Thermodynamics of Heat Activation of Single Capsaicin Ion Channels VR1

Biophysical Journal

Volumn 85, Issue 5, 2003, Pages 2988-3006

  Liu, Beiying ^a   Hui, Kwokyin ^b   Qin, Feng ^a,c  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSAICIN; CHOLESTEROL; ION CHANNEL; MEMBRANE LIPID; VANILLOID RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; AQUEOUS SOLUTION; ARTICLE; CHANNEL GATING; CONTROLLED STUDY; ELECTROPHYSIOLOGY; HEAT; HEAT SENSITIVITY; HIGH TEMPERATURE; HUMAN; HUMAN CELL; IONIC STRENGTH; NONHUMAN; PAIN RECEPTOR; RAT; TEMPERATURE DEPENDENCE; THERMODYNAMICS;

ANIMALIA;

EID: 0242385383     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(03)74719-5     Document Type: Article

References (66)

1. Anderson, C., S. Cull-Candy, and R. Miledi. 1977. Potential-dependent transition temperature of ionic channels induced by glutamate in locust muscle. Nature. 268:663-665.
2. Beam, K. G., and P. L. Donaldson. 1983. A quantitative study of potassium channel kinetics in rat skeletal muscle from 1 to 37°C. J. Gen. Physiol. 81:485-512.
3. Boheim, G., and R. Benz. 1978. Charge-pulse relaxation studies with lipid bilayer membranes modified by alamethicin. Biochim. Biophys. Acta. 507:262-270.
4. + channels and membrane fluidity in vascular smooth muscle cells. Pflugers Arch. 415:262-268.
5. Caterina, M. J., T. A. Rosen, M. Tominaga, A. J. Brake, and D. Julius. 1999. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature. 398:436-441.
6. Caterina, M. J., M. A. Schumacher, M. Tominaga, T. A. Rosen, J. D. Levine, and D. Julius. 1997. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature. 389:816-824.
7. Cesare, P., and P. McNaughton. 1996. A novel heat-activated current in nociceptive neurons and its sensitization by bradykinin. Proc. Natl. Acad. Sci. USA. 93:15435-15439.
8. Chang, H. M., R. Reitstetter, R. P. Mason, and R. Gruener. 1995. Attenuation of channel kinetics and conductance by cholesterol: an interpretation using structural stress as a unifying concept. J. Membr. Biol. 143:51-63.
9. Chiu, S. Y., H. E. Mrose, and J. M. Ritchie. 1979. Anomalous temperature dependence of the sodium conductance in rabbit nerve compared with frog nerve. Nature. 279:327-328.
10. Christian, A. E., M. P. Haynes, M. C. Phillips, and G. H. Rothblat. 1997. Use of cyclodextrins for manipulating cellular cholesterol content. J. Lipid Res. 38:2264-2272.
11. Conway, B. E. 1981. Ionic Hydration in Chemistry and Biophysics. Elsevier, Amsterdam, The Netherlands.
12. + currents in human neutrophils, rat alveolar epithelial cells, and mammalian phagocytes. J. Gen. Physiol. 112:503-522.
13. Forney, G. D. 1973. The Viterbi algorithm. Proc. IEEE. 61:268-278.
14. Garcia-Martinez, C., C. Morenilla-Palao, R. Planells-Cases, J. M. Merino, and A. Ferrer-Montiel. 2000. Identification of an aspartic residue in the P-loop of the vanilloid receptor that modulates pore properties. J. Biol. Chem. 275:32552-32558.
15. Gleason, M. M., M. S. Medow, and T. N. Tulenko. 1991. Excess membrane cholesterol alters calcium movements, cytosolic calcium levels, and membrane fluidity in arterial smooth muscle cells. Circ. Res. 69:216-227.
16. Guler, A. D., H. Lee, T. Iida, I. Shimizu, M. Tominaga, and M. Caterina. 2002. Heat-evoked activation of the ion channel, TRPV4. J. Neurosci. 22:6408-6414.
17. Gunthorpe, M. J., C. D. Benham, A. Randall, and J. B. Davis. 2002. The diversity in the vanilloid (TRPV) receptor family of ion channels. Trends Pharmacol. Sci. 23:183-191.
18. Hagen, S. J., J. Hofrichter, and W. A. Eaton. 1997. Rate of intrachain diffusion of unfolded cytochrome c. J. Phys. Chem. B. 101:2352-2365.
19. Hille, B. 2001. Ionic Channels of Excitable Membranes. Sinauer Associates, Sunderland, MA.
20. Hui, K. Y., B. Y. Liu, and F. Qin. 2003. Capsaicin activation of the pain receptor, VRI: multiple open states from both partial and full binding. Biophys. J. 84:2957-2968.
21. Jancso, N., A. Jancso-Gabor, and J. Szolcsanyi. 1967. Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br. J. Pharmacol. 31:138-151.
22. Jordt, S. E., and D. Julius. 2002. Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell. 108:421-430.
23. Jordt, S. E., M. Tominaga, and D. Julius. 2000. Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc. Natl. Acad. Sci. USA. 97:8134-8139.
24. Julius, D., and A. I. Basbaum. 2001. Molecular mechanisms of nociception. Nature. 413:203-210.
25. Jung, J., S. W. Hwang, J. Kwak, S. Y. Lee, C. J. Kang, W. B. Kim, D. Kim, and U. Oh. 1999. Capsaicin binds to the intracellular domain of the capsaicin-activated ion channel. J. Neurosci. 19:529-538.
26. Jung, J., S. Y. Lee, S. W. Hwang, H. Cho, J. Shin, Y. S. Kang, S. Kim, and U. Oh. 2002. Agonist recognition sites in the cytosolic tails of vanilloid receptor 1. J. Biol. Chem. 277:44448-44454.
27. Jurman, M. E., L. M. Boland, Y. Liu, and G. Yellen. 1994. Visual identification of individual transfected cells for electrophysiology using antibody-coated beads. Biotechniques. 17:876-881.
28. Kirsch, G. E., and J. S. Sykes. 1987. Temperature dependence of Na currents in rabbit and frog muscle membranes. J. Gen. Physiol. 89:239-251.
29. Kuzhikandathil, E. V., H. Wang, T. Szabo, N. Morozova, P. M. Blumberg, and G. S. Oxford. 2001. Functional analysis of capsaicin receptor (vanilloid receptor subtype 1) multimerization and agonist responsiveness using a dominant negative mutation. J. Neurosci. 21:8697-8706.
30. Kwak, J., M. H. Wang, S. W. Hwang, T. Y. Kim, S. Y. Lee, and U. Oh. 2000. Intracellular ATP increases capsaicin-activated channel activity by interacting with nucleotide-binding domains. J. Neurosci. 20:8298-8304.
31. +-channel properties in human T-lymphocytes. Biophys. J. 57:49-62.
32. Levitan, I., A. E. Christian, T. N. Tulenko, and G. H. Rothblat. 2000. Membrane cholesterol content modulates activation of volume-regulated anion current in bovine endothelial cells. J. Gen. Physiol. 115:405-416.
33. Lundbaek, J. A., P. Birn, J. Girshman, A. J. Hansen, and O. S. Andersen. 1996. Membrane stiffness and channel function. Biochemistry. 35:3825-3830.
34. McKemy, D. D., W. M. Neuhausser, and D. Julius. 2002. Identification of a cold receptor reveals a general role for TRP channels in thermosensation. Nature. 416:52-58.
35. McMullen, T. P. W., and R. N. McElhaney. 1996. Physical studies of cholesterol-phospholipid interactions. Curr. Opin. Colloid Interface Sci. 1:83-90.
36. Milburn, T., D. Saint, and S. Chung. 1995. The temperature dependence of conductance of the sodium channel: implications for mechanisms of ion permeation. Receptors Channels. 3:201-211.
37. Montell, C., L. Birnbaumer, V. Flockerzi, R. J. Bindels, E. A. Bruford, M. J. Caterina, D. E. Clapham, C. Harteneck, S. Heller, D. Julius, I. Kojima, Y. Mori, R. Penner, D. Prawitt, A. M. Scharenberg, G. Schultz, N. Shimizu, and M. X. Zhu. 2002. A unified nomenclature for the superfamily of TRP cation channels. Mol. Cell. 9:229-231.
38. Murrell-Lagnado, R. D., and R. W. Aldrich. 1993. Energetics of Shaker K channels block by inactivation peptides. J. Gen. Physiol. 102:977-1003.
39. Nagy, I., and H. P. Rang. 1999. Similarities and differences between the responses of rat sensory neurons to noxious heat and capsaicin. J. Neurosci. 19:10647-10655.
40. + channels is highly temperature dependent. Exp. Brain Res. 114:138-142.
41. Numazaki, M., T. Tominaga, H. Toyooka, and M. Tominaga. 2002. Direct phosphorylation of capsaicin receptor VR1 by protein kinase Cepsilon and identification of two target serine residues. J. Biol. Chem. 277:13375-13378.
42. Pace, C. N., B. A. Shirley, M. McNutt, and K. Gajiwala. 1996. Forces contributing to the conformational stability of proteins. FASEB J. 10:75-83.
43. Peier, A. M., A. Moqrich, A. C. Hergarden, A. J. Reeve, D. A. Andersson, G. M. Story, T. J. Earley, I. Dragoni, P. McIntyre, S. Bevan, and A. Patapoutian. 2002a. A TRP channel that senses cold stimuli and menthol. Cell. 108:705-715.
44. Peier, A. M., A. J. Reeve, D. A. Andersson, A. Moqrich, T. J. Earley, A. C. Hergarden, G. M. Story, S. Colley, J. B. Hogenesch, P. McIntyre, S. Bevan, and A. Patapoutian. 2002b. A heat-sensitive TRP channel expressed in keratinocytes. Science. 296:2046-2049.
45. Portman, J. J., S. Takada, and P. G. Wolynes. 2001. Microscopic theory of protein folding rates. I. Fine structure of the free energy profile and folding routes from a variational approach. J. Chem. Phys. 114:5069-5081.
46. Privalov, P. L. 1979. Stability of proteins: small globular proteins. Adv. Protein Chem. 33:167-241.
47. Pusch, M., U. Ludewig, and T. J. Jentsch. 1997. Temperature dependence of fast and slow gating relaxations of ClC-0 chloride channels. J. Gen. Physiol. 109:105-116.
48. 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.
49. Qin, F., A. Auerbach, and F. Sachs. 1997. Maximum likelihood estimation of aggregated Markov processes. Proc. R. Soc. Lond. 264:375-383.
50. Quartararo, N., and P. Barry. 1988. Ion permeation through single ACh-activated channels in denervated adult toad sartorius skeletal muscle fibres: effect of temperature. Pflugers Arch. 411:101-112.
51. Rabiner, L. R., J. G. Wilpon, and B. H. Juang. 1986. A segmental k-means training procedure for connected word recognition. AT&T Tech. ET J. 65:21-31.
52. Ryu, S. J., B. Y. Liu, and F. Qin. 2003. Low pH potentiates both capsaicin binding and channel gating of VR1 receptors. J. Gen. Physiol. 122:45-61.
53. Santiago, J., G. R. Guzman, L. V. Rojas, R. Marti, G. A. Asmar-Rovira, L. F. Santana, M. McNamee, and J. A. Lasalde-Dominicci. 2001. Probing the effects of membrane cholesterol in the Torpedo californica acetylcholine receptor and the novel lipid-exposed mutation alpha C418W in Xenopus oocytes. J. Biol. Chem. 276:46523-46532.
54. Sen, L., R. A. Bialecki, E. Smith, T. W. Smith, and W. S. Colucci. 1992. Cholesterol increases the L-type voltage-sensitive calcium channel current in arterial smooth muscle cells. Circ. Res. 71:1008-1014.
55. Smith, G. D., J. Gunthorpe, R. E. Kelsell, P. D. Hayes, P. Reilly, P. Facer, J. E. Wright, J. C. Jerman, J. P. Walhin, L. Ooi, J. Egerton, K. J. Charles, D. Smart, A. D. Randall, P. Anand, and J. B. Davis. 2002. TRPV3 is a temperature-sensitive vanilloid receptor-like protein. Nature. 418:186-190.
56. Story, G. M., A. M. Peier, A. J. Reeve, S. R. Eid, J. Mosbacher, T. R. Hricik, T. J. Earley, A. C. Hergarden, D. A. Andersson, S. W. Hwang, P. McIntyre, T. Jegla, S. Bevan, and A. Patapoutian. 2003. ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell. 112:819-829.
57. Szallasi, A., and P. M. Blumberg. 1999. Vanilloid (capsaicin) receptors and mechanisms. Pharmacol. Rev. 51:159-212.
58. Tominaga, M., M. J. Caterina, A. B. Malmberg, T. A. Rosen, H. Gilbert, K. Skinner, B. E. Raumann, A. I. Basbaum, and D. Julius. 1998. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron. 21:531-543.
59. Urry, D., S. Alonso-Romanowski, C. Venkatachalam, R. Bradley, and R. Harris. 1984. Temperature dependence of single channel currents and the peptide libration mechanism for ion transport through the gramicidin A transmembrane channel. J. Membr. Biol. 81:205-217.
60. Vlachova, V., A. Lyfenko, R. K. Orkand, and L. Vyklicky. 2001. The effects of capsaicin and acidity on currents generated by noxious heat in cultured neonatal rat dorsal root ganglion neurones. J. Physiol. 533:717-728.
61. Vlachova, V., J. Teisinger, K. Suankova, A. Lyfenko, R. Ettrich, and L. Vyklicky. 2003. Functional role of C-terminal cytoplasmic tail of rat vanilloid receptor 1. J. Neurosci, 23:1340-1350.
62. Vyklicky, L., V. Vlachova, Z. Vitaskova, I. Dittert, M. Kabat, and R. K. Orkand. 1999. Temperature coefficient of membrane currents induced by noxious heat in sensory neurones in the rat. J. Physiol. 517:181-192.
63. Welch, J. M., S. A. Simon, and P. H. Reinhart. 2000. The activation mechanism of rat vanilloid receptor 1 by capsaicin involves the pore domain and differs from the activation by either acid or heat. Proc. Natl. Acad. Sci. USA. 97:13889-13894.
64. Xu, H. X., I. S. Ramsey, S. A. Kotecha, M. M. Moran, J. H. A. Chong, D. Lawson, P. Ge, J. Lilly, I. Silos-Santiago, Y. Xie, P. S. Distefano, R. Curtis, and D. E. Clapham. 2002. TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature. 418:181-186.
65. Yang, W. Y., and M. Gruebele. 2003. Folding at the speed limit. Nature. 423:193-197.
66. Yeagle, P. L. 1985. Cholesterol and the cell membrane. Biochim. Biophys. Acta. 822:267-287.