Temperature Sensitivity of Two-Pore (K2P) Potassium Channels

Current Topics in Membranes

Volumn 74, Issue 1, 2014, Pages 113-133

  Schneider, Eve R ^a   Anderson, Evan O ^a   Gracheva, Elena O ^a   Bagriantsev, Sviatoslav N ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ion channel; K2P; Potassium channel; Thermosensitivity; Thermotransduction; TRAAK; TREK 1; TREK 2; Two pore

Indexed keywords

POTASSIUM CHANNEL;

ANIMAL; CHANNEL GATING; CHEMISTRY; MECHANICS; METABOLISM; TEMPERATURE SENSE;

ANIMALS; ION CHANNEL GATING; MECHANICAL PROCESSES; POTASSIUM CHANNELS; THERMOSENSING;

EID: 84922789571     PISSN: 10635823     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-800181-3.00005-1     Document Type: Chapter

References (104)

1. Acosta C., Djouhri L., Watkins R., Berry C., Bromage K., Lawson S.N. TREK2 expressed selectively in IB4-binding C-fiber nociceptors hyperpolarizes theirmembrane potentials and limits spontaneous pain. Journal of Neuroscience 2014, 34:1494-1509.
2. + channels. Biophysical Journal 2003, 85:300-312.
3. Alloui A., Zimmermann K., Mamet J., Duprat F., Noel J., Chemin J., et al. TREK-1, a K+ channel involved in polymodal pain perception. EMBO Journal 2006, 25:2368-2376.
4. Arnadottir J., Chalfie M. Eukaryotic mechanosensitive channels. Annual Review of Biophysics 2010, 39:111-137.
5. 2P channels. ACS Chemical Biology 2013, 8:1841-1851.
6. Bagriantsev S.N., Clark K.A., Minor D.L. Metabolic and thermal stimuli control K(2P)2.1 (TREK-1) through modular sensory and gating domains. EMBO Journal 2012, 31:3297-3308.
7. Bagriantsev S.N., Peyronnet R., Clark K.A., Honore E., Minor D.L. Multiple modalities converge on a common gate to control K(2P) channel function. EMBO Journal 2011, 30:3594-3606.
8. + channel family. Journal of Biological Chemistry 2000, 275:17412-17419.
9. Bautista D.M., Siemens J., Glazer J.M., Tsuruda P.R., Basbaum A.I., Stucky C.L., et al. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 2007, 448:204-208.
10. Bearzatto B., Lesage F., Reyes R., Lazdunski M., Laduron P.M. Axonal transport of TREK and TRAAK potassium channels in rat sciatic nerves. Neuroreport 2000, 11:927-930.
11. + channel gates underlies distinct roles in electrical signaling. Nature Structural & Molecular Biology 2009, 16:71-79.
12. Berrier C., Pozza A., de Lacroix de Lavalette A., Chardonnet S., Mesneau A., Jaxel C., et al. The purified mechanosensitive channel TREK-1 is directly sensitive to membrane tension. Journal of Biological Chemistry 2013, 288:27307-27314.
13. Bittner S., Ruck T., Schuhmann M.K., Herrmann A.M., Maati H.M., Bobak N., et al. Endothelial TWIK-related potassium channel-1 (TREK1) regulates immune-cell trafficking into the CNS. Nature Medicine 2013, 19:1161-1165.
14. Brohawn S.G., Campbell E.B., MacKinnon R. Domain-swapped chain connectivity and gated membrane access in a Fab-mediated crystal of the human TRAAK K+ channel. Proc Natl Acad Sci U S A 2013, 110:2129-2134.
15. + ion channel. Science 2012, 335:436-441.
16. Brohawn S.G., Su Z., MacKinnon R. Mechanosensitivity is mediated directly by the lipid membrane in TRAAK and TREK1 K+ channels. Proc Natl Acad Sci U S A 2014, 111:3614-3619.
17. Bryan R.M., You J., Phillips S.C., Andresen J.J., Lloyd E.E., Rogers P.A., et al. Evidence for two-pore domain potassium channels in rat cerebral arteries. American Journal of Physiology - Heart and Circulatory Physiology 2006, 291:H770-H780.
18. Cao E., Cordero-Morales J.F., Liu B., Qin F., Julius D. TRPV1 channels are intrinsically heat sensitive and negatively regulated by phosphoinositide lipids. Neuron 2013, 77:667-679.
19. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., et al. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000, 288:306-313.
20. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
21. Chatelain F.C., Bichet D., Douguet D., Feliciangeli S., Bendahhou S., Reichold M., et al. TWIK1, a unique background channel with variable ion selectivity. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:5499-5504.
22. + channel TREK-1. EMBO Journal 2005, 24:44-53.
23. Chowdhury S., Jarecki B.W., Chanda B. A molecular framework for temperature-dependent gating of ion channels. Cell 2014, 158:1148-1158.
24. Clapham D.E., Miller C. A thermodynamic framework for understanding temperature sensing by transient receptor potential (TRP) channels. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:19492-19497.
25. Cohen A., Ben-Abu Y., Hen S., Zilberberg N. A novel mechanism for human K2P2.1 channel gating. Facilitation of C-type gating by protonation of extracellular histidine residues. Journal of Biological Chemistry 2008, 283:19448-19455.
26. Colburn R.W., Lubin M.L., Stone D.J., Wang Y., Lawrence D., D'Andrea M.R., et al. Attenuated cold sensitivity in TRPM8 null mice. Neuron 2007, 54:379-386.
27. Contreras J.E., Srikumar D., Holmgren M. Gating at the selectivity filter in cyclic nucleotide-gated channels. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:3310-3314.
28. Cordero-Morales J.F., Cuello L.G., Zhao Y., Jogini V., Cortes D.M., Roux B., et al. Molecular determinants of gating at the potassium-channel selectivity filter. Nature Structural and Molecular Biology 2006, 13:311-318.
29. Coste B., Mathur J., Schmidt M., Earley T.J., Ranade S., Petrus M.J., et al. Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 2010, 330:55-60.
30. Coste B., Xiao B., Santos J.S., Syeda R., Grandl J., Spencer K.S., et al. Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 2012, 483:176-181.
31. Davis K.A., Cowley E.A. Two-pore-domain potassium channels supportanion secretion from human airway Calu-3 epithelial cells. Pflugers Archiv 2006, 451:631-641.
32. Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., et al. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 2000, 405:183-187.
33. de la Pena E., Malkia A., Vara H., Caires R., Ballesta J.J., Belmonte C., et al. The influence of cold temperature on cellular excitability of hippocampal networks. PLoS One 2012, 7:e52475.
34. Delmas P., Hao J., Rodat-Despoix L. Molecular mechanisms of mechanotransduction in mammalian sensory neurons. Nature Reviews Neuroscience 2011, 12:139-153.
35. Descoeur J., Pereira V., Pizzoccaro A., Francois A., Ling B., Maffre V., et al. Oxaliplatin-induced cold hypersensitivity is due to remodelling of ion channel expression in nociceptors. EMBO Molecular Medicine 2011, 3:266-278.
36. Dey D., Eckle V.S., Vitko I., Sullivan K.A., Lasiecka Z.M., Winckler B., et al. Apotassium leak channel silences hyperactive neurons and ameliorates status epilepticus. Epilepsia 2014, 55:203-213.
37. Dhaka A., Murray A.N., Mathur J., Earley T.J., Petrus M.J., Patapoutian A. TRPM8 is required for cold sensation in mice. Neuron 2007, 54:371-378.
38. + channels constitute a significant component of background potassium currents in murine dorsal root ganglion neurons. Journal of Physiology 2007, 585:867-879.
39. Dominguez-Lopez S., Howell R., Gobbi G. Characterization of serotonin neurotransmission in knockout mice: implications for major depression. Reviews in the Neurosciences 2012, 23:429-443.
40. Enyedi P., Czirjak G. Molecular background of leak K+ currents: two-pore domain potassium channels. Physiological Reviews 2010, 90:559-605.
41. Findeisen F., Minor D.L. Disruption of the IS6-AID linker affects voltage-gated calcium channel inactivation and facilitation. Journal of General Physiology 2009, 133:327-343.
42. + channel. EMBO Journal 1996, 15:6854-6862.
43. + ions. Biophysical Journal 2011, 101:1623-1631.
44. Garry A., Fromy B., Blondeau N., Henrion D., Brau F., Gounon P., et al. Altered acetylcholine, bradykinin and cutaneous pressure-induced vasodilation in mice lacking the TREK1 potassium channel: the endothelial link. EMBO Reports 2007, 8:354-359.
45. Gracheva E.O., Cordero-Morales J.F., Gonzalez-Carcacia J.A., Ingolia N.T., Manno C., Aranguren C.I., et al. Ganglion-specific splicing of TRPV1 underlies infrared sensation in vampire bats. Nature 2011, 476:88-91.
46. + channel involved in neuroprotection and general anesthesia. EMBOJournal 2004, 23:2684-2695.
47. Heurteaux C., Lucas G., Guy N., El Yacoubi M., Thummler S., Peng X.D., et al. Deletion of the background potassium channel TREK-1 results in a depression-resistant phenotype. Nature Neuroscience 2006, 9:1134-1141.
48. Heyman N.S., Cowles C.L., Barnett S.D., Wu Y.Y., Cullison C., Singer C.A., Leblanc N., Buxton I.L. TREK-1 currents in smooth muscle cells from pregnant human myometrium. Am J Physiol Cell Physiol 2013, 305:C632-642.
49. Honore E., Maingret F., Lazdunski M., Patel A.J. An intracellular proton sensor commands lipid- and mechano-gating of the K(+) channel TREK-1. EMBO Journal 2002, 21:2968-2976.
50. 2P channels. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:6859-6864.
51. Hwang E.M., Kim E., Yarishkin O., Woo D.H., Han K.S., Park N., et al. Adisulphide-linked heterodimer of TWIK-1 and TREK-1 mediates passive conductance in astrocytes. Nature Communications 2014, 5:3227.
52. + channels TREK-2 and TRAAK. Journal of Physiology 2005, 564:103-116.
53. Kang D., Hogan J.O., Kim D. THIK-1 (K2P13.1) is a small-conductance background K(+) channel in rat trigeminal ganglion neurons. Pflugers Arch 2014, 466:1289-1300.
54. + channels in dorsal root ganglion neurons. American Journal of Physiology - Cell Physiology 2006, 291:C138-C146.
55. Kennard L.E., Chumbley J.R., Ranatunga K.M., Armstrong S.J., Veale E.L., Mathie A. Inhibition of the human two-pore domain potassium channel, TREK-1, by fluoxetine and its metabolite norfluoxetine. British Journal of Pharmacology 2005, 144:821-829.
56. Knowlton W.M., Palkar R., Lippoldt E.K., McCoy D.D., Baluch F., Chen J., et al. A sensory-labeled line for cold: TRPM8-expressing sensory neurons define the cellular basis for cold, cold pain, and cooling-mediated analgesia. Journal of Neuroscience 2013, 33:2837-2848.
57. Kobayashi S., Hori A., Matsumura K., Hosokawa H. Point: heat-induced membrane depolarization of hypothalamic neurons: a putative mechanism of central thermosensitivity. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 2006, 290:R1479-R1480. discussion R1484.
58. Laigle C., Confort-Gouny S., Le Fur Y., Cozzone P.J., Viola A. Deletion of TRAAK potassium channel affects brain metabolism and protects against ischemia. PLoS One 2012, 7:e53266.
59. + channel with multiple regulations by polyunsaturated fatty acids, lysophospholipids, and Gs, Gi, and Gq protein-coupled receptors. Journal of Biological Chemistry 2000, 275:28398-28405.
60. Liu X., Huang H., Wang W., Wang J., Sachs F., Niu W. Stretch-activated potassium channels in hypotonically induced blebs of atrial myocytes. Journal of Membrane Biology 2008, 226:17-25.
61. + channel in a lipid membrane-like environment. Nature 2007, 450:376-382.
62. + channels. Journal of Physiology 2005, 564:117-129.
63. + channel. Journal of Biological Chemistry 1999, 274:1381-1387.
64. Maingret F., Lauritzen I., Patel A.J., Heurteaux C., Reyes R., Lesage F., et al. TREK-1 is a heat-activated background K(+) channel. EMBO Journal 2000, 19:2483-2491.
65. Maingret F., Patel A.J., Lesage F., Lazdunski M., Honore E. Mechano- or acid stimulation, two interactive modes of activation of the TREK-1 potassium channel. Journal of Biological Chemistry 1999, 274:26691-26696.
66. Ma X.Y., Yu J.M., Zhang S.Z., Liu X.Y., Wu B.H., Wei X.L., et al. External Ba2+ block of the two-pore domain potassium channel TREK-1 defines conformational transition in its selectivity filter. Journal of Biological Chemistry 2011, 286:39813-39822.
67. Ma L., Zhang X., Chen H. TWIK-1 two-pore domain potassium channels change ion selectivity and conduct inward leak sodium currents in hypokalemia. Science Signaling 2011, 4:ra37.
68. McKemy D.D., Neuhausser W.M., Julius D. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature 2002, 416:52-58.
69. Medhurst A.D., Rennie G., Chapman C.G., Meadows H., Duckworth M.D., Kelsell R.E., et al. Distribution analysis of human two pore domain potassium channels in tissues of the central nervous system and periphery. Brain Research Molecular Brain Research 2001, 86:101-114.
70. Miller A.N., Long S.B. Crystal structure of the human two-pore domain potassium channel K2P1. Science 2012, 335:432-436.
71. Murbartian J., Lei Q., Sando J.J., Bayliss D.A. Sequential phosphorylation mediates receptor- and kinase-induced inhibition of TREK-1 background potassium channels. Journal of Biological Chemistry 2005, 280:30175-30184.
72. Namiranian K., Lloyd E.E., Crossland R.F., Marrelli S.P., Taffet G.E., Reddy A.K., et al. Cerebrovascular responses in mice deficient in the potassium channel, TREK-1. American Journal of Physiology - Regulatory Integrative and Comparative Physiology 2010, 299:R461-R469.
73. 2P potassium channel TASK-2 by intra- and extracellular pH. Journal of Biological Chemistry 2010, 285:16467-16475.
74. Noel J., Sandoz G., Lesage F. Molecular regulations governing TREK and TRAAK channel functions. Channels (Austin) 2011, 5:402-409.
75. + channels TRAAK and TREK-1 control both warm and cold perception. EMBO Journal 2009, 28:1308-1318.
76. Park U., Vastani N., Guan Y., Raja S.N., Koltzenburg M., Caterina M.J. TRP vanilloid 2 knock-out mice are susceptible to perinatal lethality but display normal thermal and mechanical nociception. Journal of Neuroscience 2011, 31:11425-11436.
77. + channels. Nature Neuroscience 1999, 2:422-426.
78. + channel. EMBO Journal 1998, 17:4283-4290.
79. Peier A.M., Moqrich A., Hergarden A.C., Reeve A.J., Andersson D.A., Story G.M., et al. A TRP channel that senses cold stimuli and menthol. Cell 2002, 108:705-715.
80. 2P channels. EMBO Journal 2011, 30:3607-3619.
81. 2P channels in the operation of somatosensory nociceptors. Frontiers in Molecular Neuroscience 2012, 5:21.
82. Pogorzala L.A., Mishra S.K., Hoon M.A. The cellular code for Mammalian thermosensation. Journal of Neuroscience 2013, 33:5533-5541.
83. + channels. Journal of Biological Chemistry 2001, 276:7302-7311.
84. Roan E., Waters C.M., Teng B., Ghosh M., Schwingshackl A. The 2-Pore domain potassium channel TREK-1 regulates stretch-induced Detachment of alveolar epithelial cells. PLoS One 2014, 9:e89429.
85. Sandoz G., Bell S.C., Isacoff E.Y. Optical probing of a dynamic membrane interaction that regulates the TREK1 channel. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:2605-2610.
86. Sandoz G., Douguet D., Chatelain F., Lazdunski M., Lesage F. Extracellular acidification exerts opposite actions on TREK1 and TREK2 potassium channels via a single conserved histidine residue. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:14628-14633.
87. Schwingshackl A., Teng B., Ghosh M., Waters C.M. Regulation of monocyte chemotactic protein-1 secretion by the two-pore-domain potassium (K2P) channel TREK-1 in human alveolar epithelial cells. American Journal of Translational Research 2013, 5:530-542.
88. Stebe S., Schellig K., Lesage F., Breer H., Fleischer J. The thermosensitive potassium channel TREK-1 contributes to coolness-evoked responses of Grueneberg ganglion neurons. Cellular and molecular neurobiology 2014, 34:113-122.
89. Su Z., Anishkin A., Kung C., Saimi Y. The core domain as the force sensor of the yeast mechanosensitive TRP channel. Journal of General Physiology 2011, 138:627-640.
90. Sukharev S., Sachs F. Molecular force transduction by ion channels: diversity and unifying principles. Journal of Cell Science 2012, 125:3075-3083.
91. Talley E.M., Solorzano G., Lei Q., Kim D., Bayliss D.A. CNS distribution of members of the two-pore-domain (KCNK) potassium channel family. Journal of Neuroscience 2001, 21:7491-7505.
92. Thomas D., Plant L.D., Wilkens C.M., McCrossan Z.A., Goldstein S.A. Alternative translation initiation in rat brain yields K2P2.1 potassium channels permeable to sodium. Neuron 2008, 58:859-870.
93. Vallee N., Meckler C., Risso J.J., Blatteau J.E. Neuroprotective role of theTREK-1 channel in decompression sickness. Journal of Applied Physiology 2012, 112:1191-1196.
94. Vallee N., Rostain J.C., Risso J.J. Low susceptibility to inert gases and pressure symptoms in TREK-1-deficient mice. Neuroreport 2009, 20:343-347.
95. Wang W., Zhang M., Li P., Yuan H., Feng N., Peng Y., et al. An increased TREK-1-like potassium current in ventricular myocytes during rat cardiac hypertrophy. Journal of Cardiovascular Pharmacology 2013, 61:302-310.
96. Wechselberger M., Wright C.L., Bishop G.A., Boulant J.A. Ionic channels and conductance-based models for hypothalamic neuronal thermosensitivity. AmericanJournal of Physiology - Regulatory Integrative and Comparative Physiology 2006, 291:R518-R529.
97. Woo D.H., Han K.S., Shim J.W., Yoon B.E., Kim E., Bae J.Y., et al. TREK-1 and Best1 channels mediate fast and slow glutamate release in astrocytes upon GPCR activation. Cell 2012, 151:25-40.
98. Wu X., Liu Y., Chen X., Sun Q., Tang R., Wang W., et al. Involvement of TREK-1 activity in astrocyte function and neuroprotection under simulated ischemia conditions. Journal of Molecular Neuroscience 2013, 49:499-506.
99. Wu Y.Y., Singer C.A., Buxton I.L. Variants of stretch-activated two-pore potassium channel TREK-1 associated with preterm labor in humans. Biology of Reproduction 2012, 87:96.
100. Xian Tao L., Dyachenko V., Zuzarte M., Putzke C., Preisig-Muller R., Isenberg G., et al. The stretch-activated potassium channel TREK-1 in rat cardiac ventricular muscle. Cardiovascular Research 2006, 69:86-97.
101. Yamamoto Y., Hatakeyama T., Taniguchi K. Immunohistochemical colocalization of TREK-1, TREK-2 and TRAAK with TRP channels in the trigeminal ganglion cells. Neuroscience Letters 2009, 454:129-133.
102. Zhao Y., Boulant J.A. Temperature effects on neuronal membrane potentials and inward currents in rat hypothalamic tissue slices. Journal of Physiology 2005, 564:245-257.
103. Zhao L.N., Fu L., Gao Q.P., Xie R.S., Cao J.X. Regional differential expression of TREK-1 at left ventricle in myocardial infarction. Canadian Journal of Cardiology 2011, 27:826-833.
104. Zilberberg N., Ilan N., Goldstein S.A. KCNKO: opening and closing the 2-P-domain potassium leak channel entails "C-type" gating of the outer pore. Neuron 2001, 32:635-648.