Abstract
Membrane voltage, ligand binding, mechanical force and temperature can all induce conformational changes that open ion channel pores. A key question in understanding ion channel function is how the protein domains involved in sensing stimuli (sensors) communicate with the pore to gate its opening and closing. TRP channels are considered six-transmembrane cation-permeable channels, distant relatives of voltage-gated potassium channels (Kv), which are known to be activated by membrane depolarization. Understanding the molecular nature of thermo-TRP channel gating offers a fair challenge to biophysicists. This chapter will summarize our present knowledge on the effect of voltage and temperature during thermo-TRP channel activation.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Notes
- 1.
Change in enzyme activity over a change of 10ºC.
References
Ramsey IS, Delling M, Clapham DE (2006) An introduction to TRP channels. Annu Rev Physiol 68:619–647
Latorre R, Brauchi S, Orta G, Zaelzer C, Vargas G (2007) Thermo TRP channels as modular proteins with allosteric gating. Cell Calcium 42:427–438
Latorre R, Zaelzer C, Brauchi S (2009) Structure-functional intimacies of transient receptor potential channels. Q Rev Biophys 42:201–246
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
Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and itsapplication to conduction and excitation in nerve. J Physiol 117:500–544
Bezanilla F (2000) The voltage sensor in voltage-dependent ion channels. Physiol Rev 80:555–592
Long SB, Tao X, Campbell EB, MacKinnon R (2007) Atomic structure of a voltage-dependent k+ channel in a lipid membrane-like environment. Nature 450:376–382
Noda M, Shimizu S, Tanabe T, Takai T, Kayano T, Ikeda T, Takahashi H, Nakayama H, Kanaoka Y, Minamino N et al (1984) Primary structure of electrophorus electricus sodium channel deduced from cDNA sequence. Nature 312:121–127
Seoh SA, Sigg D, Papazian DM, Bezanilla F (1996) Voltage-sensing residues in the S2 and S4 segments of the shaker k+ channel. Neuron 16:1159–1167
Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, Mackinnon R (2003) X-ray structure of a voltage-dependent k channel. Nature 423:33–41
Swartz KJ (2008) Sensing voltage across lipid membranes. Nature 456:891–897
Murata Y, Iwasaki H, Sasaki M, Inaba K, Okamura Y (2005) Phosphoinositide phosphatase activity coupled to an intrinsic voltage sensor. Nature 435:1239–1243
Sasaki M, Takagi M, Okamura Y (2006) A voltage sensor-domain protein is a voltage-gated proton channel. Science 312:589–592
Ramsey IS, Moran MM, Chong JA, Clapham DE (2006) A voltage-gated proton-selective channel lacking the pore domain. Nature 440:1213–1216
Armstrong CM, Bezanilla F (1973) Currents related to movement of the gating particles of the sodium channels. Nature 242:459–461
Schneider MF, Chandler WK (1973) Voltage dependent charge movement of skeletal muscle: a possible step in excitation-contraction coupling. Nature 242:244–246
Schoppa NE, McCormack K, Tanouye MA, Sigworth FJ (1992) The size of gating charge in wild-type and mutant shaker potassium channels. Science (80) 255:1712–1715
Sigg D, Bezanilla F (1997) Total charge movement per channel. the relation between gating charge displacement and the voltage sensitivity of activation. J Gen Physiol 109: 27–39
Aggarwal SK, MacKinnon R (1996) Contribution of the S4 segment to gating charge in the shaker K+ channel. Neuron 16:1169–1177
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
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
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 USA 106:1273–1278
Latorre R, Vargas G, Orta G, Brauchi S (2007) Voltage and temperature gating of thermoTRP channels. In: Liedtke W, Heller S (eds) TRP ion channels function in sensory transduction and cellular signaling cascades. CRC Taylor & Francis, London, pp 287–302
Gaudet R (2008) P channels entering the structural era. J Physiol 586:3565–3575
Moiseenkova-bell VY, Stanciu LA, Serysheva II, Tobe BJ, Wensel TG (2008) Structure of TRPV1 channel revealed by electron cryomicroscopy. Proc Natl Acad Sci USA 105:7451–7455
Almers W (1978) Gating currents and charge movements in excitable membranes. Rev Physiol Biochem Pharmacol 82:96–190
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
Liu B, Hui K, Qin F (2003) Thermodynamics of heat activation of single capsaicin ion channels vr1. Biophys J 85:2988–3006
Iggo A (1969) Cutaneous thermoreceptors in primates and sub-primates. J Physiol 200: 403–430
Lecar H, Ehrenstein G, Latorre R (1975) Mechanism for channel gating in excitable bilayers. Ann NY Acad Sci 264:304–313
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 USA 107:7083–7088
Privalov PL (1989) Thermodynamic problems of protein structure. Annu Rev Biophys Chem 18:47–69
Privalov PL. Thermodynamics of protein folding. 1997; 447–474
Gursky O, Atkinson D (1996) High- and low-temperature unfolding of human high-density apolipoprotein a-2. Protein Sci 5:1874–1882
Privalov PL, Griko YV, Venyaminov S, Kutyshenko VP (1986) Cold denaturation of myoglobin. J Mol Biol 190:487–498
Griko YV, Venyaminov S, Privalov PL (1989) Heat and cold denaturation of phosphoglycerate kinase (interaction of domains). FEBS Lett 244:276–278
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
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
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 6:708–714
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 USA 104:10246–10251
Yellen G (1998) The moving parts of voltage-gated ion channels. Quart Rev Biophys 31:239–295
Matta JA, Ahern GP (2007) Voltage is a partial activator of rat thermosensitive TRP channels. J Physiol 585:469–482
Altomare C, Bucchi A, Camatini E, Baruscotti M, Viscomi C, Moroni A, DiFrancesco D (2001) Integrated allosteric model of voltage gating of HCN channels. J Gen Physiol 117:519–532
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
Horrigan FT, Cui J, Aldrich RW (1999) Allosteric voltage gating of potassium channels i. mslo ionic currents in the absence of Ca2+. J Gen Physiol 114:277–304
Colquhoun D, Hawkes AG (1981) On the stochastic properties of single ion channels. Proc R Soc Lond B Biol Sci 211:205–235
Lu Z, Klem AM, Ramu Y (2002) Coupling between voltage sensors and activation gate in voltage-gated K+ channels. J Gen Physiol 120:663–676
Yao J, Liu B, Qin F (2010) Pore turret of thermal TRP channels is not essential for temperature sensing. Proc Natl Acad Sci USA 107(32):E125
Yang F, Ciu Y, Wang K, Zheng J (2010) Reply to Yao et al.: is the pore turret just thermoTRP channels’ appendix? Proc Natl Acad Sci USA 107(32):E126–E127
Acknowledgments
SB work is funded by FONDECYT grant 11070190. PO work is funded by FONDECYT 11090308 and DIPUV 51/2007 (U. de Valparaiso) grants. We thank Dr. H. Kurata for his critical reading of the manuscript.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2011 Springer Science+Business Media B.V.
About this chapter
Cite this chapter
Brauchi, S., Orio, P. (2011). Voltage Sensing in Thermo-TRP Channels. In: Islam, M. (eds) Transient Receptor Potential Channels. Advances in Experimental Medicine and Biology, vol 704. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-0265-3_28
Download citation
DOI: https://doi.org/10.1007/978-94-007-0265-3_28
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-007-0264-6
Online ISBN: 978-94-007-0265-3
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)