1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Biophysics
  4. Volume 45, 2016
  5. Article

Annual Review of Biophysics

Volume 45, 2016

Allosterism and Structure in Thermally Activated Transient Receptor Potential Channels

Abstract

The molecular sensors that mediate temperature changes in living organisms are a large family of proteins known as thermosensitive transient receptor potential (TRP) ion channels. These membrane proteins are polymodal receptors that can be activated by cold or hot temperatures, depending on the channel subtype, voltage, and ligands. The stimuli sensors are allosterically coupled to a pore domain, increasing the probability of finding the channel in its ion conductive conformation. In this review we first discuss the allosteric coupling between the temperature and voltage sensor modules and the pore domain, and then discuss the thermodynamic foundations of thermo-TRP channel activation. We provide a structural overview of the molecular determinants of temperature sensing. We also posit an anisotropic thermal diffusion model that may explain the large temperature sensitivity of TRP channels. Additionally, we examine the effect of several ligands on TRP channel function and the evidence regarding their mechanisms of action.

Keyword(s): gating models, heat activation pathways, ligand binding, phosphatidylinositol 4,5-bisphosphate, temperature sensor, thermodynamics
Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-062215-011034
2016-07-05
2024-04-24
Loading full text...

Full text loading...

/deliver/fulltext/biophys/45/1/annurev-biophys-062215-011034.html?itemId=/content/journals/10.1146/annurev-biophys-062215-011034&mimeType=html&fmt=ahah

Literature Cited

  1. Andersson DA, Filipovic MR, Gentry C, Eberhardt M, Vastani N. 1.  et al. 2015. Streptozotocin stimulates the ion channel TRPA1 directly: involvement of peroxynitrite. J. Biol. Chem. 290:2415185–96 [Google Scholar]
  2. Ashoor A, Nordman JC, Veltri D, Yang KH, Shuba Y. 2.  et al. 2013. Menthol inhibits 5-HT3 receptor-mediated currents. J. Pharmacol. Exp. Ther. 347:2398–409 [Google Scholar]
  3. Badheka D, Borbiro I, Rohacs T. 3.  2015. Transient receptor potential melastatin 3 is a phosphoinositide-dependent ion channel. J. Gen. Physiol. 146:165–77 [Google Scholar]
  4. Baez D, Raddatz N, Ferreira G, Gonzalez C, Latorre R. 4.  2014. Gating of thermally activated channels. Curr. Top. Membr. 74:51–87 [Google Scholar]
  5. Baker NA.5.  2004. Poisson-Boltzmann methods for biomolecular electrostatics. Methods Enzymol. 383:94–118 [Google Scholar]
  6. Bandell M, Dubin AE, Petrus MJ, Orth A, Mathur J. 6.  et al. 2006. High-throughput random mutagenesis screen reveals TRPM8 residues specifically required for activation by menthol. Nat. Neurosci. 9:4493–500 [Google Scholar]
  7. Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR. 7.  et al. 2004. Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:6849–57 [Google Scholar]
  8. Banzawa N, Saito S, Imagawa T, Kashio M, Takahashi K. 8.  et al. 2014. Molecular basis determining inhibition/activation of nociceptive receptor TRPA1 protein: a single amino acid dictates species-specific actions of the most potent mammalian TRPA1 antagonist. J. Biol. Chem. 289:4631927–39 [Google Scholar]
  9. Bao L, Kaldany C, Holmstrand EC, Cox DH. 9.  2004. Mapping the BKCa channel's “Ca2+ bowl”: side-chains essential for Ca2+ sensing. J. Gen. Physiol. 123:5475–89 [Google Scholar]
  10. Bao L, Rapin AM, Holmstrand EC, Cox DH. 10.  2002. Elimination of the BKCa channel's high-affinity Ca2+ sensitivity. J. Gen. Physiol. 120:2173–89 [Google Scholar]
  11. Bautista DM, Movahed P, Hinman A, Axelsson HE, Sterner O. 11.  et al. 2005. Pungent products from garlic activate the sensory ion channel TRPA1. PNAS 102:3412248–52 [Google Scholar]
  12. Bohlen CJ, Priel A, Zhou S, King D, Siemens J, Julius D. 12.  2010. A bivalent tarantula toxin activates the capsaicin receptor, TRPV1, by targeting the outer pore domain. Cell 141:5834–45 [Google Scholar]
  13. Boukalova S, Marsakova L, Teisinger J, Vlachova V. 13.  2010. Conserved residues within the putative S4-S5 region serve distinct functions among thermosensitive vanilloid transient receptor potential (TRPV) channels. J. Biol. Chem. 285:5341455–62 [Google Scholar]
  14. Bousova K, Jirku M, Bumba L, Bednarova L, Sulc M. 14.  et al. 2015. PIP2 and PIP3 interact with N-terminus region of TRPM4 channel. Biophys. Chem. 205:24–32 [Google Scholar]
  15. Brauchi S, Orio P, Latorre R. 15.  2004. Clues to understanding cold sensation: thermodynamics and electrophysiological analysis of the cold receptor TRPM8. PNAS 101:4315494–99 [Google Scholar]
  16. Brauchi S, Orta G, Mascayano C, Salazar M, Raddatz N. 16.  et al. 2007. Dissection of the components for PIP2 activation and thermosensation in TRP channels. PNAS 104:2410246–51 [Google Scholar]
  17. Burendahl S, Nilsson L. 17.  2012. Computational studies of LXR molecular interactions reveal an allosteric communication pathway. Proteins 80:1294–306 [Google Scholar]
  18. Cao E, Cordero-Morales JF, Liu B, Qin F, Julius D. 18.  2013. TRPV1 channels are intrinsically heat sensitive and negatively regulated by phosphoinositide lipids. Neuron 77:4667–79 [Google Scholar]
  19. Cao E, Liao M, Cheng Y, Julius D. 19.  2013. TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504:7478113–18 [Google Scholar]
  20. Carrasquel-Ursulaez W, Moldenhauer H, Castillo JP, Latorre R, Alvarez O. 20.  2015. Biophysical analysis of thermosensitive TRP channels with a special focus on the cold receptor TRPM8. Temperature 2:188–200 [Google Scholar]
  21. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D. 21.  1997. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389:6653816–24 [Google Scholar]
  22. Chen J, Hackos DH. 22.  2015. TRPA1 as a drug target—promise and challenges. Naunyn Schmiedebergs Arch. Pharmacol. 388:4451–63 [Google Scholar]
  23. Chen J, Kang D, Xu J, Lake M, Hogan JO. 23.  et al. 2013. Species differences and molecular determinant of TRPA1 cold sensitivity. Nat. Commun. 4:2501 [Google Scholar]
  24. Chowdhury S, Chanda B. 24.  2013. Free-energy relationships in ion channels activated by voltage and ligand. J. Gen. Physiol. 141:111–28 [Google Scholar]
  25. Chung MK, Guler AD, Caterina MJ. 25.  2008. TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat. Neurosci. 11:5555–64 [Google Scholar]
  26. Clapham DE, Miller C. 26.  2011. A thermodynamic framework for understanding temperature sensing by transient receptor potential (TRP) channels. PNAS 108:4919492–97 [Google Scholar]
  27. Clapham DE, Montell C, Schultz G, Julius D. 27.  International Union of Pharmacology 2003. International Union of Pharmacology. XLIII. Compendium of voltage-gated ion channels: transient receptor potential channels. Pharmacol. Rev. 55:4591–96 [Google Scholar]
  28. Clapham DE, Runnels LW, Strubing C. 28.  2001. The TRP ion channel family. Nat. Rev. Neurosci. 2:6387–96 [Google Scholar]
  29. Cordero-Morales JF, Gracheva EO, Julius D. 29.  2011. Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli. PNAS 108:46E1184–91 [Google Scholar]
  30. Cui Y, Yang F, Cao X, Yarov-Yarovoy V, Wang K, Zheng J. 30.  2012. Selective disruption of high sensitivity heat activation but not capsaicin activation of TRPV1 channels by pore turret mutations. J. Gen. Physiol. 139:4273–83 [Google Scholar]
  31. Dill KA. 31.  1990. Dominant forces in protein folding. Biochemistry 29:317133–55 [Google Scholar]
  32. Doerner JF, Hatt H, Ramsey IS. 32.  2011. Voltage- and temperature-dependent activation of TRPV3 channels is potentiated by receptor-mediated PI(4,5)P2 hydrolysis. J. Gen. Physiol. 137:3271–88 [Google Scholar]
  33. Doyle DA, Morais Cabral J, Pfuetzner RA, Kuo A, Gulbis JM. 33.  et al. 1998. The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:536069–77 [Google Scholar]
  34. Dutzler R, Campbell EB, Cadene M, Chait BT, MacKinnon R. 34.  2002. X-ray structure of a ClC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity. Nature 415:6869287–94 [Google Scholar]
  35. Elokely K, Velisetty P, Delemotte L, Palovcak E, Klein ML. 35.  et al. 2016. Understanding TRPV1 activation by ligands: insights from the binding modes of capsaicin and resiniferatoxin. PNAS 113:2E137–45 [Google Scholar]
  36. Estacion M, Sinkins WG, Schilling WP. 36.  2001. Regulation of Drosophila transient receptor potential-like (TrpL) channels by phospholipase C-dependent mechanisms. J. Physiol. 530:Pt. 11–19 [Google Scholar]
  37. Fenwick RB, Orellana L, Esteban-Martín S, Orozco M, Salvatella X. 37.  2014. Correlated motions are a fundamental property of β-sheets. Nat. Commun. 5:4070 [Google Scholar]
  38. Fernández JA, Skryma R, Bidaux G, Magleby KL, Scholfield CN. 38.  et al. 2011. Voltage- and cold-dependent gating of single TRPM8 ion channels. J. Gen. Physiol. 137:2173–95 [Google Scholar]
  39. Ferrer-Montiel A, García-Martínez C, Morenilla-Palao C, García-Sanz N, Fernández-Carvajal A. 39.  et al. 2004. Molecular architecture of the vanilloid receptor. Insights for drug design. Eur. J. Biochem. 271:101820–26 [Google Scholar]
  40. Fujita F, Uchida K, Takaishi M, Sokabe T, Tominaga M. 40.  2013. Ambient temperature affects the temperature threshold for TRPM8 activation through interaction of phosphatidylinositol 4,5-bisphosphate. J. Neurosci. 33:146154–59 [Google Scholar]
  41. Garcia-Elias A, Mrkonjic S, Pardo-Pastor C, Inada H, Hellmich UA. 41.  et al. 2013. Phosphatidylinositol-4,5-biphosphate-dependent rearrangement of TRPV4 cytosolic tails enables channel activation by physiological stimuli. PNAS 110:239553–58 [Google Scholar]
  42. Gavva NR, Klionsky L, Qu Y, Shi L, Tamir R. 42.  et al. 2004. Molecular determinants of vanilloid sensitivity in TRPV1. J. Biol. Chem. 279:1920283–95 [Google Scholar]
  43. Gianni S, Walma T, Arcovito A, Calosci N, Bellelli A. 43.  et al. 2006. Demonstration of long-range interactions in a PDZ domain by NMR, kinetics, and protein engineering. Structure 14:121801–9 [Google Scholar]
  44. Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G. 44.  et al. 2010. Molecular basis of infrared detection by snakes. Nature 464:72911006–11 [Google Scholar]
  45. Grandl J, Kim SE, Uzzell V, Bursulaya B, Petrus M. 45.  et al. 2010. Temperature-induced opening of TRPV1 ion channel is stabilized by the pore domain. Nat. Neurosci. 13:6708–14 [Google Scholar]
  46. Gregorio-Teruel L, Valente P, González-Ros JM, Fernández-Ballester G, Ferrer-Montiel A. 46.  2014. Mutation of I696 and W697 in the TRP box of vanilloid receptor subtype I modulates allosteric channel activation. J. Gen. Physiol. 143:3361–75 [Google Scholar]
  47. Gregorio-Teruel L, Valente P, Liu B, Fernández-Ballester G, Qin F, Ferrer-Montiel A. 47.  2015. The integrity of the TRP domain is pivotal for correct TRPV1 channel gating. Biophys. J. 109:3529–41 [Google Scholar]
  48. Grosman C, Zhou M, Auerbach A. 48.  2000. Mapping the conformational wave of acetylcholine receptor channel gating. Nature 403:6771773–76 [Google Scholar]
  49. Hinman A, Chuang HH, Bautista DM, Julius D. 49.  2006. TRP channel activation by reversible covalent modification. PNAS 103:5119564–68 [Google Scholar]
  50. Hite RK, Yuan P, Li Z, Hsuing Y, Walz T, MacKinnon R. 50.  2015. Cryo-electron microscopy structure of the Slo2.2 Na+-activated K+ channel. Nature 527:7577198–203 [Google Scholar]
  51. Holendova B, Grycova L, Jirku M, Teisinger J. 51.  2012. PtdIns(4,5)P2 interacts with CaM binding domains on TRPM3 N-terminus. Channels 6:6479–82 [Google Scholar]
  52. Horrigan FT, Aldrich RW. 52.  1999. Allosteric voltage gating of potassium channels II: mSlo channel gating charge movement in the absence of Ca2+. J. Gen. Physiol. 114:2305–6 [Google Scholar]
  53. Horrigan FT, Aldrich RW. 53.  2002. Coupling between voltage sensor activation, Ca2+ binding and channel opening in large conductance (BK) potassium channels. J. Gen. Physiol. 120:3267–305 [Google Scholar]
  54. Horrigan FT, Cui J, Aldrich RW. 54.  1999. Allosteric voltage gating of potassium channels I: mSlo ionic currents in the absence of Ca2+. J. Gen. Physiol. 114:2277–304 [Google Scholar]
  55. Humphrey W, Dalke A, Schulten K. 55.  1996. VMD: visual molecular dynamics. J. Mol. Graph. 14:127–2833–38 [Google Scholar]
  56. Jabba S, Goyal R, Sosa-Pagan JO, Moldenhauer H, Wu J. 56.  et al. 2014. Directionality of temperature activation in mouse TRPA1 ion channel can be inverted by single-point mutations in ankyrin repeat six. Neuron 82:51017–31 [Google Scholar]
  57. Jiang Y, Lee A, Chen J, Cadene M, Chait BT, MacKinnon R.57.  2002. Crystal structure and mechanism of a calcium-gated potassium channel. Nature 417:6888515–22 [Google Scholar]
  58. Jiang Y, Lee A, Chen J, Ruta V, Cadene M. 58.  et al. 2003. X-ray structure of a voltage-dependent K+ channel. Nature 423:693533–41 [Google Scholar]
  59. Jiang Y, Pico A, Cadene M, Chait BT, MacKinnon R. 59.  2001. Structure of the RCK domain from the E. coli K+ channel and demonstration of its presence in the human BK channel. Neuron 29:3593–601 [Google Scholar]
  60. Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM. 60.  et al. 2004. Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:6971260–65 [Google Scholar]
  61. Jordt SE, Julius D. 61.  2002. Molecular basis for species-specific sensitivity to “hot” chili peppers. Cell 108:3421–30 [Google Scholar]
  62. Julius D.62.  2013. TRP channels and pain. Annu. Rev. Cell Dev. Biol. 29:355–84 [Google Scholar]
  63. Kang K, Panzano VC, Chang EC, Ni L, Dainis AM. 63.  et al. 2012. Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481:737976–80 [Google Scholar]
  64. Karashima Y, Prenen J, Meseguer V, Owsianik G, Voets T, Nilius B. 64.  2008. Modulation of the transient receptor potential channel TRPA1 by phosphatidylinositol 4,5-biphosphate manipulators. Pflüg. Arch. 457:177–89 [Google Scholar]
  65. Karashima Y, Talavera K, Everaerts W, Janssens A, Kwan KY. 65.  et al. 2009. TRPA1 acts as a cold sensor in vitro and in vivo. PNAS 106:41273–78 [Google Scholar]
  66. Kim D, Cavanaugh EJ. 66.  2007. Requirement of a soluble intracellular factor for activation of transient receptor potential A1 by pungent chemicals: role of inorganic polyphosphates. J. Neurosci. 27:266500–9 [Google Scholar]
  67. Kim D, Cavanaugh EJ, Simkin D. 67.  2008. Inhibition of transient receptor potential A1 channel by phosphatidylinositol-4,5-bisphosphate. Am. J. Physiol. Cell Physiol. 295:1C92–99 [Google Scholar]
  68. Kim SE, Patapoutian A, Grandl J. 68.  2013. Single residues in the outer pore of TRPV1 and TRPV3 have temperature-dependent conformations. PLOS ONE 8:3e59593 [Google Scholar]
  69. Klein RM, Ufret-Vincenty CA, Hua L, Gordon SE. 69.  2008. Determinants of molecular specificity in phosphoinositide regulation. Phosphatidylinositol (4,5)-bisphosphate (PI(4,5)P2) is the endogenous lipid regulating TRPV1. J. Biol. Chem. 283:3826208–16 [Google Scholar]
  70. Klement G, Eisele L, Malinowsky D, Nolting A, Svensson M. 70.  et al. 2013. Characterization of a ligand binding site in the human transient receptor potential ankyrin 1 pore. Biophys. J. 104:4798–806 [Google Scholar]
  71. Kozak JA, Matsushita M, Nairn AC, Cahalan MD. 71.  2005. Charge screening by internal pH and polyvalent cations as a mechanism for activation, inhibition, and rundown of TRPM7/MIC channels. J. Gen. Physiol. 126:5499–514 [Google Scholar]
  72. Kwon Y, Hofmann T, Montell C. 72.  2007. Integration of phosphoinositide- and calmodulin-mediated regulation of TRPC6. Mol. Cell 25:4491–503 [Google Scholar]
  73. Latorre R, Brauchi S, Orta G, Zaelzer C, Vargas G. 73.  2007. ThermoTRP channels as modular proteins with allosteric gating. Cell Calcium 42:4–5427–38 [Google Scholar]
  74. Latorre R, Zaelzer C, Brauchi S. 74.  2009. Structure-functional intimacies of transient receptor potential channels. Q. Rev. Biophys. 42:3201–46 [Google Scholar]
  75. Leitner DM.75.  2008. Energy flow in proteins. Annu. Rev. Phys. Chem. 59:233–59 [Google Scholar]
  76. Lewandowski JR, Halse ME, Blackledge M, Emsley L. 76.  2015. Protein dynamics. Direct observation of hierarchical protein dynamics. Science 348:6234578–81 [Google Scholar]
  77. Liao M, Cao E, Julius D, Cheng Y. 77.  2013. Structure of the TRPV1 ion channel determined by electron cryo-microscopy. Nature 504:7478107–12 [Google Scholar]
  78. Liao M, Cao E, Julius D, Cheng Y. 78.  2014. Single particle electron cryo-microscopy of a mammalian ion channel. Curr. Opin. Struct. Biol. 27:1–7 [Google Scholar]
  79. Lishko PV, Procko E, Jin X, Phelps CB, Gaudet R. 79.  2007. The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity. Neuron 54:6905–18 [Google Scholar]
  80. Liu B, Hui K, Qin F. 80.  2003. Thermodynamics of heat activation of single capsaicin ion channels VR1. Biophys. J. 85:52988–3006 [Google Scholar]
  81. Liu B, Yao J, Zhu MX, Qin F. 81.  2011. Hysteresis of gating underlines sensitization of TRPV3 channels. J. Gen. Physiol. 138:5509–20 [Google Scholar]
  82. Liu J, Tawa GJ, Wallqvist A. 82.  2013. Identifying cytochrome p450 functional networks and their allosteric regulatory elements. PLOS ONE 8:12e81980 [Google Scholar]
  83. Long SB, Campbell EB, Mackinnon R. 83.  2005. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science 309:5736897–903 [Google Scholar]
  84. Long SB, Tao X, Campbell EB, MacKinnon R. 84.  2007. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature 450:7168376–82 [Google Scholar]
  85. Lukacs V, Rives JM, Sun X, Zakharian E, Rohacs T. 85.  2013. Promiscuous activation of transient receptor potential vanilloid 1 (TRPV1) channels by negatively charged intracellular lipids: the key role of endogenous phosphoinositides in maintaining channel activity. J. Biol. Chem. 288:4935003–13 [Google Scholar]
  86. Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG. 86.  et al. 2007. Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445:7127541–45 [Google Scholar]
  87. Mandel AM, Akke M, Palmer AG 3rd. 87.  1996. Dynamics of ribonuclease H: temperature dependence of motions on multiple time scales. Biochemistry 35:5016009–23 [Google Scholar]
  88. Matta JA, Ahern GP. 88.  2007. Voltage is a partial activator of rat thermosensitive TRP channels. J. Physiol. 585:Pt. 2469–82 [Google Scholar]
  89. McGaraughty S, Chu KL, Perner RJ, Didomenico S, Kort ME, Kym PR. 89.  2010. TRPA1 modulation of spontaneous and mechanically evoked firing of spinal neurons in uninjured, osteoarthritic, and inflamed rats. Mol. Pain 6:14 [Google Scholar]
  90. McIntyre P, McLatchie LM, Chambers A, Phillips E, Clarke M. 90.  et al. 2001. Pharmacological differences between the human and rat vanilloid receptor 1 (VR1). Br. J. Pharmacol. 132:51084–94 [Google Scholar]
  91. McKemy DD, Neuhausser WM, Julius D. 91.  2002. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 416:687652–58 [Google Scholar]
  92. McNamara CR, Mandel-Brehm J, Bautista DM, Siemens J, Deranian KL. 92.  et al. 2007. TRPA1 mediates formalin-induced pain. PNAS 104:3313525–30 [Google Scholar]
  93. Mercado J, Gordon-Shaag A, Zagotta WN, Gordon SE. 93.  2010. Ca2+-dependent desensitization of TRPV2 channels is mediated by hydrolysis of phosphatidylinositol 4,5-bisphosphate. J. Neurosci. 30:4013338–47 [Google Scholar]
  94. Miño G, Barriga R, Gutierrez G. 94.  2014. Hydrogen bonds and heat diffusion in α-helices: a computational study. J. Phys. Chem. B 118:3410025–34 [Google Scholar]
  95. Miño-Galaz GA.95.  2015. Allosteric communication pathways and thermal rectification in PDZ-2 protein: a computational study. J. Phys. Chem. B 119:206179–89 [Google Scholar]
  96. Miranda P, Contreras JE, Plested AJ, Sigworth FJ, Holmgren M, Giraldez T. 96.  2013. State-dependent FRET reports calcium- and voltage-dependent gating-ring motions in BK channels. PNAS 110:135217–22 [Google Scholar]
  97. Moldenhauer H, Latorre R, Grandl J. 97.  2014. The pore-domain of TRPA1 mediates the inhibitory effect of the antagonist 6-methyl-5-(2-(trifluoromethyl)phenyl)-1H-indazole. PLOS ONE 9:9e106776 [Google Scholar]
  98. Montell C.98.  2001. Physiology, phylogeny, and functions of the TRP superfamily of cation channels. Sci. STKE 2001:90re1 [Google Scholar]
  99. Montell C.99.  2005. The TRP superfamily of cation channels. Sci. STKE 2005:272re3 [Google Scholar]
  100. Moparthi L, Survery S, Kreir M, Simonsen C, Kjellbom P. 100.  et al. 2014. Human TRPA1 is intrinsically cold- and chemosensitive with and without its N-terminal ankyrin repeat domain. PNAS 111:4716901–6 [Google Scholar]
  101. Myers BR, Sigal YM, Julius D. 101.  2009. Evolution of thermal response properties in a cold-activated TRP channel. PLOS ONE 4:5e5741 [Google Scholar]
  102. Nakatsuka K, Gupta R, Saito S, Banzawa N, Takahashi K. 102.  et al. 2013. Identification of molecular determinants for a potent mammalian TRPA1 antagonist by utilizing species differences. J. Mol. Neurosci. 51:3754–62 [Google Scholar]
  103. Nilius B, Mahieu F, Prenen J, Janssens A, Owsianik G. 103.  et al. 2006. The Ca2+-activated cation channel TRPM4 is regulated by phosphatidylinositol 4,5-biphosphate. EMBO J. 25:3467–78 [Google Scholar]
  104. Niu X, Qian X, Magleby KL. 104.  2004. Linker-gating ring complex as passive spring and Ca2+-dependent machine for a voltage- and Ca2+-activated potassium channel. Neuron 42:5745–56 [Google Scholar]
  105. Paulsen CE, Armache JP, Gao Y, Cheng Y, Julius D. 105.  2015. Structure of the TRPA1 ion channel suggests regulatory mechanisms. Nature 520:7548511–17 [Google Scholar]
  106. Pedretti A, Marconi C, Bettinelli I, Vistoli G. 106.  2009. Comparative modeling of the quaternary structure for the human TRPM8 channel and analysis of its binding features. Biochim. Biophys. Acta 1788:5973–82 [Google Scholar]
  107. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA. 107.  et al. 2002. A TRP channel that senses cold stimuli and menthol. Cell 108:5705–15 [Google Scholar]
  108. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ. 108.  et al. 2002. A heat-sensitive TRP channel expressed in keratinocytes. Science 296:55752046–49 [Google Scholar]
  109. Petrus M, Peier AM, Bandell M, Hwang SW, Huynh T. 109.  et al. 2007. A role of TRPA1 in mechanical hyperalgesia is revealed by pharmacological inhibition. Mol. Pain 3:40 [Google Scholar]
  110. Phillips E, Reeve A, Bevan S, McIntyre P. 110.  2004. Identification of species-specific determinants of the action of the antagonist capsazepine and the agonist PPAHV on TRPV1. J. Biol. Chem. 279:1717165–72 [Google Scholar]
  111. Pirovano W, Feenstra KA, Heringa J. 111.  2008. The meaning of alignment: lessons from structural diversity. BMC Bioinform. 9:556 [Google Scholar]
  112. Poblete H, Oyarzún I, Olivero P, Comer J, Zuñiga M. 112.  et al. 2015. Molecular determinants of phosphatidylinositol 4,5-bisphosphate (PI(4,5)P2) binding to transient receptor potential V1 (TRPV1) channels. J. Biol. Chem. 290:42086–98 [Google Scholar]
  113. Prabhu NV, Sharp KA. 113.  2005. Heat capacity in proteins. Annu. Rev. Phys. Chem. 56:521–48 [Google Scholar]
  114. Prescott ED, Julius D. 114.  2003. A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity. Science 300:56231284–88 [Google Scholar]
  115. Privalov PL.115.  1990. Cold denaturation of proteins. Crit. Rev. Biochem. Mol. Biol. 25:4281–305 [Google Scholar]
  116. Privalov PL, Gill SJ. 116.  1988. Stability of protein structure and hydrophobic interaction. Adv. Protein Chem. 39:191–234 [Google Scholar]
  117. Qin F.117.  2014. Temperature sensing by thermal TRP channels: thermodynamics basis and molecular insights. Curr. Top. Membr. 74:19–50 [Google Scholar]
  118. Raddatz N, Castillo JP, Gonzalez C, Alvarez O, Latorre R. 118.  2014. Temperature and voltage coupling to channel opening in transient receptor potential melastatin 8 (TRPM8). J. Biol. Chem. 289:5135438–54 [Google Scholar]
  119. Ramsey IS, Delling M, Clapham DE. 119.  2006. An introduction to TRP channels. Annu. Rev. Physiol. 68:619–47 [Google Scholar]
  120. Ribeiro AA, Ortiz V. 120.  2015. Energy propagation and network energetic coupling in proteins. J. Phys. Chem. B 119:51835–46 [Google Scholar]
  121. Rohacs T, Lopes CM, Michailidis I, Logothetis DE. 121.  2005. PI(4,5)P2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat. Neurosci. 8:5626–34 [Google Scholar]
  122. Rohacs T, Thyagarajan B, Lukacs V. 122.  2008. Phospholipase C mediated modulation of TRPV1 channels. Mol. Neurobiol. 37:2–3153–63 [Google Scholar]
  123. Rothberg BS, Magleby KL. 123.  2000. Voltage and Ca2+ activation of single large-conductance Ca2+-activated K+ channels described by a two-tiered allosteric gating mechanism. J. Gen. Physiol. 116:175–99 [Google Scholar]
  124. Runnels LW, Yue L, Clapham DE. 124.  2002. The TRPM7 channel is inactivated by PIP2 hydrolysis. Nat. Cell Biol. 4:5329–36 [Google Scholar]
  125. Saito S, Fukuta N, Shingai R, Tominaga M. 125.  2011. Evolution of vertebrate transient receptor potential vanilloid 3 channels: opposite temperature sensitivity between mammals and western clawed frogs. PLOS Genet. 7:4e1002041 [Google Scholar]
  126. Salazar H, Jara-Oseguera A, Hernández-García E, Llorente I, Arias-Olguín II. 126.  et al. 2009. Structural determinants of gating in the TRPV1 channel. Nat. Struct. Mol. Biol. 16:7704–10 [Google Scholar]
  127. Savidge J, Davis C, Shah K, Colley S, Phillips E. 127.  et al. 2002. Cloning and functional characterization of the guinea pig vanilloid receptor 1. Neuropharmacology 43:3450–56 [Google Scholar]
  128. Schreiber M, Salkoff L. 128.  1997. A novel calcium-sensing domain in the BK channel. Biophys. J. 73:31355–63 [Google Scholar]
  129. Stein AT, Ufret-Vincenty CA, Hua L, Santana LF, Gordon SE. 129.  2006. Phosphoinositide 3-kinase binds to TRPV1 and mediates NGF-stimulated TRPV1 trafficking to the plasma membrane. J. Gen. Physiol. 128:5509–22 [Google Scholar]
  130. Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J. 130.  et al. 2003. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:6819–29 [Google Scholar]
  131. Suh BC, Hille B. 131.  2008. PIP2 is a necessary cofactor for ion channel function: how and why?. Annu. Rev. Biophys. 37:175–95 [Google Scholar]
  132. Sun S, Chandler D, Dinner AR, Oster G. 132.  2003. Elastic energy storage in β-sheets with application to F1-ATPase. Eur. Biophys. J. 32:8676–83 [Google Scholar]
  133. Sutton KG, Garrett EM, Rutter AR, Bonnert TP, Jarolimek W, Seabrook GR. 133.  2005. Functional characterisation of the S512Y mutant vanilloid human TRPV1 receptor. Br. J. Pharmacol. 146:5702–11 [Google Scholar]
  134. Taberner FJ, Fernández-Ballester G, Fernández-Carvajal A, Ferrer-Montiel A. 134.  2015. TRP channels interaction with lipids and its implications in disease. Biochim. Biophys. Acta 1848:91818–27 [Google Scholar]
  135. Taberner FJ, López-Córdoba A, Fernández-Ballester G, Korchev Y, Ferrer-Montiel A. 135.  2014. The region adjacent to the C-end of the inner gate in transient receptor potential melastatin 8 (TRPM8) channels plays a central role in allosteric channel activation. J. Biol. Chem. 289:4128579–94 [Google Scholar]
  136. Takahashi N, Hamada-Nakahara S, Itoh Y, Takemura K, Shimada A. 136.  et al. 2014. TRPV4 channel activity is modulated by direct interaction of the ankyrin domain to PI(4,5)P2. Nat. Commun. 5:4994 [Google Scholar]
  137. Talavera K, Yasumatsu K, Voets T, Droogmans G, Shigemura N. 137.  et al. 2005. Heat activation of TRPM5 underlies thermal sensitivity of sweet taste. Nature 438:70701022–25 [Google Scholar]
  138. Thyagarajan B, Lukacs V, Rohacs T. 138.  2008. Hydrolysis of phosphatidylinositol 4,5-bisphosphate mediates calcium-induced inactivation of TRPV6 channels. J. Biol. Chem. 283:2214980–87 [Google Scholar]
  139. Ufret-Vincenty CA, Klein RM, Hua L, Angueyra J, Gordon SE. 139.  2011. Localization of the PIP2 sensor of TRPV1 ion channels. J. Biol. Chem. 286:119688–98 [Google Scholar]
  140. Uysal S, Cuello LG, Cortes DM, Koide S, Kossiakoff AA, Perozo E. 140.  2011. Mechanism of activation gating in the full-length KcsA K+ channel. PNAS 108:2911896–99 [Google Scholar]
  141. Vlachova V, Teisinger J, Susankova K, Lyfenko A, Ettrich R, Vyklicky L. 141.  2003. Functional role of C-terminal cytoplasmic tail of rat vanilloid receptor 1. J. Neurosci. 23:41340–50 [Google Scholar]
  142. Voets T.142.  2012. Quantifying and modeling the temperature-dependent gating of TRP channels. Rev. Physiol. Biochem. Pharmacol. 162:91–119 [Google Scholar]
  143. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, Nilius B. 143.  2004. The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430:7001748–54 [Google Scholar]
  144. Voets T, Owsianik G, Janssens A, Talavera K, Nilius B. 144.  2007. TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat. Chem. Biol. 3:3174–82 [Google Scholar]
  145. Voets T, Owsianik G, Nilius B. 145.  2007. Trpm8. Handb. Exp. Pharmacol. 179:329–44 [Google Scholar]
  146. Vriens J, Nilius B, Voets T. 146.  2014. Peripheral thermosensation in mammals. Nat. Rev. Neurosci. 15:9573–89 [Google Scholar]
  147. Wang H, Schupp M, Zurborg S, Heppenstall PA. 147.  2013. Residues in the pore region of Drosophila transient receptor potential A1 dictate sensitivity to thermal stimuli. J. Physiol. 591:1185–201 [Google Scholar]
  148. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ. 148.  2009. Jalview Version 2—a multiple sequence alignment editor and analysis workbench. Bioinformatics 25:91189–91 [Google Scholar]
  149. Wu Y, Yang Y, Jiang Y. 149.  2010. Structure of the gating ring from the human large-conductance Ca2+-gated K+ channel. Nature 466:7304393–97 [Google Scholar]
  150. Xia XM, Zeng X, Lingle CJ. 150.  2002. Multiple regulatory sites in large-conductance calcium-activated potassium channels. Nature 418:6900880–84 [Google Scholar]
  151. Xie J, Sun B, Du J, Yang W, Chen HC. 151.  et al. 2011. Phosphatidylinositol 4,5-bisphosphate (PIP2) controls magnesium gatekeeper TRPM6 activity. Sci. Rep. 1:146 [Google Scholar]
  152. Yang F, Cui Y, Wang K, Zheng J. 152.  2010. Thermosensitive TRP channel pore turret is part of the temperature activation pathway. PNAS 107:157083–88 [Google Scholar]
  153. Yang F, Xiao X, Cheng W, Yang W, Yu P. 153.  et al. 2015. Structural mechanism underlying capsaicin binding and activation of the TRPV1 ion channel. Nat. Chem. Biol. 11:7518–24 [Google Scholar]
  154. Yao J, Liu B, Qin F. 154.  2010. Kinetic and energetic analysis of thermally activated TRPV1 channels. Biophys. J. 99:61743–53 [Google Scholar]
  155. Yao J, Liu B, Qin F. 155.  2010. Pore turret of thermal TRP channels is not essential for temperature sensing. PNAS 107:32E125–27 [Google Scholar]
  156. Yao J, Liu B, Qin F. 156.  2011. Modular thermal sensors in temperature-gated transient receptor potential (TRP) channels. PNAS 108:2711109–14 [Google Scholar]
  157. Yuan P, Leonetti MD, Hsiung Y, MacKinnon R. 157.  2012. Open structure of the Ca2+ gating ring in the high-conductance Ca2+-activated K+ channel. Nature 481:737994–97 [Google Scholar]
  158. Yusifov T, Javaherian AD, Pantazis A, Gandhi CS, Olcese R. 158.  2010. The RCK1 domain of the human BKCa channel transduces Ca2+ binding into structural rearrangements. J. Gen. Physiol. 136:2189–202 [Google Scholar]
  159. Yusifov T, Savalli N, Gandhi CS, Ottolia M, Olcese R. 159.  2008. The RCK2 domain of the human BKCa channel is a calcium sensor. PNAS 105:1376–81 [Google Scholar]
  160. Zhang X, Huang J, McNaughton PA. 160.  2005. NGF rapidly increases membrane expression of TRPV1 heat-gated ion channels. EMBO J. 24:244211–23 [Google Scholar]
  161. Zheng J, Ma L. 161.  2014. Structure and function of the thermoTRP channel pore. Curr. Top. Membr. 74:233–57 [Google Scholar]
  162. Zhou Y, Morais-Cabral JH, Kaufman A, MacKinnon R. 162.  2001. Chemistry of ion coordination and hydration revealed by a K+ channel-Fab complex at 2.0 Å resolution. Nature 414:685943–48 [Google Scholar]
  163. Zhu MX.163.  2005. Multiple roles of calmodulin and other Ca2+-binding proteins in the functional regulation of TRP channels. Pflüg. Arch. 451:1105–15 [Google Scholar]
  164. Zimmermann K, Lennerz JK, Hein A, Link AS, Kaczmarek JS. 164.  et al. 2011. Transient receptor potential cation channel, subfamily C, member 5 (TRPC5) is a cold-transducer in the peripheral nervous system. PNAS 108:4418114–19 [Google Scholar]
/content/journals/10.1146/annurev-biophys-062215-011034
Loading
Allosterism and Structure in Thermally Activated Transient Receptor Potential Channels
Annual Review of Biophysics 45, 371 (2016); https://doi.org/10.1146/annurev-biophys-062215-011034
/content/journals/10.1146/annurev-biophys-062215-011034
/content/journals/10.1146/annurev-biophys-062215-011034
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error