Kv1.1 channels act as mechanical brake in the senses of touch and pain

Neuron

Volumn 77, Issue 5, 2013, Pages 899-914

  Hao, Jizhe ^a   Padilla, Françoise ^a   Dandonneau, Mathieu ^a   Lavebratt, Catharina ^c   Lesage, Florian ^b   Noël, Jacques ^b   Delmas, Patrick ^a  

^a University of Mediterranée   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

POTASSIUM CHANNEL KV1.1; CALCIUM ACTIVATED POTASSIUM CHANNEL; KCNH1 PROTEIN, MOUSE; POTASSIUM CHANNEL HERG; POTASSIUM CHANNEL KCNQ;

ADAPTATION; ALLODYNIA; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; HYPERALGESIA; MECHANICAL STIMULATION; MECHANORECEPTOR; MOUSE; NERVE CELL EXCITABILITY; NOCICEPTION; NONHUMAN; PAIN RECEPTOR; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPINAL GANGLION; TOUCH; TRANSPORT KINETICS; ANIMAL; BAGG ALBINO MOUSE; C3H MOUSE; C57BL MOUSE; GENETICS; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIAL; NERVE FIBER; PAIN; PAIN THRESHOLD; PATCH CLAMP; PATHOPHYSIOLOGY; PERCEPTIVE THRESHOLD; PHYSIOLOGY; SENSORY RECEPTOR; SIGNAL TRANSDUCTION; STATISTICAL ANALYSIS; STIMULATION;

ANIMALS; DATA INTERPRETATION, STATISTICAL; ETHER-A-GO-GO POTASSIUM CHANNELS; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; KCNQ POTASSIUM CHANNELS; KV1.1 POTASSIUM CHANNEL; MECHANORECEPTORS; MEMBRANE POTENTIALS; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; NERVE FIBERS; NOCICEPTORS; PAIN; PAIN THRESHOLD; PATCH-CLAMP TECHNIQUES; PHYSICAL STIMULATION; POTASSIUM CHANNELS, CALCIUM-ACTIVATED; SENSORY RECEPTOR CELLS; SENSORY THRESHOLDS; SIGNAL TRANSDUCTION; TOUCH;

MLCS; MLOWN;

EID: 84876426861     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2012.12.035     Document Type: Article

References (56)

1. Abbas, N., Belghazi, M., Abdel-Mottaleb, Y., Tytgat, J., Bougis, P.E., and Martin-Eauclaire, M.F. (2008). A new Kaliotoxin selective towards Kv1.3 and Kv1.2 but not Kv1.1 channels expressed in oocytes. Biochem. Biophys. Res. Commun. 376, 525-530.
2. + channel involved in polymodal pain perception. EMBO J. 25, 2368-2376.
3. Babila, T., Moscucci, A., Wang, H., Weaver, F.E., and Koren, G. (1994). Assembly of mammalian voltage-gated potassium channels: evidence for an important role of the first transmembrane segment. Neuron 12, 615-626.
4. Bähring, R., Boland, L.M., Varghese, A., Gebauer, M., and Pongs, O. (2001). Kinetic analysis of open- and closed-state inactivation transitions in human Kv4.2 A-type potassium channels. J. Physiol. 535, 65-81.
5. Basbaum, A.I., Bautista, D.M., Scherrer, G., and Julius, D. (2009). Cellular and molecular mechanisms of pain. Cell 139, 267-284.
6. Belmonte, C., and Viana, F. (2008). Molecular and cellular limits to somatosensory specificity. Mol. Pain 4, 14.
7. Brew, H.M., Hallows, J.L., and Tempel, B.L. (2003). Hyperexcitability and reduced low threshold potassium currents in auditory neurons of mice lacking the channel subunit Kv1.1. J. Physiol. 548, 1-20.
8. Chalfie, M. (2009). Neurosensory mechanotransduction. Nat. Rev. Mol. Cell Biol. 10, 44-52.
9. + channels. Ann. N Y Acad. Sci. 868, 233-285.
10. Coste, B., Osorio, N., Padilla, F., Crest, M., and Delmas, P. (2004). Gating and modulation of presumptive NaV1.9 channels in enteric and spinal sensory neurons. Mol. Cell. Neurosci. 26, 123-134.
11. Coste, B., Crest, M., and Delmas, P. (2007). Pharmacological dissection and distribution of NaN/Nav1.9, T-type Ca2+ currents, and mechanically activated cation currents in different populations of DRG neurons. J. Gen. Physiol. 129, 57-77.
12. Coste, B., Mathur, J., Schmidt, M., Earley, T.J., Ranade, S., Petrus, M.J., Dubin, A.E., and Patapoutian, A. (2010). Piezo1 and Piezo2 are essential components of distinct mechanically activated cation channels. Science 330, 55-60.
13. Coste, B., Xiao, B., Santos, J.S., Syeda, R., Grandl, J., Spencer, K.S., Kim, S.E., Schmidt, M., Mathur, J., Dubin, A.E., et al. (2012). Piezo proteins are pore-forming subunits of mechanically activated channels. Nature 483, 176-181.
14. Delmas, P., Hao, J., and Rodat-Despoix, L. (2011). Molecular mechanisms of mechanotransduction in mammalian sensory neurons. Nat. Rev. Neurosci. 12, 139-153.
15. Drew, L.J., Wood, J.N., and Cesare, P. (2002). Distinct mechanosensitive properties of capsaicin-sensitive and -insensitive sensory neurons. J. Neurosci. 22, RC228.
16. Escoubas, P., Diochot, S., Célérier, M.L., Nakajima, T., and Lazdunski, M. (2002). Novel tarantula toxins for subtypes of voltage-dependent potassium channels in the Kv2 and Kv4 subfamilies. Mol. Pharmacol. 62, 48-57.
17. Ferber, M., Al-Sabi, A., Stocker, M., Olivera, B.M., and Terlau, H. (2004). Identification of a mammalian target of kappaM-conotoxin RIIIK. Toxicon 43, 915-921.
18. Giamarchi, A., Feng, S., Rodat-Despoix, L., Xu, Y., Bubenshchikova, E., Newby, L.J., Hao, J., Gaudioso, C., Crest, M., Lupas, A.N., et al. (2010). A polycystin-2 (TRPP2) dimerization domain essential for the function of heteromeric polycystin complexes. EMBO J. 29, 1176-1191.
19. Gillespie, P.G., and Müller, U. (2009). Mechanotransduction by hair cells: models, molecules, and mechanisms. Cell 139, 33-44.
20. Gittelman, J.X., and Tempel, B.L. (2006). Kv1.1-containing channels are critical for temporal precision during spike initiation. J. Neurophysiol. 96, 1203-1214.
21. Grissmer, S., Nguyen, A.N., Aiyar, J., Hanson, D.C., Mather, R.J., Gutman, G.A., Karmilowicz, M.J., Auperin, D.D., and Chandy, K.G. (1994). Pharmacological characterization of five cloned voltage-gated K+ channels, types Kv1.1, 1.2, 1.3, 1.5, and 3.1, stably expressed in mammalian cell lines. Mol. Pharmacol. 45, 1227-1234.
22. Gutman, G.A., Chandy, K.G., Adelman, J.P., Aiyar, J., Bayliss, D.A., Clapham, D.E., Covarriubias, M., Desir, G.V., Furuichi, K., Ganetzky, B., et al.; International Union of Pharmacology. (2003). International Union of Pharmacology. XLI. Compendium of voltage-gated ion channels: potassium channels. Pharmacol. Rev. 55, 583-586.
23. Haeberle, H., and Lumpkin, E.A. (2008). Merkel cells in somatosensation. Chem. Percept. 1, 110-118.
24. Hao, J., and Delmas, P. (2010). Multiple desensitization mechanisms of mechanotransducer channels shape firing of mechanosensory neurons. J. Neurosci. 30, 13384-13395.
25. Hao, J., and Delmas, P. (2011). Recording of mechanosensitive currents using piezoelectrically driven mechanostimulator. Nat. Protoc. 6, 979-990.
26. Harvey, A.L. (2001). Twenty years of dendrotoxins. Toxicon 39, 15-26.
27. Hatton, W.J., Mason, H.S., Carl, A., Doherty, P., Latten, M.J., Kenyon, J.L., Sanders, K.M., and Horowitz, B. (2001). Functional and molecular expression of a voltage-dependent K(+) channel (Kv1.1) in interstitial cells of Cajal. J. Physiol. 533, 315-327.
28. Honoré, E. (2007). The neuronal background K2P channels: focus on TREK1. Nat. Rev. Neurosci. 8, 251-261.
29. Hopkins, W.F. (1998). Toxin and subunit specificity of blocking affinity of three peptide toxins for heteromultimeric, voltage-gated potassium channels expressed in Xenopus oocytes. J. Pharmacol. Exp. Ther. 285, 1051-1060.
30. Hu, J., and Lewin, G.R. (2006). Mechanosensitive currents in the neurites of cultured mouse sensory neurones. J. Physiol. 577, 815-828.
31. Iggo, A., and Andres, K.H. (1982). Morphology of cutaneous receptors. Annu. Rev. Neurosci. 5, 1-31.
32. + channels. J. Biol. Chem. 283, 23026-23032.
33. Johansson, R.S., and Birznieks, I. (2004). First spikes in ensembles of human tactile afferents code complex spatial fingertip events. Nat. Neurosci. 7, 170-177.
34. Kawakubo, T., Naruse, K., Matsubara, T., Hotta, N., and Sokabe, M. (1999). Characterization of a newly found stretch-activated KCa,ATP channel in cultured chick ventricular myocytes. Am. J. Physiol. 276, H1827-H1838.
35. Kerstein, P.C., del Camino, D., Moran, M.M., and Stucky, C.L. (2009). Pharmacological blockade of TRPA1 inhibits mechanical firing in nociceptors. Mol. Pain 5, 19.
36. Li, L., Rutlin, M., Abraira, V.E., Cassidy, C., Kus, L., Gong, S., Jankowski, M.P., Luo, W., Heintz, N., Koerber, H.R., et al. (2011). The functional organization of cutaneous low-threshold mechanosensory neurons. Cell 147, 1615-1627.
37. Lumpkin, E.A., and Caterina, M.J. (2007). Mechanisms of sensory transduction in the skin. Nature 445, 858-865.
38. McCarter, G.C., and Levine, J.D. (2006). Ionic basis of a mechanotransduction current in adult rat dorsal root ganglion neurons. Mol. Pain 2, 28.
39. McCarter, G.C., Reichling, D.B., and Levine, J.D. (1999). Mechanical transduction by rat dorsal root ganglion neurons in vitro. Neurosci. Lett. 273, 179-182.
40. Morris, C.E. (2011). Voltage-gated channel mechanosensitivity: fact or friction? Front. Physiol. 2, 25.
41. Noël, J., Zimmermann, K., Busserolles, J., Deval, E., Alloui, A., Diochot, S., Guy, N., Borsotto, M., Reeh, P., Eschalier, A., and Lazdunski, M. (2009). The mechano-activated K+ channels TRAAK and TREK-1 control both warm and cold perception. EMBO J. 28, 1308-1318.
42. Noël, J., Sandoz, G., and Lesage, F. (2011). Molecular regulations governing TREK and TRAAK channel functions. Channels (Austin) 5, 402-409.
43. Padilla, F., Couble, M.L., Coste, B., Maingret, F., Clerc, N., Crest, M., Ritter, A.M., Magloire, H., and Delmas, P. (2007). Expression and localization of the Nav1.9 sodium channel in enteric neurons and in trigeminal sensory endings: implication for intestinal reflex function and orofacial pain. Mol. Cell. Neurosci. 35, 138-152.
44. Perl, E.R. (1996). Cutaneous polymodal receptors: characteristics and plasticity. Prog. Brain Res. 113, 21-37.
45. Persson, A.S., Klement, G., Almgren, M., Sahlholm, K., Nilsson, J., Petersson, S., Arhem, P., Schalling, M., and Lavebratt, C. (2005). A truncated Kv1.1 protein in the brain of the megencephaly mouse: expression and interaction. BMC Neurosci. 6, 65.
46. Petersson, S., Persson, A.S., Johansen, J.E., Ingvar, M., Nilsson, J., Klement, G., Arhem, P., Schalling, M., and Lavebratt, C. (2003). Truncation of the Shaker-like voltage-gated potassium channel, Kv1.1, causes megencephaly. Eur. J. Neurosci. 18, 3231-3240.
47. Rasband, M.N., Park, E.W., Vanderah, T.W., Lai, J., Porreca, F., and Trimmer, J.S. (2001). Distinct potassium channels on pain-sensing neurons. Proc. Natl. Acad. Sci. USA 98, 13373-13378.
48. Reeh, P.W. (1986). Sensory receptors in mammalian skin in an in vitro preparation. Neurosci. Lett. 66, 141-146.
49. Saal, H.P., Vijayakumar, S., and Johansson, R.S. (2009). Information about complex fingertip parameters in individual human tactile afferent neurons. J. Neurosci. 29, 8022-8031.
50. Schmidt, D., Jiang, Q.X., and MacKinnon, R. (2006). Phospholipids and the origin of cationic gating charges in voltage sensors. Nature 444, 775-779.
51. + channels. Proc. Natl. Acad. Sci. USA 109, 10352-10357.
52. Schulteis, C.T., Nagaya, N., and Papazian, D.M. (1998). Subunit folding and assembly steps are interspersed during Shaker potassium channel biogenesis. J. Biol. Chem. 273, 26210-26217.
53. Seal, R.P., Wang, X., Guan, Y., Raja, S.N., Woodbury, C.J., Basbaum, A.I., and Edwards, R.H. (2009). Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature 462, 651-655.
54. + currents yield pharmacologically distinguishable heteromers. Neuropharmacology 53, 272-282.
55. Vilceanu, D., and Stucky, C.L. (2010). TRPA1 mediates mechanical currents in the plasma membrane of mouse sensory neurons. PLoS ONE 5, e12177.
56. + channel subtypes fractionated from rat brain using dendrotoxins. Eur. J. Biochem. 263, 230-237.