From these subfamilies, some types of channels have been distinguished as being temperature-sensitive, such as TRPV1–4, TRPM 2–5/8, TRPA1 and TRPC5. In this chapter, thermosensitivity will be defined. Then, we will describe the thermosensitive molecules identified so far, focusing our analysis on ion channels, particularly on thermosensitive TRP channels involved in sensory transduction. Their gating and permeation properties and gating modifiers shall be at the center of the discussion so as to place them in the context of ion channels and life evolution.

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References

  • Ahern GP, Brooks IM, Miyares RL, Wang XB (2005) Extracellular cations sensitize and gate capsaicin receptor TRPV1 modulating pain signaling. J Neurosci 25:5109–5116

    CAS  PubMed  Google Scholar 

  • Akopian AN (2011) Regulation of nociceptive transmission at the periphery via TRPA1-TRPV1 interactions. Curr Pharm Biotechnol 12:89–94

    CAS  PubMed  Google Scholar 

  • Al-Fageeh MB, Smales CM (2006) Control and regulation of the cellular responses to cold shock: the responses in yeast and mammalian systems. Biochem J 397:247–259

    PubMed Central  CAS  PubMed  Google Scholar 

  • Alessandri-Haber N, Joseph E, Dina OA, Liedtke W, Levine JD (2005) TRPV4 mediates pain-related behavior induced by mild hypertonic stimuli in the presence of inflammatory mediator. Pain 118:70–79

    CAS  PubMed  Google Scholar 

  • Alpizar YA, Gees M, Sanchez A, Apetrei A, Voets T, Nilius B, Talavera K (2013) Bimodal effects of cinnamaldehyde and camphor on mouse TRPA1. Pflugers Arch 465:853–864

    CAS  PubMed  Google Scholar 

  • Andersson DA, Chase HW, Bevan S (2004) TRPM8 activation by menthol, icilin, and cold is differentially modulated by intracellular pH. J Neurosci 24:5364–5369

    CAS  PubMed  Google Scholar 

  • Babes A (2009) Ion channels involved in cold detection in mammals: TRP and non-TRP mechanisms. Biophys Rev 1:193–200

    CAS  Google Scholar 

  • Baez-Nieto D, Castillo JP, Dragicevic C, Alvarez O, Latorre R (2011) Thermo-TRP channels: biophysics of polymodal receptors. Adv Exp Med Biol 704:469–490

    CAS  PubMed  Google Scholar 

  • Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849–857

    CAS  PubMed  Google Scholar 

  • Bandell M, Dubin AE, Petrus MJ, Orth A, Mathur J, Hwang SW, Patapoutian A (2006) High-throughput random mutagenesis screen reveals TRPM8 residues specifically required for activation by menthol. Nat Neurosci 9:493–500

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Bargal R, Avidan N, Ben-Asher E, Olender Z, Zeigler M, Frumkin A, Raas-Rothschild A, Glusman G, Lancet D, Bach G (2000) Identification of the gene causing mucolipidosis type IV. Nat Genet 26:118–123

    CAS  PubMed  Google Scholar 

  • Baroiller JF, D’Cotta H (2001) Environment and sex determination in farmed fish. Comp Biochem Physiol C Toxicol Pharmacol 130:399–409

    CAS  PubMed  Google Scholar 

  • Bassi MT, Manzoni M, Monti E, Pizzo MT, Ballabio A, Borsani G (2000) Cloning of the gene encoding a novel integral membrane protein, mucolipidin-and identification of the two major founder mutations causing mucolipidosis type IV. Am J Hum Genet 67:1110–1120

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bautista D, Julius D (2008) Fire in the hole: pore dilation of the capsaicin receptor TRPV1. Nat Neurosci 11:528–529

    CAS  PubMed  Google Scholar 

  • Bautista DM, Jordt SE, Nikai T, Tsuruda PR, Read AJ, Poblete J, Yamoah EN, Basbaum AI, Julius D (2006) TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124:1269–1282

    CAS  PubMed  Google Scholar 

  • Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, Stucky CL, Jordt SE, Julius D (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448:204–208

    CAS  PubMed  Google Scholar 

  • Beech, DJ (2007) Canonical transient receptor potential 5. Handb Exp Pharmacol 179:109-123

    Google Scholar 

  • Benedikt J, Samad A, Ettrich R, Teisinger J, Vlachova V (2009) Essential role for the putative S6 inner pore region in the activation gating of the human TRPA1 channel. Biochim Biophys Acta 1793:1279–1288

    CAS  PubMed  Google Scholar 

  • Bidaux G, Beck B, Zholos A, Gordienko D, Lemonnier L, Flourakis M, Roudbaraki M, Borowiec AS, Fernandez J, Delcourt P, Lepage G, Shuba Y, Skryma R, Prevarskaya N (2012) Regulation of activity of transient receptor potential melastatin 8 (TRPM8) channel by its short isoforms. J Biol Chem 287:2948–2962

    PubMed Central  CAS  PubMed  Google Scholar 

  • Blair NT, Kaczmarek JS, Clapham DE (2009) Intracellular calcium strongly potentiates agonist-activated TRPC5 channels. J Gen Physiol 133:525–546

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bodding M, Wissenbach U, Flockerzi V (2007) Characterisation of TRPM8 as a pharmacophore receptor. Cell Calcium 42:618–628

    PubMed  Google Scholar 

  • Boukalova S, Marsakova L, Teisinger J, Vlachova V. 2010. Conserved residues within the putative S4-S5 region serve distinct functions among thermosensitive vanilloid transient receptor potential (TRPV) channels. J Biol Chem 285:41455–41462

    Google Scholar 

  • 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 USA 101:15494–15499

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brauchi S, Orta G, Salazar M, Rosenmann E, Latorre R (2006) A hot-sensing cold receptor: C-terminal domain determines thermosensation in transient receptor potential channels. J Neurosci 26:4835–4840

    CAS  PubMed  Google Scholar 

  • Brauchi S, Orta G, Mascayano C, Salazar M, Raddatz N, Urbina H, Rosenmann E, Gonzalez-Nilo F, Latorre R (2007) Dissection of the components for PIP2 activation and thermosensation in TRP channels. Proc Natl Acad Sci U S A 104:10246–10251

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cao E, Cordero-Morales JF, Liu B, Qin F, Julius D (2013a) TRPV1 channels are intrinsically heat sensitive and negatively regulated by phosphoinositide lipids. Neuron 77:667–679

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cao E, Liao M, Cheng Y, Julius D (2013b) TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504:113–118

    PubMed Central  CAS  PubMed  Google Scholar 

  • Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:816–824

    CAS  PubMed  Google Scholar 

  • Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436–441

    CAS  PubMed  Google Scholar 

  • Cesare P, McNaughton P (1996) A novel heat-activated current in nociceptive neurons and its sensitization by bradykinin. Proc Natl Acad Sci U S A 93:15435–15439

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chen J, Kim D, Bianchi BR, Cavanaugh EJ, Faltynek CR, Kym PR, Reilly RM (2009) Pore dilation occurs in TRPA1 but not in TRPM8 channels. Mol Pain 5:3

    PubMed Central  PubMed  Google Scholar 

  • Chen J, Kang D, Xu J, Lake M, Hogan JO, Sun C, Walter K, Yao B, Kim D (2013) Species differences and molecular determinant of TRPA1 cold sensitivity. Nat Commun 4:2501

    PubMed Central  PubMed  Google Scholar 

  • Chuang HH, Neuhausser WM, Julius D (2004) The super-cooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron 43:859–869

    CAS  PubMed  Google Scholar 

  • Chun JN, Lim JM, Kang Y, Kim EH, Shin YC, Kim HG, Jang D, Kwon D, Shin SY, So I, Jeon JH (2013) A network perspective on unraveling the role of TRP channels in biology and disease. Pflugers Archiv: Eur J Physiol. doi:10.1007/s00424-013-1292-2

    Google Scholar 

  • Chung MK, Lee H, Caterina MJ (2003) Warm temperatures activate TRPV4 in mouse 308 keratinocytes. J Biol Chem 278:32037–32046

    CAS  PubMed  Google Scholar 

  • Chung MK, Lee H, Mizuno A, Suzuki M, Caterina MJ (2004) 2-aminoethoxydiphenyl borate activates and sensitizes the heat-gated ion channel TRPV3. J Neurosci 24:5177–5182

    CAS  PubMed  Google Scholar 

  • Chung MK, Guler 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

    CAS  PubMed  Google Scholar 

  • Clapham DE (2003) TRP channels as cellular sensors. Nature 426:517–524

    CAS  PubMed  Google Scholar 

  • Clapham DE, Runnels LW, Strubing C (2001) The TRP ion channel family. Nat Rev Neurosci 2:387–396

    CAS  PubMed  Google Scholar 

  • Colburn RW, Lubin ML, Stone DJ Jr, Wang Y, Lawrence D, D’Andrea MR, Brandt MR, Liu Y, Flores CM, Qin N (2007) Attenuated cold sensitivity in TRPM8 null mice. Neuron 54:379–386

    CAS  PubMed  Google Scholar 

  • Cole KS, Moore JW (1960) Potassium ion current in the squid giant axon: dynamic characteristic. Biophys J 1:1–14

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cordero-Morales JF, Gracheva EO, Julius D (2011) Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli. Proc Natl Acad Sci U S A 108:E1184–1191

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cosens DJ, Manning A (1969) Abnormal electroretinogram from a Drosophila mutant. Nature 224:285–287

    CAS  PubMed  Google Scholar 

  • Csanady L, Torocsik B (2009) Four Ca2+ ions activate TRPM2 channels by binding in deep crevices near the pore but intracellularly of the gate. J Gen Physiol 133:189–203

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dattilo M, Penington NJ, Williams K (2008) Inhibition of TRPC5 channels by intracellular ATP. Mol Pharmacol 73:42–49

    CAS  PubMed  Google Scholar 

  • De Petrocellis L, Chu CJ, Moriello AS, Kellner JC, Walker JM, Di Marzo V (2004) Actions of two naturally occurring saturated N-acyldopamines on transient receptor potential vanilloid 1 (TRPV1) channels. Br J Pharmacol 143:251–256

    PubMed Central  PubMed  Google Scholar 

  • del Camino D, Murphy S, Heiry M, Barrett LB, Earley TJ, Cook CA, Petrus MJ, Zhao M, D’Amours M, Deering N, Brenner GJ, Costigan M, Hayward NJ, Chong JA, Fanger CM, Woolf CJ, Patapoutian A, Moran MM (2010) TRPA1 contributes to cold hypersensitivity. J Neurosci 30:15165–15174

    PubMed Central  PubMed  Google Scholar 

  • Delany NS, Hurle M, Facer P, Alnadaf T, Plumpton C, Kinghorn I, See CG, Costigan M, Anand P, Woolf CJ, Crowther D, Sanseau P, Tate SN (2001) Identification and characterization of a novel human vanilloid receptor-like protein, VRL-2. Physiol Genomics 4:165–174

    CAS  PubMed  Google Scholar 

  • Denis V, Cyert MS (2002) Internal Ca(2+) release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol 156:29–34

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dhaka A, Viswanath V, Patapoutian A (2006) TRP ion channels and temperature sensation. Annu Rev Neurosci 29:135–161

    CAS  PubMed  Google Scholar 

  • Dhaka A, Murray AN, Mathur J, Earley TJ, Petrus MJ, Patapoutian A (2007) TRPM8 is required for cold sensation in mice. Neuron 54:371–378

    CAS  PubMed  Google Scholar 

  • Digel I, Kayser P, Artmann GM (2008) Molecular processes in biological thermosensation. J Biophys 2008:60287

    Google Scholar 

  • Doerner JF, Gisselmann G, Hatt H, Wetzel CH (2007) Transient receptor potential channel A1 is directly gated by calcium ions. J Biol Chem 282:13180–13189

    CAS  PubMed  Google Scholar 

  • Dragoni I, Guida E, McIntyre P (2006) The cold and menthol receptor TRPM8 contains a functionally important double cysteine motif. J Biol Chem 281:37353–37360

    CAS  PubMed  Google Scholar 

  • Eisfeld J, Luckhoff A (2007) TRPM2. Handb Exp Pharmacol 179:237–252

    CAS  PubMed  Google Scholar 

  • Erler I, Al-Ansary DM, Wissenbach U, Wagner TF, Flockerzi V, Niemeyer BA (2006) Trafficking and assembly of the cold-sensitive TRPM8 channel. J Biol Chem 281:38396–38404

    CAS  PubMed  Google Scholar 

  • Fajardo O, Meseguer V, Belmonte C, Viana F (2008) TRPA1 channels mediate cold temperature sensing in mammalian vagal sensory neurons: pharmacological and genetic evidence. J Neurosci 28:7863–7875

    CAS  PubMed  Google Scholar 

  • Fernandez JA, Skryma R, Bidaux G, Magleby KL, Scholfield CN, McGeown JG, Prevarskaya N, Zholos AV (2011) Voltage- and cold-dependent gating of single TRPM8 ion channels. J Gen Physiol 137:173–195

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fernandez JA, Skryma R, Bidaux G, Magleby KL, Scholfield CN, McGeown JG, Prevarskaya N, Zholos AV (2012) Short isoforms of the cold receptor TRPM8 inhibit channel gating by mimicking heat action rather than chemical inhibitors. J Biol Chem 287:2963–2970

    PubMed Central  CAS  PubMed  Google Scholar 

  • Garcia-Martinez C, Morenilla-Palao C, Planells-Cases R, Merino JM, Ferrer-Montiel A (2000) Identification of an aspartic residue in the P-loop of the vanilloid receptor that modulates pore properties. J Biol Chem 275:32552–32558

    CAS  PubMed  Google Scholar 

  • Garcia-Sanz N, Fernandez-Carvajal A, Morenilla-Palao C, Planells-Cases R, Fajardo-Sanchez E, Fernandez-Ballester G, Ferrer-Montiel A (2004) Identification of a tetramerization domain in the C terminus of the vanilloid receptor. J Neurosci 24:5307–5314

    CAS  PubMed  Google Scholar 

  • Gaudet R (2008) A primer on ankyrin repeat function in TRP channels and beyond. Mol Biosyst 4:372–379

    PubMed Central  CAS  PubMed  Google Scholar 

  • Goel M, Sinkins WG, Schilling WP (2002) Selective association of TRPC channel subunits in rat brain synaptosomes. J Biol Chem 277:48303–48310

    CAS  PubMed  Google Scholar 

  • Gomis A, Soriano S, Belmonte C, Viana F (2008) Hypoosmotic- and pressure-induced membrane stretch activate TRPC5 channels. J Physiol 586:5633–5649

    PubMed Central  CAS  PubMed  Google Scholar 

  • Gong Z, Son W, Chung YD, Kim J, Shin DW, McClung CA, Lee Y, Lee HW, Chang DJ, Kaang BK, Cho H, Oh U, Hirsh J, Kernan MJ, Kim C (2004) Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. J Neurosci 24:9059–9066

    CAS  PubMed  Google Scholar 

  • Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G, Chesler AT, Sanchez EE, Perez JC, Weissman JS, Julius D (2010) Molecular basis of infrared detection by snakes. Nature 464:1006–1011

    PubMed Central  CAS  PubMed  Google Scholar 

  • Grandl J, Hu H, Bandell M, Bursulaya B, Schmidt M, Petrus M, Patapoutian A (2008) Pore region of TRPV3 ion channel is specifically required for heat activation. Nat Neurosci 11:1007–1013

    PubMed Central  CAS  PubMed  Google Scholar 

  • Grandl J, Kim SE, Uzzell V, Bursulaya B, Petrus M, Bandell M, Patapoutian A (2010) Temperature-induced opening of TRPV1 ion channel is stabilized by the pore domain. Nat Neurosci 13:708–714

    PubMed Central  CAS  PubMed  Google Scholar 

  • Grimm C, Kraft R, Sauerbruch S, Schultz G, Harteneck C (2003) Molecular and functional characterization of the melastatin-related cation channel TRPM3. J Biol Chem 278:21493–21501

    CAS  PubMed  Google Scholar 

  • Grycova L, Holendova B, Bumba L, Bily J, Jirku M, Lansky Z, Teisinger J (2012) Integrative binding sites within intracellular termini of TRPV1 receptor. PloS One 7:e48437

    PubMed Central  CAS  PubMed  Google Scholar 

  • Guinamard R, Salle L, Simard C (2011) The non-selective monovalent cationic channels TRPM4 and TRPM5. Adv Exp Med Biol 704:147–171

    CAS  PubMed  Google Scholar 

  • Gutman GA, Chandy KG, Adelman JP, Aiyar J, Bayliss DA, Clapham DE, Covarriubias M, Desir GV, Furuichi K, Ganetzky B, Garcia ML, Grissmer S, Jan LY, Karschin A, Kim D, Kuperschmidt S, Kurachi Y, Lazdunski M, Lesage F, Lester HA, McKinnon D, Nichols CG, O’Kelly I, Robbins J, Robertson GA, Rudy B, Sanguinetti M, Seino S, Stuehmer W, Tamkun MM, Vandenberg CA, Wei A, Wulff H, Wymore RS (2003) International Union of Pharmacology. XLI. Compendium of voltage-gated ion channels: potassium channels. Pharmacol Rev 55:583–586

    CAS  PubMed  Google Scholar 

  • Hardie RC, Minke B (1992) The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8:643–651

    CAS  PubMed  Google Scholar 

  • Hellwig N, Plant TD, Janson W, Schafer M, Schultz G, Schaefer M (2004) TRPV1 acts as proton channel to induce acidification in nociceptive neurons. J Biol Chem 279:34553–34561

    CAS  PubMed  Google Scholar 

  • Hille B (2001) Ion channels of excitable membranes. Sinauer Associates Inc., Sunderland

    Google Scholar 

  • Hofmann T, Schaefer M, Schultz G, Gudermann T (2002) Subunit composition of mammalian transient receptor potential channels in living cells. Proc Natl Acad Sci U S A 99:7461–7466

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hofmann T, Chubanov V, Gudermann T, Montell C (2003) TRPM5 is a voltage-modulated and Ca(2+)-activated monovalent selective cation channel. Curr Biol 13:1153–1158

    CAS  PubMed  Google Scholar 

  • Holakovska B, Grycova L, Bily J, Teisinger J (2011) Characterization of calmodulin binding domains in TRPV2 and TRPV5 C-tails. Amino Acids 40:741–748

    CAS  PubMed  Google Scholar 

  • Hori T, Katafuchi T (1998) Cell biology and the functions of thermosensitive neurons in the brain. Prog Brain Res 115:9–23

    CAS  PubMed  Google Scholar 

  • Horrigan FT, Aldrich RW (2002) Coupling between voltage sensor activation, Ca2+ binding and channel opening in large conductance (BK) potassium channels. J Gen Physiol 120:267–305

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hu HZ, Gu Q, Wang C, Colton CK, Tang J, Kinoshita-Kawada M, Lee LY, Wood JD, Zhu MX (2004) 2-aminoethoxydiphenyl borate is a common activator of TRPV1, TRPV2, and TRPV3. J Biol Chem 279:35741–35748

    CAS  PubMed  Google Scholar 

  • Huang J, Zhang X, McNaughton PA (2006) Modulation of temperature-sensitive TRP channels. Semin Cell Dev Biol 17:638–645

    CAS  PubMed  Google Scholar 

  • Hui K, Guo Y, Feng ZP (2005) Biophysical properties of menthol-activated cold receptor TRPM8 channels. Biochem Biophys Res Commun 333:374–382

    CAS  PubMed  Google Scholar 

  • Hurme R, Rhen M (1998) Temperature sensing in bacterial gene regulation—what it all boils down to. Mol Microbiol 30:1–6

    CAS  PubMed  Google Scholar 

  • Huynh KW, Cohen MR, Chakrapani S, Holdaway HA, Stewart PL, Moiseenkova-Bell VY (2014) Structural insight into the assembly of TRPV channels. Structure 22:260–268

    CAS  PubMed  Google Scholar 

  • Hwang SW, Cho H, Kwak J, Lee SY, Kang CJ, Jung J, Cho S, Min KH, Suh YG, Kim D, Oh U (2000) Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc Natl Acad Sci U S A 97:6155–6160

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jara-Oseguera A, Islas LD (2013) The role of allosteric coupling on thermal activation of thermoTRP channels. Biophys J 104:2160–2169

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jemal I, Soriano S, Conte AL, Morenilla C, Gomis A (2013) G protein-coupled receptor signalling potentiates the osmo-mechanical activation of TRPC5 channels. Pflugers Arch466(8):1635–1646. doi:10.1007/s00424-013-1392-z

    Google Scholar 

  • Jin M, Berrout J, O’Neil RG (2011) Regulation of TRP channels by osmomechanical stress. In: Zhu MX (ed) TRP channels. Boca Raton. ISBN:9781439818602

    Google Scholar 

  • Jordt SE, Julius D (2002) Molecular basis for species-specific sensitivity to “hot” chili peppers. Cell 108:421–430

    CAS  PubMed  Google Scholar 

  • Jordt SE, Tominaga M, Julius D (2000) Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc Natl Acad Sci U S A 97:8134–8139

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jordt SE, McKemy DD, Julius D (2003) Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 13:487–492

    CAS  PubMed  Google Scholar 

  • Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestatt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260–265

    CAS  PubMed  Google Scholar 

  • Kang D, Choe C, Kim D (2005) Thermosensitivity of the two-pore domain K+ channels TREK-2 and TRAAK. J Physiol 564:103–116

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kang K, Panzano VC, Chang EC, Ni L, Dainis AM, Jenkins AM, Regna K, Muskavitch MA, Garrity PA (2012) Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481:76–80

    CAS  Google Scholar 

  • Karashima Y, Talavera K, Everaerts W, Janssens A, Kwan KY, Vennekens R, Nilius B, Voets T (2009) TRPA1 acts as a cold sensor in vitro and in vivo. Proc Natl Acad Sci U S A 106:1273–1278

    PubMed Central  CAS  PubMed  Google Scholar 

  • Karashima Y, Prenen J, Talavera K, Janssens A, Voets T, Nilius B (2010) Agonist-induced changes in Ca(2+) permeation through the nociceptor cation channel TRPA1. Biophys J 98:773–783

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kim J, Chung YD, Park DY, Choi S, Shin DW, Soh H, Lee HW, Son W, Yim J, Park CS, Kernan MJ, Kim C (2003) A TRPV family ion channel required for hearing in Drosophila. Nature 424:81–84

    CAS  PubMed  Google Scholar 

  • Kim SE, Patapoutian A, Grandl J (2013) Single residues in the outer pore of TRPV1 and TRPV3 have temperature-dependent conformations. PloS One 8:e59593

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kiselyov K, Chen J, Rbaibi Y, Oberdick D, Tjon-Kon-Sang S, Shcheynikov N, Muallem S, Soyombo A (2005) TRP-ML1 is a lysosomal monovalent cation channel that undergoes proteolytic cleavage. J Biol Chem 280:43218–43223

    CAS  PubMed  Google Scholar 

  • Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277–289

    CAS  PubMed  Google Scholar 

  • Latorre R, Brauchi S, Orta G, Zaelzer C, Vargas G (2007a) ThermoTRP channels as modular proteins with allosteric gating. Cell Calcium 42:427–438

    CAS  PubMed  Google Scholar 

  • Latorre R, Vargas G, Orta G, Brauchi S (2007b) Voltage and temperature gating of thermoTRP channels. In: Liedtke WB, Heller S (eds) TRP ion channel function in sensory transduction and cellular signaling cascades. Boca Raton. ISBN: 08493404899780849340482

    Google Scholar 

  • Latorre R, Morera FJ, Zaelzer C (2010) Allosteric interactions and the modular nature of the voltage- and Ca2+ -activated (BK) channel. J Physiol 588:3141–3148

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lau SY, Procko E, Gaudet R (2012) Distinct properties of Ca2+ -calmodulin binding to N- and C-terminal regulatory regions of the TRPV1 channel. J Gen Physiol 140:541–555

    PubMed Central  CAS  PubMed  Google Scholar 

  • Launay P, Fleig A, Perraud AL, Scharenberg AM, Penner R, Kinet JP (2002) TRPM4 is a Ca2+ -activated nonselective cation channel mediating cell membrane depolarization. Cell 109:397–407

    CAS  PubMed  Google Scholar 

  • Launay P, Cheng H, Srivatsan S, Penner R, Fleig A, Kinet JP (2004) TRPM4 regulates calcium oscillations after T cell activation. Science 306:1374–1377

    CAS  PubMed  Google Scholar 

  • Li M, Yu Y, Yang J (2011) Structural biology of TRP channels. Adv Exp Med Biol 704:1–23

    Google Scholar 

  • Liao M, Cao E, Julius D, Cheng Y (2013) Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504:107–112

    CAS  PubMed  Google Scholar 

  • Liedtke W, Choe Y, Marti-Renom MA, Bell AM, Denis CS, Sali A, Hudspeth AJ, Friedman JM, Heller S (2000) Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103:525–535

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lishko PV, Procko E, Jin X, Phelps CB, Gaudet R (2007) The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity. Neuron 54:905–918

    CAS  PubMed  Google Scholar 

  • Littleton JT, Ganetzky B (2000) Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26:35–43

    CAS  PubMed  Google Scholar 

  • Liu B, Qin F (2005) Functional control of cold- and menthol-sensitive TRPM8 ion channels by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:1674–1681

    CAS  PubMed  Google Scholar 

  • Liu B, Hui K, Qin F (2003) Thermodynamics of heat activation of single capsaicin ion channels VR1. Biophys J 85:1–19

    Google Scholar 

  • Lopez GA, Jan YN, Jan LY (1994) Evidence that the S6 segment of the shaker voltage-gated K+ channel comprises part of the pore. Nature 367:179–182

    CAS  PubMed  Google Scholar 

  • Lopez F, Delgado R, Lopez R, Bacigalupo J, Restrepo D (2014) Transduction for pheromones in the main olfactory epithelium is mediated by the Ca2+ -activated channel TRPM5. J Neurosci 34:3268–3278

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ludeman DA, Farrar N, Riesgo A, Paps J, Leys SP (2014) Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges. BMC Evol Biol 14:3

    PubMed Central  PubMed  Google Scholar 

  • Macpherson LJ, Geierstanger BH, Viswanath V, Bandell M, Eid SR, Hwang S, Patapoutian A (2005) The pungency of garlic: activation of TRPA1 and TRPV1 in response to allicin. Curr Biol 15:929–934

    CAS  PubMed  Google Scholar 

  • Madrid R, Donovan-Rodriguez T, Meseguer V, Acosta MC, Belmonte C, Viana F (2006) Contribution of TRPM8 channels to cold transduction in primary sensory neurons and peripheral nerve terminals. J Neurosci 26:12512–12525

    CAS  PubMed  Google Scholar 

  • Madrid R, de la Pena E, Donovan-Rodriguez T, Belmonte C, Viana F (2009) Variable threshold of trigeminal cold-thermosensitive neurons is determined by a balance between TRPM8 and Kv1 potassium channels. J Neurosci 29:3120–3131

    CAS  PubMed  Google Scholar 

  • Maingret F, Lauritzen I, Patel AJ, Heurteaux C, Reyes R, Lesage F, Lazdunski M, Honore E (2000) TREK-1 is a heat-activated background K(+) channel. EMBO J 19:2483–2491

    PubMed Central  CAS  PubMed  Google Scholar 

  • Malkia A, Madrid R, Meseguer V, de la Pena E, Valero M, Belmonte C, Viana F (2007) Bidirectional shifts of TRPM8 channel gating by temperature and chemical agents modulate the cold sensitivity of mammalian thermoreceptors. J Physiol 581:155–174

    PubMed Central  CAS  PubMed  Google Scholar 

  • Malkia A, Pertusa M, Fernandez-Ballester G, Ferrer-Montiel A, Viana F (2009) Differential role of the menthol-binding residue Y745 in the antagonism of thermally gated TRPM8 channels. Mol Pain 5:62

    PubMed Central  PubMed  Google Scholar 

  • Mandal M, Breaker RR (2004) Gene regulation by riboswitches. Nat Rev Mol Cell Biol 5:451–463

    CAS  PubMed  Google Scholar 

  • Mandadi S, Sokabe T, Shibasaki K, Katanosaka K, Mizuno A, et al (2009) TRPV3 in keratinocytes transmits temperature information to sensory neurons via ATP. Pflugers Arch 458:1093–1102

    Google Scholar 

  • Manzoni M, Monti E, Bresciani R, Bozzato A, Barlati S, Bassi MT, Borsani G (2004) Overexpression of wild-type and mutant mucolipin proteins in mammalian cells: effects on the late endocytic compartment organization. FEBS Lett 567:219–224

    CAS  PubMed  Google Scholar 

  • Matta JA, Ahern GP (2007) Voltage is a partial activator of rat thermosensitive TRP channels. J Physiol 585:469–482

    PubMed Central  CAS  PubMed  Google Scholar 

  • McHugh D, Flemming R, Xu SZ, Perraud AL, Beech DJ (2003) Critical intracellular Ca2+ dependence of transient receptor potential melastatin 2 (TRPM2) cation channel activation. J Biol Chem 278:11002–11006

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • McNamara FN, Randall A, Gunthorpe MJ (2005) Effects of piperine, the pungent component of black pepper, at the human vanilloid receptor (TRPV1). Br J Pharmacol 144:781–790

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mei ZZ, Xia R, Beech DJ, Jiang LH (2006) Intracellular coiled-coil domain engaged in subunit interaction and assembly of melastatin-related transient receptor potential channel 2. J Biol Chem 281:38748–38756

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mercado J, Gordon-Shaag A, Zagotta WN, Gordon SE (2010) Ca2+ -dependent desensitization of TRPV2 channels is mediated by hydrolysis of phosphatidylinositol 4,5-bisphosphate. J Neurosci 30:13338–13347

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mercer JB, Simon E (1984) A comparison between total body thermosensitivity and local thermosensitivity in mammals and birds. Pflugers Arch 400:228–234

    CAS  PubMed  Google Scholar 

  • Monteilh-Zoller MK, Hermosura MC, Nadler MJ, Scharenberg AM, Penner R, Fleig A (2003) TRPM7 provides an ion channel mechanism for cellular entry of trace metal ions. J Gen Physiol 121:49–60

    PubMed Central  CAS  PubMed  Google Scholar 

  • Montell C 2005. The TRP superfamily of cation channels. Sci STKE: Signal Transduct Knowl Environ 2005:re3

    Google Scholar 

  • Montell C, Rubin GM (1989) Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2:1313–1323

    CAS  PubMed  Google Scholar 

  • Montell C, Birnbaumer L, Flockerzi V (2002a) The TRP channels, a remarkably functional family. Cell 108:595–598

    CAS  PubMed  Google Scholar 

  • Montell C, Birnbaumer L, Flockerzi V, Bindels RJ, Bruford EA, Caterina MJ, Clapham DE, Harteneck C, Heller S, Julius D, Kojima I, Mori Y, Penner R, Prawitt D, Scharenberg AM, Schultz G, Shimizu N, Zhu MX (2002b) A unified nomenclature for the superfamily of TRP cation channels. Mol Cell 9:229–231

    CAS  PubMed  Google Scholar 

  • Moqrich A, Hwang SW, Earley TJ, Petrus MJ, Murray AN, Spencer KS, Andahazy M, Story GM, Patapoutian A (2005) Impaired thermosensation in mice lacking TRPV3, a heat and camphor sensor in the skin. Science 307:1468–1472

    CAS  PubMed  Google Scholar 

  • Muraki K, Iwata Y, Katanosaka Y, Ito T, Ohya S, Shigekawa M, Imaizumi Y (2003) TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ Res 93:829–838

    CAS  PubMed  Google Scholar 

  • Myers BR, Bohlen CJ, Julius D (2008) A yeast genetic screen reveals a critical role for the pore helix domain in TRP channel gating. Neuron 58:362–373

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nadler MJ, Hermosura MC, Inabe K, Perraud AL, Zhu Q, Stokes AJ, Kurosaki T, Kinet JP, Penner R, Scharenberg AM, Fleig A (2001) LTRPC7 is a Mg.ATP-regulated divalent cation channel required for cell viability. Nature 411:590–595

    CAS  PubMed  Google Scholar 

  • Nara T, Lee L, Imae Y (1991) Thermosensing ability of Trg and Tap chemoreceptors in Escherichia coli. J Bacteriol 173:1120–1124

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nauli SM, Alenghat FJ, Luo Y, Williams E, Vassilev P, Li X, Elia AE, Lu W, Brown EM, Quinn SJ, Ingber DE, Zhou J (2003) Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells. Nat Genet 33:129–137

    CAS  PubMed  Google Scholar 

  • Nelson DL, Lehninger AL, Cox MM (2008) Lehninger principles of biochemistry. Macmillan. ISBN: 071677108X

    Google Scholar 

  • Nilius B, Owsianik G (2011) The transient receptor potential family of ion channels. Genome Biol 12:218

    CAS  PubMed  Google Scholar 

  • Nilius B, Vennekens R, Prenen J, Hoenderop JG, Droogmans G, Bindels RJ (2001) The single pore residue Asp542 determines Ca2+ permeation and Mg2+ block of the epithelial Ca2+ channel. J Biol Chem 276:1020–1025

    CAS  PubMed  Google Scholar 

  • Nilius B, Prenen J, Droogmans G, Voets T, Vennekens R, Freichel M, Wissenbach U, Flockerzi V (2003) Voltage dependence of the Ca2+ -activated cation channel TRPM4. J Biol Chem 278:30813–30820

    CAS  PubMed  Google Scholar 

  • Nilius B, Prenen J, Janssens A, Voets T, Droogmans G (2004a) Decavanadate modulates gating of TRPM4 cation channels. J Physiol 560:753–765

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nilius B, Prenen J, Voets T, Droogmans G (2004b) Intracellular nucleotides and polyamines inhibit the Ca2+ -activated cation channel TRPM4b. Pflugers Arch 448:70–75

    CAS  PubMed  Google Scholar 

  • Nilius B, Prenen J, Janssens A, Owsianik G, Wang C, Zhu MX, Voets T (2005a) The selectivity filter of the cation channel TRPM4. J Biol Chem 280:22899–22906

    CAS  PubMed  Google Scholar 

  • Nilius B, Talavera K, Owsianik G, Prenen J, Droogmans G, Voets T (2005b) Gating of TRP channels: a voltage connection? J Physiol 567:35–44

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nilius B, Prenen J, Owsianik G (2011) Irritating channels: the case of TRPA1. J Physiol 589:1543–1549

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nilius B, Appendino G, Owsianik G (2012) The transient receptor potential channel TRPA1: from gene to pathophysiology. Pflugers Arch 464:425–458

    CAS  PubMed  Google Scholar 

  • Numazaki M, Tominaga T, Takeuchi K, Murayama N, Toyooka H, Tominaga M (2003) Structural determinant of TRPV1 desensitization interacts with calmodulin. Proc Natl Acad Sci U S A 100:8002–8006

    PubMed Central  CAS  PubMed  Google Scholar 

  • Oberwinkler J, Phillipp SE (2007) TRPM3. Handb Exp Pharmacol 179:253–267

    Google Scholar 

  • Obukhov AG, Nowycky MC (2005) A cytosolic residue mediates Mg2+ block and regulates inward current amplitude of a transient receptor potential channel. J Neurosci 25:1234–1239

    CAS  PubMed  Google Scholar 

  • Ordaz B, Tang J, Xiao R, Salgado A, Sampieri A, Zhu MX, Vaca L (2005) Calmodulin and calcium interplay in the modulation of TRPC5 channel activity. Identification of a novel C-terminal domain for calcium/calmodulin-mediated facilitation. J Biol Chem 280:30788–30796

    CAS  PubMed  Google Scholar 

  • Orio P, Latorre R (2005) Differential effects of beta 1 and beta 2 subunits on BK channel activity. J Gen Physiol 125:395–411

    PubMed Central  CAS  PubMed  Google Scholar 

  • Orio P, Madrid R, de la Pena E, Parra A, Meseguer V, Bayliss DA, Belmonte C, Viana F (2009) Characteristics and physiological role of hyperpolarization activated currents in mouse cold thermoreceptors. J Physiol 587:1961–1976

    PubMed Central  CAS  PubMed  Google Scholar 

  • Owsianik G, Talavera K, Voets T, Nilius B (2006) Permeation and selectivity of TRP channels. Annu Rev Physiol 68:685–717

    CAS  PubMed  Google Scholar 

  • Palmer CP, Zhou XL, Lin J, Loukin SH, Kung C, Saimi Y (2001) A TRP homolog in Saccharomyces cerevisiae forms an intracellular Ca(2+)-permeable channel in the yeast vacuolar membrane. Proc Natl Acad Sci U S A 98:7801–7805

    PubMed Central  CAS  PubMed  Google Scholar 

  • Papakosta M, Dalle C, Haythornthwaite A, Cao L, Stevens EB, Burgess G, Russell R, Cox PJ, Phillips SC, Grimm C (2011) The chimeric approach reveals that differences in the TRPV1 pore domain determine species-specific sensitivity to block of heat activation. J Biol Chem 286:39663–39672

    PubMed Central  CAS  PubMed  Google Scholar 

  • Park U, Vastani N, Guan Y, Raja SN, Koltzenburg M, Caterina MJ (2011) TRP vanilloid 2 knock-out mice are susceptible to perinatal lethality but display normal thermal and mechanical nociception. J Neurosci 31:11425–11436

    PubMed Central  CAS  PubMed  Google Scholar 

  • Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, Story GM, Earley TJ, Dragoni I, McIntyre P, Bevan S, Patapoutian A (2002a) A TRP channel that senses cold stimuli and menthol. Cell 108:705–715

    CAS  PubMed  Google Scholar 

  • Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, Hergarden AC, Story GM, Colley S, Hogenesch JB, McIntyre P, Bevan S, Patapoutian A (2002b) A heat-sensitive TRP channel expressed in keratinocytes. Science 296:2046–2049

    CAS  PubMed  Google Scholar 

  • Perraud AL, Fleig A, Dunn CA, Bagley LA, Launay P, Schmitz C, Stokes AJ, Zhu Q, Bessman MJ, Penner R, Kinet JP, Scharenberg AM (2001) ADP-ribose gating of the calcium-permeable LTRPC2 channel revealed by Nudix motif homology. Nature 411:595–599

    CAS  PubMed  Google Scholar 

  • Perraud AL, Schmitz C, Scharenberg AM (2003) TRPM2 Ca2+ permeable cation channels: from gene to biological function. Cell Calcium 33:519–531

    CAS  PubMed  Google Scholar 

  • Pertusa M, Madrid R, Morenilla-Palao C, Belmonte C, Viana F (2012) N-glycosylation of TRPM8 ion channels modulates temperature sensitivity of cold thermoreceptor neurons. J Biol Chem 287:18218–18229

    PubMed Central  CAS  PubMed  Google Scholar 

  • Petersen CC, Berridge MJ, Borgese MF, Bennett DL (1995) Putative capacitative calcium entry channels: expression of Drosophila trp and evidence for the existence of vertebrate homologues. Biochem J 311(Pt 1):41–44

    PubMed Central  CAS  PubMed  Google Scholar 

  • Petsko GA, Ringe D (2004) Protein structure and function. New Science Press

    Google Scholar 

  • Phelps CB, Gaudet R (2007) The role of the N terminus and transmembrane domain of TRPM8 in channel localization and tetramerization. J Biol Chem 282:36474–36480

    CAS  PubMed  Google Scholar 

  • Phelps CB, Wang RR, Choo SS, Gaudet R (2010) Differential regulation of TRPV1, TRPV3, and TRPV4 sensitivity through a conserved binding site on the ankyrin repeat domain. J Biol Chem 285:731–740

    PubMed Central  CAS  PubMed  Google Scholar 

  • Phillips AM, Bull A, Kelly LE (1992) Identification of a Drosophila gene encoding a calmodulin-binding protein with homology to the trp phototransduction gene. Neuron 8:631–642

    CAS  PubMed  Google Scholar 

  • Pieau C, Dorizzi M, Richard-Mercier N (2001) Temperature-dependent sex determination and gonadal differentiation in reptiles. EXS 117–141

    Google Scholar 

  • Premkumar LS, Agarwal S, Steffen D (2002) Single-channel properties of native and cloned rat vanilloid receptors. J Physiol 545:107–117

    PubMed Central  CAS  PubMed  Google Scholar 

  • Prescott ED, Julius D (2003) A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300:1284–1288

    Google Scholar 

  • Prober DA, Zimmerman S, Myers BR, McDermott BM Jr, Kim SH, Caron S, Rihel J, Solnica-Krezel L, Julius D, Hudspeth AJ, Schier AF (2008) Zebrafish TRPA1 channels are required for chemosensation but not for thermosensation or mechanosensory hair cell function. J Neurosci 28:10102–10110

    PubMed Central  CAS  PubMed  Google Scholar 

  • Prole DL, Taylor CW (2011) Identification of intracellular and plasma membrane calcium channel homologues in pathogenic parasites. PloS One 6:e26218

    PubMed Central  CAS  PubMed  Google Scholar 

  • Qin N, Neeper MP, Liu Y, Hutchinson TL, Lubin ML, Flores CM (2008) TRPV2 is activated by cannabidiol and mediates CGRP release in cultured rat dorsal root ganglion neurons. J Neurosci 28:6231–6238

    CAS  PubMed  Google Scholar 

  • Ramsey IS, Delling M, Clapham DE (2006) An introduction to TRP channels. Annu Rev Physiol 68:619–647

    CAS  PubMed  Google Scholar 

  • Reid G (2005) ThermoTRP channels and cold sensing: what are they really up to? Pflugers Archiv 451:250–263

    Google Scholar 

  • Rohacs T, Lopes CM, Michailidis I, Logothetis DE (2005) PI(4,5)P2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat Neurosci 8:626–634

    CAS  PubMed  Google Scholar 

  • Rosenbaum T, Gordon-Shaag A, Munari M, Gordon SE (2004) Ca2+/calmodulin modulates TRPV1 activation by capsaicin. J Gen Physiol 123:53–62

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ross RA (2003) Anandamide and vanilloid TRPV1 receptors. Br J Pharmacol 140:790–801

    PubMed Central  CAS  PubMed  Google Scholar 

  • Runnels LW, Yue L, Clapham DE (2001) TRP-PLIK, a bifunctional protein with kinase and ion channel activities. Science 291:1043–1047

    CAS  PubMed  Google Scholar 

  • Ryu S, Liu B, Yao J, Fu Q, Qin F (2007) Uncoupling proton activation of vanilloid receptor TRPV1. J Neurosci 27:12797–12807

    CAS  PubMed  Google Scholar 

  • Saito S, Shingai R (2006) Evolution of thermoTRP ion channel homologs in vertebrates. Physiol Genomics 27:219–230

    CAS  PubMed  Google Scholar 

  • Saito S, Fukuta N, Shingai R, Tominaga M (2011) Evolution of vertebrate transient receptor potential vanilloid 3 channels: opposite temperature sensitivity between mammals and western clawed frogs. PLoS Genet 7:e1002041

    PubMed Central  CAS  PubMed  Google Scholar 

  • Saito S, Nakatsuka K, Takahashi K, Fukuta N, Imagawa T, Ohta T, Tominaga M (2012) Analysis of transient receptor potential ankyrin 1 (TRPA1) in frogs and lizards illuminates both nociceptive heat and chemical sensitivities and coexpression with TRP vanilloid 1 (TRPV1) in ancestral vertebrates. J Biol Chem 287:30743–30754

    PubMed Central  CAS  PubMed  Google Scholar 

  • Salas MM, Hargreaves KM, Akopian AN (2009) TRPA1-mediated responses in trigeminal sensory neurons: interaction between TRPA1 and TRPV1. Eur J Neurosci 29:1568–1578

    PubMed Central  PubMed  Google Scholar 

  • Salazar H, Llorente I, Jara-Oseguera A, Garcia-Villegas R, Munari M, Gordon SE, Islas LD, Rosenbaum T (2008) A single N-terminal cysteine in TRPV1 determines activation by pungent compounds from onion and garlic. Nat Neurosci 11:255–261

    PubMed Central  CAS  PubMed  Google Scholar 

  • Samad A, Sura L, Benedikt J, Ettrich R, Minofar B, Teisinger J, Vlachova V (2011) The C-terminal basic residues contribute to the chemical- and voltage-dependent activation of TRPA1. Biochem J 433:197–204

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sano Y, Inamura K, Miyake A, Mochizuki S, Yokoi H, Matsushime H, Furuichi K (2001) Immunocyte Ca2+ influx system mediated by LTRPC2. Science 293:1327–1330

    CAS  PubMed  Google Scholar 

  • Sardar P, Kumar A, Bhandari A, Goswami C (2012) Conservation of tubulin-binding sequences in TRPV1 throughout evolution. PloS One 7:e31448

    PubMed Central  CAS  PubMed  Google Scholar 

  • Schaefer M (2005) Homo- and heteromeric assembly of TRP channel subunits. Pflugers Arch 451:35–42

    CAS  PubMed  Google Scholar 

  • Schlingmann KP, Weber S, Peters M, Niemann Nejsum L, Vitzthum H, Klingel K, Kratz M, Haddad E, Ristoff E, Dinour D, Syrrou M, Nielsen S, Sassen M, Waldegger S, Seyberth HW, Konrad M (2002) Hypomagnesemia with secondary hypocalcemia is caused by mutations in TRPM6, a new member of the TRPM gene family. Nat Genet 31:166–170

    CAS  PubMed  Google Scholar 

  • Schoppa NE, Sigworth FJ (1998) Activation of shaker potassium channels. III. An activation gating model for wild-type and V2 mutant channels. J Gen Physiol 111:313–342

    PubMed Central  CAS  PubMed  Google Scholar 

  • Semtner M, Schaefer M, Pinkenburg O, Plant TD (2007) Potentiation of TRPC5 by protons. J Biol Chem 282:33868–33878

    CAS  PubMed  Google Scholar 

  • Shimizu S, Yoshida T, Wakamori M, Ishii M, Okada T, Takahashi M, Seto M, Sakurada K, Kiuchi Y, Mori Y (2006) Ca2+ -calmodulin-dependent myosin light chain kinase is essential for activation of TRPC5 channels expressed in HEK293 cells. J Physiol 570:219–235

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96–99

    CAS  PubMed  Google Scholar 

  • Smith GD, Gunthorpe MJ, Kelsell RE, Hayes PD, Reilly P, Facer P, Wright JE, Jerman JC, Walhin JP, Ooi L, Egerton J, Charles KJ, Smart D, Randall AD, Anand P, Davis JB (2002) TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature 418:186–190

    CAS  PubMed  Google Scholar 

  • Staruschenko A, Jeske NA, Akopian AN (2010) Contribution of TRPV1-TRPA1 interaction to the single channel properties of the TRPA1 channel. J Biol Chem 285:15167–15177

    PubMed Central  CAS  PubMed  Google Scholar 

  • Stayner C, Zhou J (2001) Polycystin channels and kidney disease. Trends Pharmacol Sci 22:543–546

    CAS  PubMed  Google Scholar 

  • Stewart AP, Egressy K, Lim A, Edwardson JM (2010) AFM imaging reveals the tetrameric structure of the TRPM8 channel. Biochem Biophys Res Commun 394:383–386

    CAS  PubMed  Google Scholar 

  • Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–829

    CAS  PubMed  Google Scholar 

  • Strotmann R, Harteneck C, Nunnenmacher K, Schultz G, Plant TD (2000) OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity. Nat Cell Biol 2:695–702

    CAS  PubMed  Google Scholar 

  • Strotmann R, Schultz G, Plant TD (2003) Ca2+ -dependent potentiation of the nonselective cation channel TRPV4 is mediated by a C-terminal calmodulin binding site. J Biol Chem 278:26541–26549

    CAS  PubMed  Google Scholar 

  • Strotmann R, Semtner M, Kepura F, Plant TD, Schoneberg T (2010) Interdomain interactions control Ca2+ -dependent potentiation in the cation channel TRPV4. PloS One 5:e10580

    PubMed Central  PubMed  Google Scholar 

  • Strubing C, Krapivinsky G, Krapivinsky L, Clapham DE (2003) Formation of novel TRPC channels by complex subunit interactions in embryonic brain. J Biol Chem 278:39014–39019

    PubMed  Google Scholar 

  • Sun M, Goldin E, Stahl S, Falardeau JL, Kennedy JC, Acierno JS Jr, Bove C, Kaneski CR, Nagle J, Bromley MC, Colman M, Schiffmann R, Slaugenhaupt SA (2000) Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum Mol Genet 9:2471–2478

    CAS  PubMed  Google Scholar 

  • Sung TS, Jeon JP, Kim BJ, Hong C, Kim SY, Kim J, Jeon JH, Kim HJ, Suh CK, Kim SJ, So I (2011) Molecular determinants of PKA-dependent inhibition of TRPC5 channel. Am J Physiol Cell Physiol 301:C823–C832

    CAS  PubMed  Google Scholar 

  • Sura L, Zima V, Marsakova L, Hynkova A, Barvik I, Vlachova V (2012) C-terminal acidic cluster is involved in Ca2+ -induced regulation of human transient receptor potential ankyrin 1 channel. J Biol Chem 287:18067–18077

    PubMed Central  CAS  PubMed  Google Scholar 

  • Susankova K, Ettrich R, Vyklicky L, Teisinger J, Vlachova V (2007) Contribution of the putative inner-pore region to the gating of the transient receptor potential vanilloid subtype 1 channel (TRPV1). J Neurosci 27:7578–7585

    CAS  PubMed  Google Scholar 

  • Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N, Ninomiya Y, Margolskee RF, Nilius B (2005) Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438:1022–1025

    CAS  PubMed  Google Scholar 

  • Todaka H, Taniguchi J, Satoh J, Mizuno A, Suzuki M (2004) Warm temperature-sensitive transient receptor potential vanilloid 4 (TRPV4) plays an essential role in thermal hyperalgesia. J Biol Chem 279:35133–35138

    CAS  PubMed  Google Scholar 

  • Togashi K, Hara Y, Tominaga T, Higashi T, Konishi Y, Mori Y, Tominaga M (2006) TRPM2 activation by cyclic ADP-ribose at body temperature is involved in insulin secretion. EMBO J 25:1804–1815

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, Raumann BE, Basbaum AI, Julius D (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21:531–543

    CAS  PubMed  Google Scholar 

  • Tong Q, Zhang W, Conrad K, Mostoller K, Cheung JY, Peterson BZ, Miller BA (2006) Regulation of the transient receptor potential channel TRPM2 by the Ca2+ sensor calmodulin. J Biol Chem 281:9076–9085

    CAS  PubMed  Google Scholar 

  • Topala CN, Groenestege WT, Thebault S, van den Berg D, Nilius B, Hoenderop JG, Bindels RJ (2007) Molecular determinants of permeation through the cation channel TRPM6. Cell Calcium 41:513–523

    CAS  PubMed  Google Scholar 

  • Trevisani M, Smart D, Gunthorpe MJ, Tognetto M, Barbieri M, Campi B, Amadesi S, Gray J, Jerman JC, Brough SJ, Owen D, Smith GD, Randall AD, Harrison S, Bianchi A, Davis JB, Geppetti P (2002) Ethanol elicits and potentiates nociceptor responses via the vanilloid receptor-1. Nat Neurosci 5:546–551

    CAS  PubMed  Google Scholar 

  • Tse-Dinh YC, Qi H, Menzel R (1997) DNA supercoiling and bacterial adaptation: thermotolerance and thermoresistance. Trends Microbiol 5:323–326

    CAS  PubMed  Google Scholar 

  • Tsuruda PR, Julius D, Minor DL Jr (2006) Coiled coils direct assembly of a cold-activated TRP channel. Neuron 51:201–212

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ufret-Vincenty CA, Klein RM, Hua L, Angueyra J, Gordon SE (2011) Localization of the PIP2 sensor of TRPV1 ion channels. J Biol Chem 286:9688–9698

    PubMed Central  CAS  PubMed  Google Scholar 

  • Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417

    PubMed Central  CAS  PubMed  Google Scholar 

  • Venkatachalam K, Hofmann T, Montell C (2006) Lysosomal localization of TRPML3 depends on TRPML2 and the mucolipidosis-associated protein TRPML1. J Biol Chem 281:17517–17527

    PubMed Central  CAS  PubMed  Google Scholar 

  • Vennekens R, Nilius B (2007) Insights into TRPM4 function, regulation and physiological role. Handb Exp pharmacol. pp 269–285

    Google Scholar 

  • Vigh L, Maresca B, Harwood JL (1998) Does the membrane’s physical state control the expression of heat shock and other genes? Trends Biochem Sci 23:369–374

    CAS  PubMed  Google Scholar 

  • Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM, Hwang SW, Patapoutian A, Jegla T (2003) Opposite thermosensor in fruitfly and mouse. Nature 423:822–823

    CAS  PubMed  Google Scholar 

  • Vlachova V, Teisinger J, Susankova K, Lyfenko A, Ettrich R, Vyklicky L (2003) Functional role of C-terminal cytoplasmic tail of rat vanilloid receptor 1. J Neurosci 23:1340–1350

    CAS  PubMed  Google Scholar 

  • Voets T, Nilius B (2003) The pore of TRP channels: trivial or neglected? Cell Calcium 33:299–302

    CAS  PubMed  Google Scholar 

  • Voets T, Prenen J, Vriens J, Watanabe H, Janssens A, Wissenbach U, Bodding M, Droogmans G, Nilius B (2002) Molecular determinants of permeation through the cation channel TRPV4. J Biol Chem 277:33704–33710

    CAS  PubMed  Google Scholar 

  • Voets T, Janssens A, Prenen J, Droogmans G, Nilius B (2003) Mg2+ -dependent gating and strong inward rectification of the cation channel TRPV6. J Gen Physiol 121:245–260

    PubMed Central  CAS  PubMed  Google Scholar 

  • Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430:748–754

    CAS  PubMed  Google Scholar 

  • Voets T, Owsianik G, Janssens A, Talavera K, Nilius B (2007) TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat Chem Biol 3:174–182

    CAS  PubMed  Google Scholar 

  • Vriens J, Owsianik G, Hofmann T, Philipp SE, Stab J, Chen X, Benoit M, Xue F, Janssens A, Kerselaers S, Oberwinkler J, Vennekens R, Gudermann T, Nilius B, Voets T (2011) TRPM3 is a nociceptor channel involved in the detection of noxious heat. Neuron 70:482–494

    CAS  PubMed  Google Scholar 

  • Wagner TF, Loch S, Lambert S, Straub I, Mannebach S, Mathar I, Dufer M, Lis A, Flockerzi V, Philipp SE, Oberwinkler J (2008) Transient receptor potential M3 channels are ionotropic steroid receptors in pancreatic beta cells. Nat Cell Biol 10:1421–1430

    CAS  PubMed  Google Scholar 

  • Walder RY, Landau D, Meyer P, Shalev H, Tsolia M, Borochowitz Z, Boettger MB, Beck GE, Englehardt RK, Carmi R, Sheffield VC (2002) Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat Genet 31:171–174

    CAS  PubMed  Google Scholar 

  • Walker RG, Willingham AT, Zuker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229–2234

    CAS  PubMed  Google Scholar 

  • Wang G, Qiu YT, Lu T, Kwon HW, Pitts RJ, Van Loon JJ, Takken W, Zwiebel LJ (2009) Anopheles gambiae TRPA1 is a heat-activated channel expressed in thermosensitive sensilla of female antennae. Eur J Neurosci 30:967–974

    PubMed Central  PubMed  Google Scholar 

  • Wang H, Schupp M, Zurborg S, Heppenstall PA (2013) Residues in the pore region of Drosophila transient receptor potential A1 dictate sensitivity to thermal stimuli. J Physiol 591:185–201

    PubMed Central  CAS  PubMed  Google Scholar 

  • Watanabe H, Davis JB, Smart D, Jerman JC, Smith GD, Hayes P, Vriens J, Cairns W, Wissenbach U, Prenen J, Flockerzi V, Droogmans G, Benham CD, Nilius B (2002a) Activation of TRPV4 channels (hVRL-2/mTRP12) by phorbol derivatives. J Biol Chem 277:13569–13577

    CAS  PubMed  Google Scholar 

  • Watanabe H, Vriens J, Suh SH, Benham CD, Droogmans G, Nilius B (2002b) Heat-evoked activation of TRPV4 channels in a HEK293 cell expression system and in native mouse aorta endothelial cells. J Biol Chem 277:47044–47051

    CAS  PubMed  Google Scholar 

  • Wes PD, Chevesich J, Jeromin A, Rosenberg C, Stetten G, Montell C (1995) TRPC1, a human homolog of a Drosophila store-operated channel. Proc Natl Acad Sci U S A 92:9652–9656

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wirkner K, Hognestad H, Jahnel R, Hucho F, Illes P (2005) Characterization of rat transient receptor potential vanilloid 1 receptors lacking the N-glycosylation site N604. Neuroreport 16:997–1001

    CAS  PubMed  Google Scholar 

  • Wissenbach U, Bodding M, Freichel M, Flockerzi V (2000) Trp12, a novel Trp related protein from kidney. FEBS Lett 485:127–134

    CAS  PubMed  Google Scholar 

  • Wolstenholme AJ, Williamson SM, Reaves BJ (2011) TRP channels in parasites. Adv Exp Med Biol 704:359–371

    CAS  PubMed  Google Scholar 

  • Xiao R, Tang J, Wang C, Colton CK, Tian J, Zhu MX (2008) Calcium plays a central role in the sensitization of TRPV3 channel to repetitive stimulations. J Biol Chem 283:6162–6174

    PubMed Central  CAS  PubMed  Google Scholar 

  • Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA, Lawson D, Ge P, Lilly J, Silos-Santiago I, Xie Y, DiStefano PS, Curtis R, Clapham DE (2002) TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418:181–186

    CAS  PubMed  Google Scholar 

  • Xu H, Blair NT, Clapham DE (2005) Camphor activates and strongly desensitizes the transient receptor potential vanilloid subtype 1 channel in a vanilloid-independent mechanism. J Neurosci 25:8924–8937

    CAS  PubMed  Google Scholar 

  • Xu H, Delling M, Jun JC, Clapham DE (2006) Oregano, thyme and clove-derived flavors and skin sensitizers activate specific TRP channels. Nat Neurosci 9:628–635

    CAS  PubMed  Google Scholar 

  • Yang F, Cui Y, Wang K, Zheng J (2010) Thermosensitive TRP channel pore turret is part of the temperature activation pathway. Proc Natl Acad Sci U S A 107:7083–7088

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang F, Ma L, Cao X, Wang K, Zheng J (2014) Divalent cations activate TRPV1 through promoting conformational change of the extracellular region. J Gen Physiol 143:91–103

    PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yeh BI, Kim YK, Jabbar W, Huang CL (2005) Conformational changes of pore helix coupled to gating of TRPV5 by protons. EMBO J 24:3224–3234

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshida T, Inoue R, Morii T, Takahashi N, Yamamoto S, Hara Y, Tominaga M, Shimizu S, Sato Y, Mori Y (2006) Nitric oxide activates TRP channels by cysteine S-nitrosylation. Nat Chem Biol 2:596–607

    CAS  PubMed  Google Scholar 

  • Zakharian E, Cao C, Rohacs T (2010) Gating of transient receptor potential melastatin 8 (TRPM8) channels activated by cold and chemical agonists in planar lipid bilayers. J Neurosci 30:12526–12534

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zaritsky JJ, Redell JB, Tempel BL, Schwarz TL (2001) The consequences of disrupting cardiac inwardly rectifying K(+) current (I(K1)) as revealed by the targeted deletion of the murine Kir2.1 and Kir2.2 genes. J Physiol 533:697–710

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zeng F, Xu SZ, Jackson PK, McHugh D, Kumar B, Fountain SJ, Beech DJ (2004) Human TRPC5 channel activated by a multiplicity of signals in a single cell. J Physiol 559:739–750

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zhang F, Liu S, Yang F, Zheng J, Wang K (2011) Identification of a tetrameric assembly domain in the C terminus of heat-activated TRPV1 channels. J Biol Chem 286:15308–15316

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zhu X, Chu PB, Peyton M, Birnbaumer L (1995) Molecular cloning of a widely expressed human homologue for the Drosophila trp gene. FEBS Lett 373:193–198

    CAS  PubMed  Google Scholar 

  • Zimmermann K, Lennerz JK, Hein A, Link AS, Kaczmarek JS, Delling M, Uysal S, Pfeifer JD, Riccio A, Clapham DE (2011) Transient receptor potential cation channel, subfamily C, member 5 (TRPC5) is a cold-transducer in the peripheral nervous system. Proc Natl Acad Sci U S A 108:18114–18119

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zurborg S, Yurgionas B, Jira JA, Caspani O, Heppenstall PA (2007) Direct activation of the ion channel TRPA1 by Ca2+. Nat Neurosci 10:277–279

    CAS  PubMed  Google Scholar 

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Acknowledgements

This work was supported by FONDECYT Grants 1110430 and 1150273 (to Latorre R), 1120802 (to González C); ANILLO Grant ACT1104 (to Gonzalez C). CSIC p944, the CSIC International Cooperation Program, U de la R-CINV-UV and the Chilean Conicyt International Cooperation Program (to Ferreira G and González C). The Centro Interdisciplinario de Neurociencia de Valparaíso is a Millennium Institute supported by the Millennium Scientific Initiative of the Chilean Ministry of Economy, Public Works, and Tourism.

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Authors and Affiliations

  1. Departamento de Biofísica, Facultad de Medicina, Universidad de La República, Montevideo, Uruguay

    Gonzalo Ferreira

  2. Facultad de Ciencias, Centro Interdisciplinario de Neurociencia de Valparaíso, Universidad de Valparaiso, Pasaje Harrington 287, Playa Ancha, Valparaíso, Chile

    Natalia Raddatz, Yenisleidy Lorenzo, Carlos González & Ramón Latorre

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  1. Gonzalo Ferreira
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  2. Natalia Raddatz
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  3. Yenisleidy Lorenzo
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  4. Carlos González
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  5. Ramón Latorre
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Correspondence to Ramón Latorre .

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  1. Faculty of Chemistry and Biology, University of Santiago de Chile, Santiago, Chile

    Rodolfo Madrid

  2. Faculty of Science, University of Chile, Santiago, Chile

    Juan Bacigalupo

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Ferreira, G., Raddatz, N., Lorenzo, Y., González, C., Latorre, R. (2015). Biophysical and Molecular Features of Thermosensitive TRP Channels Involved in Sensory Transduction. In: Madrid, R., Bacigalupo, J. (eds) TRP Channels in Sensory Transduction. Springer, Cham. https://doi.org/10.1007/978-3-319-18705-1_1

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