Global versus local mechanisms of temperature sensing in ion channels

Invited Review

Abstract

Ion channels turn diverse types of inputs, ranging from neurotransmitters to physical forces, into electrical signals. Channel responses to ligands generally rely on binding to discrete sensor domains that are coupled to the portion of the channel responsible for ion permeation. By contrast, sensing physical cues such as voltage, pressure, and temperature arises from more varied mechanisms. Voltage is commonly sensed by a local, domain-based strategy, whereas the predominant paradigm for pressure sensing employs a global response in channel structure to membrane tension changes. Temperature sensing has been the most challenging response to understand and whether discrete sensor domains exist for pressure and temperature has been the subject of much investigation and debate. Recent exciting advances have uncovered discrete sensor modules for pressure and temperature in force-sensitive and thermal-sensitive ion channels, respectively. In particular, characterization of bacterial voltage-gated sodium channel (BacNaV) thermal responses has identified a coiled-coil thermosensor that controls channel function through a temperature-dependent unfolding event. This coiled-coil thermosensor blueprint recurs in other temperature sensitive ion channels and thermosensitive proteins. Together with the identification of ion channel pressure sensing domains, these examples demonstrate that “local” domain-based solutions for sensing force and temperature exist and highlight the diversity of both global and local strategies that channels use to sense physical inputs. The modular nature of these newly discovered physical signal sensors provides opportunities to engineer novel pressure-sensitive and thermosensitive proteins and raises new questions about how such modular sensors may have evolved and empowered ion channel pores with new sensibilities.

Keywords

Ion channel Temperature sensing Heat capacity ΔCp BacNav Bacterial voltage gated sodium channel Coiled-coil TRP channels 

References

  1. 1.
    Abenavoli A, DiFrancesco ML, Schroeder I, Epimashko S, Gazzarrini S, Hansen UP, Thiel G, Moroni A (2009) Fast and slow gating are inherent properties of the pore module of the K+ channel Kcv. J Gen Physiol 134(3):219–229.  https://doi.org/10.1085/jgp.200910266PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Abriata LA, Albanesi D, Dal Peraro M, de Mendoza D (2017) Signal sensing and transduction by histidine kinases as unveiled through studies on a temperature sensor. Acc Chem Res 50(6):1359–1366.  https://doi.org/10.1021/acs.accounts.6b00593PubMedCrossRefGoogle Scholar
  3. 3.
    Aguilar PS, Hernandez-Arriaga AM, Cybulski LE, Erazo AC, de Mendoza D (2001) Molecular basis of thermosensing: a two-component signal transduction thermometer in Bacillus subtilis. EMBO J 20(7):1681–1691.  https://doi.org/10.1093/emboj/20.7.1681PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Akyuz N, Holt JR (2016) Plug-N-Play: mechanotransduction goes modular. Neuron 89(6):1128–1130.  https://doi.org/10.1016/j.neuron.2016.02.041PubMedCrossRefGoogle Scholar
  5. 5.
    Alabi AA, Bahamonde MI, Jung HJ, Kim JI, Swartz KJ (2007) Portability of paddle motif function and pharmacology in voltage sensors. Nature 450(7168):370–375.  https://doi.org/10.1038/nature06266PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Albanesi D, Martin M, Trajtenberg F, Mansilla MC, Haouz A, Alzari PM, de Mendoza D, Buschiazzo A (2009) Structural plasticity and catalysis regulation of a thermosensor histidine kinase. Proc Natl Acad Sci U S A 106(38):16185–16190.  https://doi.org/10.1073/pnas.0906699106PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Alexander P, Fahnestock S, Lee T, Orban J, Bryan P (1992) Thermodynamic analysis of the folding of the streptococcal protein G IgG-binding domains B1 and B2: why small proteins tend to have high denaturation temperatures. Biochemistry 31(14):3597–3603.  https://doi.org/10.1021/bi00129a007PubMedCrossRefGoogle Scholar
  8. 8.
    Anishkin A, Loukin SH, Teng J, Kung C (2014) Feeling the hidden mechanical forces in lipid bilayer is an original sense. Proc Natl Acad Sci U S A 111(22):7898–7905.  https://doi.org/10.1073/pnas.1313364111PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Arrigoni C, Rohaim A, Shaya D, Findeisen F, Stein RA, Nurva SR, Mishra S, McHaourab HS, Minor DL Jr (2016) Unfolding of a temperature-sensitive domain controls voltage-gated channel activation. Cell 164(5):922–936.  https://doi.org/10.1016/j.cell.2016.02.001PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Arrigoni C, Schroeder I, Romani G, Van Etten JL, Thiel G, Moroni A (2013) The voltage-sensing domain of a phosphatase gates the pore of a potassium channel. J Gen Physiol 141(3):389–395.  https://doi.org/10.1085/jgp.201210940PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Aryal P, Jarerattanachat V, Clausen MV, Schewe M, McClenaghan C, Argent L, Conrad LJ, Dong YY, Pike ACW, Carpenter EP, Baukrowitz T, Sansom MSP, Tucker SJ (2017) Bilayer-mediated structural transitions control mechanosensitivity of the TREK-2 K2P channel. Structure 25:708–718 e702.  https://doi.org/10.1016/j.str.2017.03.006PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Bagriantsev SN, Clark KA, Minor DL Jr (2012) Metabolic and thermal stimuli control K(2P)2.1 (TREK-1) through modular sensory and gating domains. EMBO J 31(15):3297–3308.  https://doi.org/10.1038/emboj.2012.171PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Beadle BM, Shoichet BK (2002) Structural bases of stability-function tradeoffs in enzymes. J Mol Biol 321(2):285–296.  https://doi.org/10.1016/S0022-2836(02)00599-5PubMedCrossRefGoogle Scholar
  14. 14.
    Becktel WJ, Schellman JA (1987) Protein stability curves. Biopolymers 26(11):1859–1877.  https://doi.org/10.1002/bip.360261104PubMedCrossRefGoogle Scholar
  15. 15.
    Berneche S, Roux B (2005) A gate in the selectivity filter of potassium channels. Structure 13(4):591–600.  https://doi.org/10.1016/j.str.2004.12.019PubMedCrossRefGoogle Scholar
  16. 16.
    Berrier C, Pozza A, de Lacroix de Lavalette A, Chardonnet S, Mesneau A, Jaxel C, le Maire M, Ghazi A (2013) The purified mechanosensitive channel TREK-1 is directly sensitive to membrane tension. J Biol Chem 288(38):27307–27314.  https://doi.org/10.1074/jbc.M113.478321PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Bhattacharyya RP, Remenyi A, Yeh BJ, Lim WA (2006) Domains, motifs, and scaffolds: the role of modular interactions in the evolution and wiring of cell signaling circuits. Annu Rev Biochem 75(1):655–680.  https://doi.org/10.1146/annurev.biochem.75.103004.142710PubMedCrossRefGoogle Scholar
  18. 18.
    Bosmans F, Martin-Eauclaire MF, Swartz KJ (2008) Deconstructing voltage sensor function and pharmacology in sodium channels. Nature 456(7219):202–208.  https://doi.org/10.1038/nature07473PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    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(18):4835–4840.  https://doi.org/10.1523/JNEUROSCI.5080-05.2006PubMedCrossRefGoogle Scholar
  20. 20.
    Brohawn SG, Su Z, MacKinnon R (2014) Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K+ channels. Proc Natl Acad Sci U S A 111(9):3614–3619.  https://doi.org/10.1073/pnas.1320768111PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Cao E, Liao M, Cheng Y, Julius D (2013) TRPV1 structures in distinct conformations reveal activation mechanisms. Nature 504(7478):113–118.  https://doi.org/10.1038/nature12823PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Catterall WA, Wisedchaisri G, Zheng N (2017) The chemical basis for electrical signaling. Nat Chem Biol 13(5):455–463.  https://doi.org/10.1038/nchembio.2353PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Celic AS, Petri ET, Benbow J, Hodsdon ME, Ehrlich BE, Boggon TJ (2012) Calcium-induced conformational changes in C-terminal tail of polycystin-2 are necessary for channel gating. J Biol Chem 287(21):17232–17240.  https://doi.org/10.1074/jbc.M112.354613PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Chothia C, Gough J, Vogel C, Teichmann SA (2003) Evolution of the protein repertoire. Science 300(5626):1701–1703.  https://doi.org/10.1126/science.1085371PubMedCrossRefGoogle Scholar
  25. 25.
    Chowdhury S, Jarecki BW, Chanda B (2014) A molecular framework for temperature-dependent gating of ion channels. Cell 158(5):1148–1158.  https://doi.org/10.1016/j.cell.2014.07.026PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Clapham DE, Miller C (2011) A thermodynamic framework for understanding temperature sensing by transient receptor potential (TRP) channels. Proc Natl Acad Sci U S A 108(49):19492–19497.  https://doi.org/10.1073/pnas.1117485108PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Clausen MV, Jarerattanachat V, Carpenter EP, Sansom MSP, Tucker SJ (2017) Asymmetric mechanosensitivity in a eukaryotic ion channel. Proc Natl Acad Sci U S A 114(40):E8343–E8351.  https://doi.org/10.1073/pnas.1708990114PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Cordero-Morales JF, Cuello LG, Perozo E (2006) Voltage-dependent gating at the KcsA selectivity filter. Nat Struct Mol Biol 13(4):319–322.  https://doi.org/10.1038/nsmb1070PubMedCrossRefGoogle Scholar
  29. 29.
    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(46):E1184–E1191.  https://doi.org/10.1073/pnas.1114124108PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Creighton TE (1993) Proteins: structures and molecular properties, 2nd edn. W.H. Freeman and Company, New YorkGoogle Scholar
  31. 31.
    Creighton TE (2010) The biophysical chemistry of nucleic acids & proteins. Helvetian Press,Google Scholar
  32. 32.
    Cybulski LE, Ballering J, Moussatova A, Inda ME, Vazquez DB, Wassenaar TA, de Mendoza D, Tieleman DP, Killian JA (2015) Activation of the bacterial thermosensor DesK involves a serine zipper dimerization motif that is modulated by bilayer thickness. Proc Natl Acad Sci U S A 112(20):6353–6358.  https://doi.org/10.1073/pnas.1422446112PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    DeCaen PG, Takahashi Y, Krulwich TA, Ito M, Clapham DE (2014) Ionic selectivity and thermal adaptations within the voltage-gated sodium channel family of alkaliphilic Bacillus. eLife 3. doi: https://doi.org/10.7554/eLife.04387
  34. 34.
    Devi VS, Binz HK, Stumpp MT, Pluckthun A, Bosshard HR, Jelesarov I (2004) Folding of a designed simple ankyrin repeat protein. Protein Sci 13(11):2864–2870.  https://doi.org/10.1110/ps.04935704PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Diaz-Franulic I, Poblete H, Mino-Galaz G, Gonzalez C, Latorre R (2016) Allosterism and structure in thermally activated transient receptor potential channels. Annu Rev Biophys 45(1):371–398.  https://doi.org/10.1146/annurev-biophys-062215-011034PubMedCrossRefGoogle Scholar
  36. 36.
    Dubin AE, Murthy S, Lewis AH, Brosse L, Cahalan SM, Grandl J, Coste B, Patapoutian A (2017) Editorial note to: endogenous Piezo1 can confound mechanically activated channel identification and characterization. Neuron 94(2):265–265.  https://doi.org/10.1016/j.neuron.2017.03.041PubMedCrossRefGoogle Scholar
  37. 37.
    Dubin AE, Murthy S, Lewis AH, Brosse L, Cahalan SM, Grandl J, Coste B, Patapoutian A (2017) Endogenous Piezo1 can confound mechanically activated channel identification and characterization. Neuron 94:266.  https://doi.org/10.1016/j.neuron.2017.03.039PubMedCrossRefGoogle Scholar
  38. 38.
    Dutzler R, Campbell EB, MacKinnon R (2003) Gating the selectivity filter in ClC chloride channels. Science 300(5616):108–112.  https://doi.org/10.1126/science.1082708PubMedCrossRefGoogle Scholar
  39. 39.
    Eisele JL, Bertrand S, Galzi JL, Devillers-Thiery A, Changeux JP, Bertrand D (1993) Chimaeric nicotinic-serotonergic receptor combines distinct ligand binding and channel specificities. Nature 366(6454):479–483.  https://doi.org/10.1038/366479a0PubMedCrossRefGoogle Scholar
  40. 40.
    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(50):38396–38404.  https://doi.org/10.1074/jbc.M607756200PubMedCrossRefGoogle Scholar
  41. 41.
    Fujiwara Y, Kurokawa T, Takeshita K, Kobayashi M, Okochi Y, Nakagawa A, Okamura Y (2012) The cytoplasmic coiled-coil mediates cooperative gating temperature sensitivity in the voltage-gated H(+) channel Hv1. Nat Commun 3:816.  https://doi.org/10.1038/ncomms1823PubMedCrossRefGoogle Scholar
  42. 42.
    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 NeurosciGoogle Scholar
  43. 43.
    Haswell ES, Phillips R, Rees DC (2011) Mechanosensitive channels: what can they do and how do they do it? Structure 19(10):1356–1369.  https://doi.org/10.1016/j.str.2011.09.005PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Hille B (2001) Ion channels of excitable membranes, 3rd edn. Sinauer Associates, Inc., SunderlandGoogle Scholar
  45. 45.
    Howard RJ, Clark KA, Holton JM, Minor DL Jr (2007) Structural insight into KCNQ (Kv7) channel assembly and channelopathy. Neuron 53(5):663–675.  https://doi.org/10.1016/j.neuron.2007.02.010PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Hurme R, Berndt KD, Namork E, Rhen M (1996) DNA binding exerted by a bacterial gene regulator with an extensive coiled-coil domain. J Biol Chem 271(21):12626–12631.  https://doi.org/10.1074/jbc.271.21.12626PubMedCrossRefGoogle Scholar
  47. 47.
    Hurme R, Berndt KD, Normark SJ, Rhen M (1997) A proteinaceous gene regulatory thermometer in Salmonella. Cell 90(1):55–64.  https://doi.org/10.1016/S0092-8674(00)80313-XPubMedCrossRefGoogle Scholar
  48. 48.
    Inda ME, Oliveira RG, de Mendoza D, Cybulski LE (2016) The single transmembrane segment of minimal sensor DesK senses temperature via a membrane-thickness caliper. J Bacteriol 198(21):2945–2954.  https://doi.org/10.1128/JB.00431-16PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Jabba S, Goyal R, Sosa-Pagan JO, Moldenhauer H, Wu J, Kalmeta B, Bandell M, Latorre R, Patapoutian A, Grandl J (2014) Directionality of temperature activation in mouse TRPA1 ion channel can be inverted by single-point mutations in ankyrin repeat six. Neuron 82(5):1017–1031.  https://doi.org/10.1016/j.neuron.2014.04.016PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Janovjak H, Szobota S, Wyart C, Trauner D, Isacoff EY (2010) A light-gated, potassium-selective glutamate receptor for the optical inhibition of neuronal firing. Nat Neurosci 13(8):1027–1032.  https://doi.org/10.1038/nn.2589PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Jenke M, Sanchez A, Monje F, Stuhmer W, Weseloh RM, Pardo LA (2003) C-terminal domains implicated in the functional surface expression of potassium channels. EMBO J 22(3):395–403.  https://doi.org/10.1093/emboj/cdg035PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Jin J, Xie X, Chen C, Park JG, Stark C, James DA, Olhovsky M, Linding R, Mao Y, Pawson T (2009) Eukaryotic protein domains as functional units of cellular evolution. Sci Signal 2(98):ra76.  https://doi.org/10.1126/scisignal.2000546PubMedCrossRefGoogle Scholar
  53. 53.
    Jin P, Bulkley D, Guo Y, Zhang W, Guo Z, Huynh W, Wu S, Meltzer S, Cheng T, Jan LY, Jan YN, Cheng Y (2017) Electron cryo-microscopy structure of the mechanotransduction channel NOMPC. Nature 547(7661):118–122.  https://doi.org/10.1038/nature22981PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Kiyonaka S, Kajimoto T, Sakaguchi R, Shinmi D, Omatsu-Kanbe M, Matsuura H, Imamura H, Yoshizaki T, Hamachi I, Morii T, Mori Y (2013) Genetically encoded fluorescent thermosensors visualize subcellular thermoregulation in living cells. Nat Methods 10(12):1232–1238.  https://doi.org/10.1038/nmeth.2690PubMedCrossRefGoogle Scholar
  55. 55.
    Koishi R, Xu H, Ren D, Navarro B, Spiller BW, Shi Q, Clapham DE (2004) A superfamily of voltage-gated sodium channels in bacteria. J Biol Chem 279(10):9532–9538.  https://doi.org/10.1074/jbc.M313100200PubMedCrossRefGoogle Scholar
  56. 56.
    Kung C (2005) A possible unifying principle for mechanosensation. Nature 436(7051):647–654.  https://doi.org/10.1038/nature03896PubMedCrossRefGoogle Scholar
  57. 57.
    Laursen WJ, Bagriantsev SN, Gracheva EO (2014) TRPA1 channels: chemical and temperature sensitivity. Curr Top Membr 74:89–112.  https://doi.org/10.1016/B978-0-12-800181-3.00004-XPubMedCrossRefGoogle Scholar
  58. 58.
    Laursen WJ, Schneider ER, Merriman DK, Bagriantsev SN, Gracheva EO (2016) Low-cost functional plasticity of TRPV1 supports heat tolerance in squirrels and camels. Proc Natl Acad Sci U S A 113(40):11342–11347.  https://doi.org/10.1073/pnas.1604269113PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Loladze VV, Ermolenko DN, Makhatadze GI (2001) Heat capacity changes upon burial of polar and nonpolar groups in proteins. Protein Sci 10(7):1343–1352.  https://doi.org/10.1110/ps.370101PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Loladze VV, Ermolenko DN, Makhatadze GI (2002) Thermodynamic consequences of burial of polar and non-polar amino acid residues in the protein interior. J Mol Biol 320(2):343–357.  https://doi.org/10.1016/S0022-2836(02)00465-5PubMedCrossRefGoogle Scholar
  61. 61.
    Lolicato M, Arrigoni C, Mori T, Sekioka Y, Bryant C, Clark KA, Minor DL Jr (2017) K2P2.1 (TREK-1)-activator complexes reveal a cryptic selectivity filter binding site. Nature 547(7663):364–368.  https://doi.org/10.1038/nature22988PubMedCrossRefGoogle Scholar
  62. 62.
    Lumb KJ, Kim PS (1995) A buried polar interaction imparts structural uniqueness in a designed heterodimeric coiled coil. Biochemistry 34(27):8642–8648.  https://doi.org/10.1021/bi00027a013PubMedCrossRefGoogle Scholar
  63. 63.
    Lupas AN, Gruber M (2005) The structure of alpha-helical coiled coils. Adv Protein Chem 70:37–78.  https://doi.org/10.1016/S0065-3233(05)70003-6PubMedCrossRefGoogle Scholar
  64. 64.
    Marchesi A, Mazzolini M, Torre V (2012) Gating of cyclic nucleotide-gated channels is voltage dependent. Nat Commun 3:973.  https://doi.org/10.1038/ncomms1972PubMedCrossRefGoogle Scholar
  65. 65.
    McCusker EC, Bagneris C, Naylor CE, Cole AR, D'Avanzo N, Nichols CG, Wallace BA (2012) Structure of a bacterial voltage-gated sodium channel pore reveals mechanisms of opening and closing. Nat Commun 3:1102.  https://doi.org/10.1038/ncomms2077PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    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(50):38748–38756.  https://doi.org/10.1074/jbc.M607591200PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Minor DL Jr, Kim PS (1994) Context is a major determinant of beta-sheet propensity. Nature 371(6494):264–267.  https://doi.org/10.1038/371264a0PubMedCrossRefGoogle Scholar
  68. 68.
    Minor DL Jr, Kim PS (1994) Measurement of the beta-sheet-forming propensities of amino acids. Nature 367(6464):660–663.  https://doi.org/10.1038/367660a0PubMedCrossRefGoogle Scholar
  69. 69.
    Minor DL Jr, Lin YF, Mobley BC, Avelar A, Jan YN, Jan LY, Berger JM (2000) The polar T1 interface is linked to conformational changes that open the voltage-gated potassium channel. Cell 102:657–670PubMedCrossRefGoogle Scholar
  70. 70.
    Morales-Perez CL, Noviello CM, Hibbs RE (2016) X-ray structure of the human alpha4beta2 nicotinic receptor. Nature 538(7625):411–415.  https://doi.org/10.1038/nature19785PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Naik RR, Kirkpatrick SM, Stone MO (2001) The thermostability of an alpha-helical coiled-coil protein and its potential use in sensor applications. Biosens Bioelectron 16(9-12):1051–1057.  https://doi.org/10.1016/S0956-5663(01)00226-3PubMedCrossRefGoogle Scholar
  72. 72.
    Nemecz A, Prevost MS, Menny A, Corringer PJ (2016) Emerging molecular mechanisms of signal transduction in pentameric ligand-gated ion channels. Neuron 90(3):452–470.  https://doi.org/10.1016/j.neuron.2016.03.032PubMedCrossRefGoogle Scholar
  73. 73.
    Ohndorf UM, MacKinnon R (2005) Construction of a cyclic nucleotide-gated KcsA K+ channel. J Mol Biol 350(5):857–865.  https://doi.org/10.1016/j.jmb.2005.05.050PubMedCrossRefGoogle Scholar
  74. 74.
    Okamura Y, Fujiwara Y, Sakata S (2015) Gating mechanisms of voltage-gated proton channels. Annu Rev Biochem 84(1):685–709.  https://doi.org/10.1146/annurev-biochem-060614-034307PubMedCrossRefGoogle Scholar
  75. 75.
    Paulsen CE, Armache JP, Gao Y, Cheng Y, Julius D (2015) Structure of the TRPA1 ion channel suggests regulatory mechanisms. Nature 520(7548):511–517.  https://doi.org/10.1038/nature14367PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Payandeh J, Gamal El-Din TM, Scheuer T, Zheng N, Catterall WA (2012) Crystal structure of a voltage-gated sodium channel in two potentially inactivated states. Nature 486:135–139.  https://doi.org/10.1038/nature11077PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Payandeh J, Minor DL Jr (2015) Bacterial voltage-gated sodium channels (BacNas) from the soil, sea, and salt lakes enlighten molecular mechanisms of electrical signaling and pharmacology in the brain and heart. J Mol Biol 427(1):3–30.  https://doi.org/10.1016/j.jmb.2014.08.010PubMedCrossRefGoogle Scholar
  78. 78.
    Payandeh J, Scheuer T, Zheng N, Catterall WA (2011) The crystal structure of a voltage-gated sodium channel. Nature 475(7356):353–358.  https://doi.org/10.1038/nature10238PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Perozo E (2006) Gating prokaryotic mechanosensitive channels. Nat Rev Mol Cell Biol 7(2):109–119.  https://doi.org/10.1038/nrm1833PubMedCrossRefGoogle Scholar
  80. 80.
    Pliotas C, Naismith JH (2017) Spectator no more, the role of the membrane in regulating ion channel function. Curr Opin Struct Biol 45:59–66.  https://doi.org/10.1016/j.sbi.2016.10.017PubMedCrossRefGoogle Scholar
  81. 81.
    Powl AM, O'Reilly AO, Miles AJ, Wallace BA (2010) Synchrotron radiation circular dichroism spectroscopy-defined structure of the C-terminal domain of NaChBac and its role in channel assembly. Proc Natl Acad Sci U S A 107(32):14064–14069.  https://doi.org/10.1073/pnas.1001793107PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Prabhu NV, Sharp KA (2005) Heat capacity in proteins. Annu Rev Phys Chem 56(1):521–548.  https://doi.org/10.1146/annurev.physchem.56.092503.141202PubMedCrossRefGoogle Scholar
  83. 83.
    Privalov PL, Gill SJ (1988) Stability of protein structure and hydrophobic interaction. Adv Protein Chem 39:191–234.  https://doi.org/10.1016/S0065-3233(08)60377-0PubMedCrossRefGoogle Scholar
  84. 84.
    Pucci F, Rooman M (2017) Physical and molecular bases of protein thermal stability and cold adaptation. Curr Opin Struct Biol 42:117–128.  https://doi.org/10.1016/j.sbi.2016.12.007PubMedCrossRefGoogle Scholar
  85. 85.
    Pusch M, Ludewig U, Rehfeldt A, Jentsch TJ (1995) Gating of the voltage-dependent chloride channel CIC-0 by the permeant anion. Nature 373(6514):527–531.  https://doi.org/10.1038/373527a0PubMedCrossRefGoogle Scholar
  86. 86.
    Qian F, Germino FJ, Cai Y, Zhang X, Somlo S, Germino GG (1997) PKD1 interacts with PKD2 through a probable coiled-coil domain. Nat Genet 16(2):179–183.  https://doi.org/10.1038/ng0697-179PubMedCrossRefGoogle Scholar
  87. 87.
    Razvi A, Scholtz JM (2006) Lessons in stability from thermophilic proteins. Protein Sci 15(7):1569–1578.  https://doi.org/10.1110/ps.062130306PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Ren D, Navarro B, Xu H, Yue L, Shi Q, Clapham DE (2001) A prokaryotic voltage-gated sodium channel. Science 294(5550):2372–2375.  https://doi.org/10.1126/science.1065635PubMedCrossRefGoogle Scholar
  89. 89.
    Saita E, Abriata LA, Tsai YT, Trajtenberg F, Lemmin T, Buschiazzo A, Dal Peraro M, de Mendoza D, Albanesi D (2015) A coiled coil switch mediates cold sensing by the thermosensory protein DesK. Mol Microbiol 98(2):258–271.  https://doi.org/10.1111/mmi.13118PubMedCrossRefGoogle Scholar
  90. 90.
    Schewe M, Nematian-Ardestani E, Sun H, Musinszki M, Cordeiro S, Bucci G, de Groot BL, Tucker SJ, Rapedius M, Baukrowitz T (2016) A non-canonical voltage-sensing mechanism controls gating in K2P K(+) channels. Cell 164(5):937–949.  https://doi.org/10.1016/j.cell.2016.02.002PubMedPubMedCentralCrossRefGoogle Scholar
  91. 91.
    Schneider ER, Anderson EO, Gracheva EO, Bagriantsev SN (2014) Temperature sensitivity of two-pore (K2P) potassium channels. Curr Top Membr 74:113–133.  https://doi.org/10.1016/B978-0-12-800181-3.00005-1PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Sengupta P, Garrity P (2013) Sensing temperature. Curr Biol : CB 23(8):R304–R307.  https://doi.org/10.1016/j.cub.2013.03.009PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Shaya D, Findeisen F, Abderemane-Ali F, Arrigoni C, Wong S, Nurva SR, Loussouarn G, Minor DL Jr (2014) Structure of a prokaryotic sodium channel pore reveals essential gating elements and an outer ion binding site common to eukaryotic channels. J Mol Biol 426(2):467–483.  https://doi.org/10.1016/j.jmb.2013.10.010PubMedCrossRefGoogle Scholar
  94. 94.
    Shaya D, Kreir M, Robbins RA, Wong S, Hammon J, Bruggemann A, Minor DL Jr (2011) Voltage-gated sodium channel (NaV) protein dissection creates a set of functional pore-only proteins. Proc Natl Acad Sci U S A 108(30):12313–12318.  https://doi.org/10.1073/pnas.1106811108PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Shoichet BK, Baase WA, Kuroki R, Matthews BW (1995) A relationship between protein stability and protein function. Proc Natl Acad Sci U S A 92(2):452–456.  https://doi.org/10.1073/pnas.92.2.452PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Steinbacher S, Bass R, Strop P, Rees DC (2007) Structures of the prokaryotic mechanosensitive channels MscL and MscS in: Hamill OP (ed) current topics in membranes mechanosensitive ion channels, Part A. Academic Press, London, pp 1–24Google Scholar
  97. 97.
    Sukharev S, Durell SR, Guy HR (2001) Structural models of the MscL gating mechanism. Biophys J 81(2):917–936.  https://doi.org/10.1016/S0006-3495(01)75751-7PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Syeda R, Florendo MN, Cox CD, Kefauver JM, Santos JS, Martinac B, Patapoutian A (2016) Piezo1 channels are inherently mechanosensitive. Cell Rep 17(7):1739–1746.  https://doi.org/10.1016/j.celrep.2016.10.033PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Takeshita K, Sakata S, Yamashita E, Fujiwara Y, Kawanabe A, Kurokawa T, Okochi Y, Matsuda M, Narita H, Okamura Y, Nakagawa A (2014) X-ray crystal structure of voltage-gated proton channel. Nat Struct Mol Biol 21(4):352–U170.  https://doi.org/10.1038/nsmb.2783PubMedCrossRefGoogle Scholar
  100. 100.
    Tsiokas L, Kim E, Arnould T, Sukhatme VP, Walz G (1997) Homo- and heterodimeric interactions between the gene products of PKD1 and PKD2. Proc Natl Acad Sci U S A 94(13):6965–6970.  https://doi.org/10.1073/pnas.94.13.6965PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Tsuruda PR, Julius D, Minor DL Jr (2006) Coiled coils direct assembly of a cold-activated TRP channel. Neuron 51(2):201–212.  https://doi.org/10.1016/j.neuron.2006.06.023PubMedPubMedCentralCrossRefGoogle Scholar
  102. 102.
    Twomey EC, Sobolevsky AI (2017) Structural mechanisms of gating in ionotropic glutamate receptors. Biochemistry.  https://doi.org/10.1021/acs.biochem.7b00891
  103. 103.
    Vargas E, Yarov-Yarovoy V, Khalili-Araghi F, Catterall WA, Klein ML, Tarek M, Lindahl E, Schulten K, Perozo E, Bezanilla F, Roux B (2012) An emerging consensus on voltage-dependent gating from computational modeling and molecular dynamics simulations. J Gen Physiol 140(6):587–594.  https://doi.org/10.1085/jgp.201210873PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Vriens J, Nilius B, Voets T (2014) Peripheral thermosensation in mammals. Nat Rev Neurosci 15(9):573–589.  https://doi.org/10.1038/nrn3784PubMedCrossRefGoogle Scholar
  105. 105.
    Whorton MR, MacKinnon R (2013) X-ray structure of the mammalian GIRK2-betagamma G-protein complex. Nature 498(7453):190–197.  https://doi.org/10.1038/nature12241PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Wiener R, Haitin Y, Shamgar L, Fernandez-Alonso MC, Martos A, Chomsky-Hecht O, Rivas G, Attali B, Hirsch JA (2008) The KCNQ1 (Kv7.1) COOH terminus, a multitiered scaffold for subunit assembly and protein interaction. J Biol Chem 283(9):5815–5830.  https://doi.org/10.1074/jbc.M707541200PubMedCrossRefGoogle Scholar
  107. 107.
    Wu J, Goyal R, Grandl J (2016) Localized force application reveals mechanically sensitive domains of Piezo1. Nat Commun 7:12939.  https://doi.org/10.1038/ncomms12939PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Yu FH, Yarov-Yarovoy V, Gutman GA, Catterall WA (2005) Overview of molecular relationships in the voltage-gated ion channel superfamily. Pharmacol Rev 57:387–395PubMedCrossRefGoogle Scholar
  109. 109.
    Yu Y, Ulbrich MH, Li MH, Buraei Z, Chen XZ, Ong AC, Tong L, Isacoff EY, Yang J (2009) Structural and molecular basis of the assembly of the TRPP2/PKD1 complex. Proc Natl Acad Sci U S A 106(28):11558–11563.  https://doi.org/10.1073/pnas.0903684106PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Yu Y, Ulbrich MH, Li MH, Dobbins S, Zhang WK, Tong L, Isacoff EY, Yang J (2012) Molecular mechanism of the assembly of an acid-sensing receptor ion channel complex. Nat Commun 3:1252.  https://doi.org/10.1038/ncomms2257PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Zhang W, Cheng LE, Kittelmann M, Li JF, Petkovic M, Cheng T, Jin P, Guo ZH, Gopfert MC, Jan LY, Jan YN (2015) Ankyrin repeats convey force to gate the NOMPC mechanotransduction channel. Cell 162(6):1391–1403.  https://doi.org/10.1016/j.cell.2015.08.024PubMedPubMedCentralCrossRefGoogle Scholar
  112. 112.
    Zhao QC, Wu K, Chi SP, Geng J, Xiao BL (2017) Heterologous expression of the Piezo1-ASIC1 chimera induces mechanosensitive currents with properties distinct from Piezo1. Neuron 94(2):274–277.  https://doi.org/10.1016/j.neuron.2017.03.040PubMedCrossRefGoogle Scholar
  113. 113.
    Zhao QC, Wu K, Geng J, Chi SP, Wang YF, Zhi P, Zhang MM, Xiao BL (2016) Ion permeation and mechanotransduction mechanisms of mechanosensitive piezo channels. Neuron 89(6):1248–1263.  https://doi.org/10.1016/j.neuron.2016.01.046PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Cardiovascular Research InstituteUniversity of CaliforniaSan FranciscoUSA
  2. 2.Departments of Biochemistry and Biophysics, and Cellular and Molecular PharmacologyUniversity of CaliforniaSan FranciscoUSA
  3. 3.California Institute for Quantitative Biomedical ResearchUniversity of CaliforniaSan FranciscoUSA
  4. 4.Kavli Institute for Fundamental NeuroscienceUniversity of CaliforniaSan FranciscoUSA
  5. 5.Molecular Biophysics and Integrated Bio-imaging DivisionLawrence Berkeley National LaboratoryBerkeleyUSA

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