Divalent cations activate TRPV1 through promoting conformational change of the extracellular region

Journal of General Physiology

Volumn 143, Issue 1, 2014, Pages 91-103

  Yang, Fan ^a   Ma, Linlin ^a,b   Cao, Xu ^a,c   Wang, KeWei ^c   Zheng, Jie ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DIVALENT CATION; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHANNEL GATING; CHEMISTRY; DRUG EFFECT; HEAT; HEK293 CELL LINE; HUMAN; METABOLISM; MOLECULAR GENETICS; MOUSE; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; CATIONS, DIVALENT; HEK293 CELLS; HOT TEMPERATURE; HUMANS; ION CHANNEL GATING; MICE; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, TERTIARY; TRPV CATION CHANNELS;

EID: 84891438325     PISSN: 00221295     EISSN: 15407748     Source Type: Journal    
DOI: 10.1085/jgp.201311024     Document Type: Article

References (44)

1. Ahern, G.P., I.M. Brooks, R.L. Miyares, and X.B. Wang. 2005. Extracellular cations sensitize and gate capsaicin receptor TRPV1 modulating pain signaling. J. Neurosci. 25:5109-5116. http://dx.doi.org/10.1523/JNEUROSCI.0237-05.2005
2. Ahern, G.P., X. Wang, and R.L. Miyares. 2006. Polyamines are potent ligands for the capsaicin receptor TRPV1. J. Biol. Chem. 281:8991-8995. http://dx.doi.org/10.1074/jbc. M513429200
3. Bezanilla, F. 2008. How membrane proteins sense voltage. Nat. Rev. Mol. Cell Biol. 9:323-332. http://dx.doi.org/10.1038/nrm2376
4. Boukalova, S., J. Teisinger, and V. Vlachova. 2013. Protons stabilize the closed conformation of gain-of-function mutants of the TRPV1 channel. Biochim. Biophys. Acta. 1833:520-528. http://dx.doi.org/10.1016/j.bbamcr.2012.11.017
5. Bykova, E.A., X.D. Zhang, T.Y. Chen, and J. Zheng. 2006. Large movement in the C terminus of CLC-0 chloride channel during slow gating. Nat. Struct. Mol. Biol. 13:1115-1119. http://dx.doi.org/10.1038/nsmb1176
6. Cao, X., L. Ma, F. Yang, K. Wang, and J. Zheng. 2013. Divalent cations potentiate TRPV1 channel by lowering the heat activation threshold. J. Gen. Physiol. 143:75-90.
7. Cheng, W., F. Yang, C.L. Takanishi, and J. Zheng. 2007. Thermosensitive TRPV channel subunits coassemble into heteromeric channels with intermediate conductance and gating properties. J. Gen. Physiol. 129:191-207. http://dx.doi.org/10.1085/jgp.200709731
8. Ciani, S., and B. Ribalet. 1988. Ion permeation and rectification in ATPsensitive channels from insulin-secreting cells (RINm5F): effects of K+, Na+ and Mg2+. J. Membr. Biol. 103:171-180. http://dx.doi.org/10.1007/BF01870947
9. Clapham, D.E., and C. Miller. 2011. A thermodynamic framework for understanding temperature sensing by transient receptor potential (TRP) channels. Proc. Natl. Acad. Sci. USA. 108:19492-19497. http://dx.doi.org/10.1073/pnas.1117485108
10. Cui, Y., F. Yang, X. Cao, V. Yarov-Yarovoy, K. Wang, and J. Zheng. 2012. Selective disruption of high sensitivity heat activation but not capsaicin activation of TRPV1 channels by pore turret mutations. J. Gen. Physiol. 139:273-283. http://dx.doi.org/10.1085/jgp.201110724
11. Erickson, M.G., B.A. Alseikhan, B.Z. Peterson, and D.T. Yue. 2001. Preassociation of calmodulin with voltage-gated Ca2+ channels revealed by FRET in single living cells. Neuron. 31:973-985. http://dx.doi.org/10.1016/S0896-6273(01)00438-X
12. Fersht, A. 1998. Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding. W.H. Freeman and Company, New York. 650 pp.
13. Grandl, J., S.E. Kim, V. Uzzell, B. Bursulaya, M. Petrus, M. Bandell, and A. Patapoutian. 2010. Temperature-induced opening of TRPV1 ion channel is stabilized by the pore domain. Nat. Neurosci. 13:708-714. http://dx.doi.org/10.1038/nn.2552
14. Gyires, K., and Z. Torma. 1984. The use of the writhing test in mice for screening different types of analgesics. Arch. Int. Pharmacodyn. Ther. 267:131-140.
15. Horie, M., H. Irisawa, and A. Noma. 1987. Voltage-dependent magnesium block of adenosine-triphosphate-sensitive potassium channel in guinea-pig ventricular cells. J. Physiol. 387:251-272.
16. Islas, L.D., and F.J. Sigworth. 2001. Electrostatics and the gating pore of Shaker potassium channels. J. Gen. Physiol. 117:69-90. http://dx.doi.org/10.1085/jgp.117.1.69
17. 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. http://dx.doi.org/10.1073/pnas.100129497
18. Lansman, J.B., P. Hess, and R.W. Tsien. 1986. Blockade of current through single calcium channels by Cd2+, Mg2+, and Ca2+. Voltage and concentration dependence of calcium entry into the pore. J. Gen. Physiol. 88:321-347. http://dx.doi.org/10.1085/jgp.88.3.321
19. Lee, S.Y., A. Banerjee, and R. MacKinnon. 2009. Two separate interfaces between the voltage sensor and pore are required for the function of voltage-dependent K+ channels. PLoS Biol. 7:e47. http://dx.doi.org/10.1371/journal.pbio.1000047
20. Long, S.B., E.B. Campbell, and R. Mackinnon. 2005. Crystal structure of a mammalian voltage-dependent Shaker family K+ channel. Science. 309:897-903. http://dx.doi.org/10.1126/science.1116269
21. Long, S.B., X. Tao, E.B. Campbell, and R. MacKinnon. 2007. Atomic structure of a voltage-dependent K+ channel in a lipid membrane-like environment. Nature. 450:376-382. http://dx.doi.org/10.1038/nature06265
22. Luebbert, M., D. Radtke, R. Wodarski, N. Damann, H. Hatt, and C.H. Wetzel. 2010. Direct activation of transient receptor potential V1 by nickel ions. Pflugers Arch. 459:737-750. http://dx.doi.org/10.1007/s00424-009-0782-8
23. Mogil, J.S., S.G. Wilson, K. Bon, S.E. Lee, K. Chung, P. Raber, J.O. Pieper, H.S. Hain, J.K. Belknap, L. Hubert, et al. 1999. Heritability of nociception I: responses of 11 inbred mouse strains on 12 measures of nociception. Pain. 80:67-82. http://dx.doi.org/10.1016/S0304-3959(98)00197-3
24. Moiseenkova-Bell, V.Y., L.A. Stanciu, I.I. Serysheva, B.J. Tobe, and T.G. Wensel. 2008. Structure of TRPV1 channel revealed by electron cryomicroscopy. Proc. Natl. Acad. Sci. USA. 105:7451-7455. http://dx.doi.org/10.1073/pnas.0711835105
25. Myers, B.R., C.J. Bohlen, and D. Julius. 2008. A yeast genetic screen reveals a critical role for the pore helix domain in TRP channel gating. Neuron. 58:362-373. http://dx.doi.org/10.1016/j.neuron.2008.04.012
26. Neyton, J., and C. Miller. 1988. Potassium blocks barium permeation through a calcium-activated potassium channel. J. Gen. Physiol. 92:549-567. http://dx.doi.org/10.1085/jgp.92.5.549
27. Nowak, L., P. Bregestovski, P. Ascher, A. Herbet, and A. Prochiantz. 1984. Magnesium gates glutamate-activated channels in mouse central neurones. Nature. 307:462-465. http://dx.doi.org/10.1038/307462a0
28. Ohta, T., T. Imagawa, and S. Ito. 2008. Novel gating and sensitizing mechanism of capsaicin receptor (TRPV1): tonic inhibitory regulation of extracellular sodium through the external protonation sites on TRPV1. J. Biol. Chem. 283:9377-9387. http://dx.doi.org/10.1074/jbc. M709377200
29. Piasta, K.N., D.L. Theobald, and C. Miller. 2011. Potassium-selective block of barium permeation through single KcsA channels. J. Gen. Physiol. 138:421-436. http://dx.doi.org/10.1085/jgp.201110684
30. Riera, C.E., H. Vogel, S.A. Simon, and J. le Coutre. 2007. Artificial sweeteners and salts producing a metallic taste sensation activate TRPV1 receptors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293:R626-R634. http://dx.doi.org/10.1152/ajpregu.00286.2007
31. Sigworth, F.J. 1994. Voltage gating of ion channels. Q. Rev. Biophys. 27:1-40. http://dx.doi.org/10.1017/S0033583500002894
32. Silverman, W.R., C.Y. Tang, A.F. Mock, K.B. Huh, and D.M. Papazian. 2000. Mg2+ modulates voltage-dependent activation in ether-à-go-go potassium channels by binding between transmembrane segments S2 and S3. J. Gen. Physiol. 116:663-678. http://dx.doi.org/10.1085/jgp.116.5.663
33. Takanishi, C.L., E.A. Bykova, W. Cheng, and J. Zheng. 2006. GFPbased FRET analysis in live cells. Brain Res. 1091:132-139. http://dx.doi.org/10.1016/j.brainres.2006.01.119
34. Tang, C.Y., F. Bezanilla, and D.M. Papazian. 2000. Extracellular Mg2+ modulates slow gating transitions and the opening of Drosophila ether-à-go-go potassium channels. J. Gen. Physiol. 115:319-338. http://dx.doi.org/10.1085/jgp.115.3.319
35. Terlau, H., J. Ludwig, R. Steffan, O. Pongs, W. Stühmer, and S.H. Heinemann. 1996. Extracellular Mg2+ regulates activation of rat eag potassium channel. Pflugers Arch. 432:301-312. http://dx.doi.org/10.1007/s004240050137
36. 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. http://dx.doi.org/10.1016/S0896-6273(00)80564-4
37. Tousova, K., L. Vyklicky, K. Susankova, J. Benedikt, and V. Vlachova. 2005. Gadolinium activates and sensitizes the vanilloid receptor TRPV1 through the external protonation sites. Mol. Cell. Neurosci. 30:207-217. http://dx.doi.org/10.1016/j.mcn.2005.07.004
38. 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. http://dx.doi.org/10.1038/nature02732
39. Wang, S., K. Poon, R.E. Oswald, and H.H. Chuang. 2010. Distinct modulations of human capsaicin receptor by protons and magnesium through different domains. J. Biol. Chem. 285:11547-11556. http://dx.doi.org/10.1074/jbc. M109.058727
40. Yang, F., Y. Cui, K. Wang, and J. Zheng. 2010. Thermosensitive TRP channel pore turret is part of the temperature activation pathway. Proc. Natl. Acad. Sci. USA. 107:7083-7088. http://dx.doi.org/10.1073/pnas.1000357107
41. Zheng, J. 2013a. Domain-domain interactions in ion channels. J. Gen. Physiol. 142:347-350. http://dx.doi.org/10.1085/jgp.201311090
42. Zheng, J. 2013b. Molecular mechanism of TRP channels. Compr Physiol. 3:221-242.
43. Zheng, J., and W.N. Zagotta. 2000. Gating rearrangements in cyclic nucleotide-gated channels revealed by patch-clamp fluorometry. Neuron. 28:369-374. http://dx.doi.org/10.1016/S0896-6273 (00)00117-3
44. Zheng, J., M.C. Trudeau, and W.N. Zagotta. 2002. Rod cyclic nucleotide-gated channels have a stoichiometry of three CNGA1 subunits and one CNGB1 subunit. Neuron. 36:891-896. http://dx.doi.org/10.1016/S0896-6273(02)01099-1