Voltage-and cold-dependent gating of single TRPM8 ion channels

Journal of General Physiology

Volumn 137, Issue 2, 2011, Pages 173-195

  Fernández, José A ^a   Skryma, Roman ^b   Bidaux, Gabriel ^b   Magleby, Karl L ^c   Scholfeld, C Norman ^a   McGeown, J Graham ^a   Prevarskaya, Natalia ^b   Zholos, Alexander V ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b Université des Sciences et Technologies de Lille   (France)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSIENT RECEPTOR POTENTIAL CHANNEL M; TRPM8 PROTEIN, HUMAN;

ARTICLE; CELL MEMBRANE POTENTIAL; CELL STRAIN HEK293; CHANNEL GATING; CHEMICAL PHENOMENA; HUMAN; KINETICS; PHYSIOLOGY; TEMPERATURE;

HEK293 CELLS; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; ION CHANNEL GATING; KINETICS; MEMBRANE POTENTIALS; TEMPERATURE; TRPM CATION CHANNELS;

EID: 79951632602     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201010498     Document Type: Article

References (61)

1. Andersson, D. A., M. Nash, and S. Bevan. 2007. Modulation of the cold-activated channel TRPM8 by lysophospholipids and polyunsaturated fatty acids. J. Neurosci. 27:3347-3355. doi:10.1523/JNEUROSCI.4846-06.2007 (Pubitemid 46474120)
2. Bautista, D. M., J. Siemens, J. M. Glazer, P. R. Tsuruda, A. I. Basbaum, C. L. Stucky, S. E. Jordt, and D. Julius. 2007. The menthol receptor TRPM8 is the principal detector of environmental cold. Nature. 448:204-208. doi:10.1038/nature05910 (Pubitemid 47067367)
3. Blatz, A. L., and K. L. Magleby. 1986. Correcting single channel data for missed events. Biophys. J. 49:967-980. doi:10.1016/S0006-3495 (86) 83725-0
4. Bödding, M., U. Wissenbach, and V. Flockerzi. 2007. Characterisation of TRPM8 as a pharmacophore receptor. Cell Calcium. 42:618-628. doi:10.1016/j.ceca.2007.03.005 (Pubitemid 47471362)
5. Brauchi, S., P. Orio, and R. Latorre. 2004. Clues to understanding cold sensation: thermodynamics and electrophysiological analysis of the cold receptor TRPM8. Proc. Natl. Acad. Sci. USA. 101:15494-15499. doi:10.1073/pnas.0406773101 (Pubitemid 39441569)
6. Brauchi, S., G. Orta, M. Salazar, E. Rosenmann, and R. Latorre. 2006. A hot-sensing cold receptor: C-terminal domain determines thermosensation in transient receptor potential channels. J. Neurosci. 26:4835-4840. doi:10.1523/JNEUROSCI.5080-05.2006 (Pubitemid 44315324)
7. Chuang, H. H., W. M. Neuhausser, and D. Julius. 2004. The supercooling agent icilin reveals a mechanism of coincidence detection by a temperature-sensitive TRP channel. Neuron. 43:859-869. doi:10.1016/j.neuron. 2004.08.038 (Pubitemid 39215016)
8. Colquhoun, D., and A. G. Hawkes. 1995. Stochastic interpretation of mechanisms. In Single-Channel Recording. B. Sakmann and E. Neher, editors. Plenum Press, New York. 397-482.
9. Colquhoun, D., and F. J. Sigworth. 1995. Fitting and statistical analysis of single-channel records. In Single-Channel Recording. B. Sakmann and E. Neher, editors. Plenum Press, New York. 483-587.
10. Colquhoun, D., C. J. Hatton, and A. G. Hawkes. 2003. The quality of maximum likelihood estimates of ion channel rate constants. J. Physiol. 547:699-728. doi:10.1113/jphysiol.2002.034165 (Pubitemid 36367358)
11. + channel. J. Gen. Physiol. 110:257-281. doi:10.1085/jgp. 110.3.257 (Pubitemid 27388118)
12. 2+ regulation of mslo large conductance Ca-activated K+ channels. J. Gen. Physiol. 109:647-673. doi:10.1085/jgp. 109.5.647 (Pubitemid 27212383)
13. Gil, Z., K. L. Magleby, and S. D. Silberberg. 2001. Two-dimensional kinetic analysis suggests nonsequential gating of mechanosensitive channels in Xenopus oocytes. Biophys. J. 81:2082-2099. doi:10.1016/S0006-3495 (01) 75857-2 (Pubitemid 32917158)
14. Hawkes, A. G., A. Jalali, and D. Colquhoun. 1990. The distributions of the apparent open times and shut times in a single channel record when brief events cannot be detected. Philos. Trans. R. Soc. Lond. A. 332:511-538. doi:10.1098/rsta.1990.0129
15. Hawkes, A. G., A. Jalali, and D. Colquhoun. 1992. Asymptotic distributions of apparent open times and shut times in a single channel record allowing for the omission of brief events. Philos. Trans. R. Soc. Lond. B Biol. Sci. 337:383-404. doi:10.1098/rstb.1992.0116
16. Horn, R., and K. Lange. 1983. Estimating kinetic constants from single channel data. Biophys. J. 43:207-223.
17. 2+. J. Gen. Physiol. 114:305-336. doi:10.1085/jgp. 114.2.305 (Pubitemid 29380156)
18. 2+ binding and channel opening in large conductance (BK) potassium channels. J. Gen. Physiol. 120:267-305. doi:10.1085/jgp. 20028605 (Pubitemid 35014730)
19. Jerng, H. H., M. Shahidullah, and M. Covarrubias. 1999. Inactivation gating of Kv4 potassium channels: molecular interactions involving the inner vestibule of the pore. J. Gen. Physiol. 113:641-660. doi:10.1085/jgp. 113.5.641
20. + channels must deactivate to recover from inactivation. Neuron. 12:819-829. doi:10.1016/0896-6273 (94) 90335-2 (Pubitemid 24126243)
21. Latorre, R., S. Brauchi, G. Orta, C. Zaelzer, and G. Vargas. 2007. ThermoTRP channels as modular proteins with allosteric gating. Cell Calcium. 42:427-438. doi:10.1016/j.ceca.2007.04.004 (Pubitemid 47264003)
22. Latorre, R., C. Zaelzer, and S. Brauchi. 2009. Structure-functional intimacies of transient receptor potential channels. Q. Rev. Biophys. 42:201-246. doi:10.1017/S0033583509990072
23. Liu, B., and F. Qin. 2005. Functional control of cold-and mentholsensitive TRPM8 ion channels by phosphatidylinositol 4,5-bisphosphate. J. Neurosci. 25:1674-1681. doi:10.1523/JNEUROSCI.3632-04.2005 (Pubitemid 40279272)
24. Liu, B., K. Hui, and F. Qin. 2003. Thermodynamics of heat activation of single capsaicin ion channels VR1. Biophys. J. 85:2988-3006. doi:10.1016/S0006-3495 (03) 74719-5 (Pubitemid 37345788)
25. Magleby, K. L., and L. Song. 1992. Dependency plots suggest the kinetic structure of ion channels. Proc. Biol. Sci. 249:133-142. doi:10.1098/rspb.1992. 0095
26. Mälkiä, A., R. Madrid, V. Meseguer, E. de la Peña, M. Valero, C. Belmonte, and F. Viana. 2007. Bidirectional shifts of TRPM8 channel gating by temperature and chemical agents modulate the cold sensitivity of mammalian thermoreceptors. J. Physiol. 581:155-174. doi:10.1113/jphysiol.2006. 123059 (Pubitemid 46712034)
27. Marks, T. N., and S. W. Jones. 1992. Calcium currents in the A7r5 smooth muscle-derived cell line. An allosteric model for calcium channel activation and dihydropyridine agonist action. J. Gen. Physiol. 99:367-390. doi:10.1085/jgp. 99.3.367
28. Matta, J. A., and G. P. Ahern. 2007. Voltage is a partial activator of rat thermosensitive TRP channels. J. Physiol. 585:469-482. doi:10.1113/jphysiol. 2007.144287 (Pubitemid 350193918)
29. + channels. Neuron. 12:301-315. doi:10.1016/0896-6273 (94) 90273-9
30. McKemy, D. D., W. M. Neuhausser, and D. Julius. 2002. Identifcation of a cold receptor reveals a general role for TRP channels in thermosensation. Nature. 416:52-58. doi:10.1038/nature719 (Pubitemid 34215395)
31. McManus, O. B., and K. L. Magleby. 1988. Kinetic states and modes of single large-conductance calcium-activated potassium channels in cultured rat skeletal muscle. J. Physiol. 402:79-120.
32. McManus, O. B., A. L. Blatz, and KL. Magleby. 1985. Inverse relationship of the durations of adjacent open and shut intervals for C1 and K channels. Nature. 317:625-627. doi:10.1038/317625a0 (Pubitemid 16222532)
33. Nilius, B., K. Talavera, G. Owsianik, J. Prenen, G. Droogmans, and T. Voets. 2005. Gating of TRP channels: a voltage connection? J. Physiol. 567:35-44. doi:10.1113/jphysiol.2005.088377 (Pubitemid 41167302)
34. Peier, A. M., A. Moqrich, A. C. Hergarden, AJ. Reeve, DA. Andersson, GM. Story, T. J. Earley, I. Dragoni, P. McIntyre, S. Bevan, and A. Patapoutian. 2002. A TRP channel that senses cold stimuli and menthol. Cell. 108:705-715. doi:10.1016/S0092-8674 (02) 00652-9 (Pubitemid 34241429)
35. Qin, F. 2004. Restoration of single-channel currents using the segmental k-means method based on hidden Markov modeling. Biophys. J. 86:1488-1501. doi:10.1016/S0006-3495 (04) 74217-4 (Pubitemid 38295584)
36. Qin, F., A. Auerbach, and F. Sachs. 1996. Estimating single-channel kinetic parameters from idealized patch-clamp data containing missed events. Biophys. J. 70:264-280. doi:10.1016/S0006-3495 (96) 79568-1 (Pubitemid 26021465)
37. Qin, F, A. Auerbach, and F. Sachs. 1997. Maximum likelihood estimation of aggregated Markov processes. Proc. Biol. Sci. 264:375-383. doi:10.1098/rspb. 1997.0054 (Pubitemid 27144045)
38. Ríos, E., M. Karhanek, J. Ma, and A. González. 1993. An allosteric model of the molecular interactions of excitation-contraction coupling in skeletal muscle. J. Gen. Physiol. 102:449-481. doi:10.1085/jgp. 102.3.449 (Pubitemid 23307825)
39. 2 regulates the activation and desensitization of TRPM8 channels through the TRP domain. Nat. Neurosci. 8:626-634. doi: 10.1038/nn 1451 (Pubitemid 40594204)
40. + channels suggests that the gating includes transitions through intermediate or secondary states. A mechanism for fickers. J. Gen. Physiol. 111:751-780. doi: 10.1085/jgp. 111.6.751 (Pubitemid 28265645)
41. 2+ suggest a two-tiered allosteric gating mechanism. J. Gen. Physiol. 114:93-124. doi:10.1085/jgp. 114.1.93 (Pubitemid 29323758)
42. + channels described by a two-tiered allosteric gating mechanism. J. Gen. Physiol. 116:75-99. doi:10.1085/jgp. 116.1.75 (Pubitemid 30456944)
43. Rothberg, B. S., RA. Bello, and KL. Magleby. 1997. Two-dimensional components and hidden dependencies provide insight into ion channel gating mechanisms. Biophys. J. 72:2524-2544. doi:10.1016/S0006-3495 (97) 78897-0 (Pubitemid 27227589)
44. Schoppa, N. E., K McCormack, MA. Tanouye, and F. J. Sigworth. 1992. The size of gating charge in wild-type and mutant Shaker potassium channels. Science. 255:1712-1715. doi:10.1126/science.1553560
45. Serrano, J. R., E. Perez-Reyes, and S. W. Jones. 1999. State-dependent inactivation of the a1G T-type calcium channel. J. Gen. Physiol. 114:185-201. doi:10.1085/jgp. 114.2.185 (Pubitemid 29380149)
46. Shelley, C., and KL. Magleby. 2008. Linking exponential components to kinetic states in Markov models for single-channel gating. J. Gen. Physiol. 132:295-312. doi:10.1085/jgp. 200810008
47. 2+. J. Gen. Physiol. 135:461-480. doi:10.1085/jgp. 200910331
48. Sigworth, F. J. 1994. Voltage gating of ion channels. Q. Rev. Biophys. 27:1-40. doi:10.1017/S0033583500002894 (Pubitemid 24280678)
49. Sigworth, F. J., and S. M. Sine. 1987. Data transformations for improved display and ftting of single-channel dwell time histograms. Biophys. J. 52:1047-1054. doi:10.1016/S0006-3495 (87) 83298-8
50. Studer, M., and P. A. McNaughton. 2010. Modulation of single-channel properties of TRPV1 by phosphorylation. J. Physiol. 588:3743-3756. doi:10.1113/jphysiol.2010.190611
51. Tsvilovskyy, V. V., A. V. Zholos, T. Aberle, S. E. Philipp, A. Dietrich, M. X. Zhu, L. Birnbaumer, M. Freichel, and V. Flockerzi. 2009. Deletion of TRPC4 and TRPC6 in mice impairs smooth muscle contraction and intestinal motility in vivo. Gastroenterology. 137:1415-1424. doi:10.1053/j.gastro.2009.06.046
52. 2-dependent gating of TRPM8 by lysophospholipids. J. Biol. Chem. 281:40174-40182. doi:10.1074/jbc. M605779200 (Pubitemid 44537031)
53. Venkatachalam, K., and C. Montell. 2007. TRP channels. Annu. Rev. Biochem. 76:387-417. doi:10.1146/annurev. biochem.75.103004.142819
54. Voets, T., G. Droogmans, U. Wissenbach, A. Janssens, V. Flockerzi, and B. Nilius. 2004. The principle of temperature-dependent gating in cold-and heat-sensitive TRP channels. Nature. 430:748-754. doi:10.1038/nature02732 (Pubitemid 39071340)
55. Voets, T., G. Owsianik, A. Janssens, K. Talavera, and B. Nilius. 2007. TRPM8 voltage sensor mutants reveal a mechanism for integrating thermal and chemical stimuli. Nat. Chem. Biol. 3:174-182. doi:10.1038/nchembio862
56. Weiss, D. S., and K. L. Magleby. 1992. Voltage-dependent gating mechanism for single fast chloride channels from rat skeletal muscle. J. Physiol. 453:279-306.
57. + channels. J. Physiol. 582:1059-1072. doi:10.1113/jphysiol.2007.131490 (Pubitemid 47104340)
58. Yao, J., B. Liu, and F. Qin. 2010. Kinetic and energetic analysis of thermally activated TRPV1 channels. Biophys. J. 99:1743-1753. doi:10.1016/j.bpj.2010.07.022
59. Zakharian, E., C. Cao, and T. Rohacs. 2010. Gating of transient receptor potential melastatin 8 (TRPM8) channels activated by cold and chemical agonists in planar lipid bilayers. J. Neurosci. 30:12526-12534. doi:10.1523/JNEUROSCI. 3189-10.2010
60. Zholos, A. V., A. A. Zholos, and T. B. Bolton. 2004. G-protein-gated TRP-like cationic channel activated by muscarinic receptors: effect of potential on single-channel gating. J. Gen. Physiol. 123:581-598. doi:10.1085/jgp. 200309002 (Pubitemid 38590860)
61. Zhu, M. X. 2007. Understanding the role of voltage gating of polymodal TRP channels. J. Physiol. 585:321-322. doi:10.1113/jphysiol.2007.147082 (Pubitemid 350193907)