Single Residues in the Outer Pore of TRPV1 and TRPV3 Have Temperature-Dependent Conformations

PLoS ONE

Volumn 8, Issue 3, 2013, Pages

  Kim, Sung Eun ^a   Patapoutian, Ardem ^a,b   Grandl, Jörg ^a,c  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Genomics Institute of Novartis Research Foundation (GNF)   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; VANILLOID RECEPTOR 1; VANILLOID RECEPTOR 3;

ARTICLE; CALCIUM TRANSPORT; CELL STRAIN HEK293; CHANNEL GATING; CHEMICAL LABELING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HIGH TEMPERATURE; LOW TEMPERATURE; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; RESIDUE ANALYSIS; SOLVENT EFFECT; TEMPERATURE DEPENDENCE;

AMINO ACID SEQUENCE; ANIMALS; CYSTEINE; ELECTROPHYSIOLOGICAL PROCESSES; EXTRACELLULAR SPACE; HEK293 CELLS; HUMANS; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; POROSITY; PROTEIN STRUCTURE, TERTIARY; RATS; SOLVENTS; TEMPERATURE; TRPV CATION CHANNELS;

EID: 84875455117     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0059593     Document Type: Article

References (32)

1. Dhaka A, Viswanath V, Patapoutian A, (2006) Trp ion channels and temperature sensation. Annu Rev Neurosci 29: 135-161.
2. Baez-Nieto D, Castillo JP, Dragicevic C, Alvarez O, Latorre R, (2011) Thermo-TRP channels: biophysics of polymodal receptors. Adv Exp Med Biol 704: 469-490.
3. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, et al. (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824.
4. Peier AM, Moqrich A, Hergarden AC, Reeve AJ, Andersson DA, et al. (2002) A TRP channel that senses cold stimuli and menthol. Cell 108: 705-715.
5. Bautista DM, Siemens J, Glazer JM, Tsuruda PR, Basbaum AI, et al. (2007) The menthol receptor TRPM8 is the principal detector of environmental cold. Nature 448: 204-208.
6. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, et al. (1998) The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21: 531-543.
7. Voets T, Droogmans G, Wissenbach U, Janssens A, Flockerzi V, et al. (2004) The principle of temperature-dependent gating in cold- and heat-sensitive TRP channels. Nature 430: 748-754.
8. Grandl J, Hu H, Bandell M, Bursulaya B, Schmidt M, et al. (2008) Pore region of TRPV3 ion channel is specifically required for heat activation. Nat Neurosci 11: 1007-1013.
9. Grandl J, Kim SE, Uzzell V, Bursulaya B, Petrus M, et al. (2010) Temperature-induced opening of TRPV1 ion channel is stabilized by the pore domain. Nat Neurosci 13: 708-714.
10. Kang K, Panzano VC, Chang EC, Ni L, Dainis AM, et al. (2012) Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481: 76-80.
11. Yao J, Liu B, Qin F, (2011) Modular thermal sensors in temperature-gated transient receptor potential (TRP) channels. Proc Natl Acad Sci U S A 108: 11109-11114.
12. Zhong L, Bellemer A, Yan H, Ken H, Jessica R, et al. (2012) Thermosensory and nonthermosensory isoforms of Drosophila melanogaster TRPA1 reveal heat-sensor domains of a thermoTRP Channel. Cell Rep 1: 43-55.
13. Cordero-Morales JF, Gracheva EO, Julius D, (2011) Cytoplasmic ankyrin repeats of transient receptor potential A1 (TRPA1) dictate sensitivity to thermal and chemical stimuli. Proc Natl Acad Sci U S A 108: E1184-E1191.
14. Wang H, Schupp M, Zurborg S, Heppenstall PA, (2013) Residues in the pore region of Drosophila transient receptor potential A1 dictate sensitivity to thermal stimuli. J Physiol 591: 185-201.
15. Yang F, Cui Y, Wang K, Zheng J, (2010) Thermosensitive TRP channel pore turret is part of the temperature activation pathway. Proc Natl Acad Sci U S A 107: 7083-7088.
16. Chung MK, Guler AD, Caterina MJ, (2005) Biphasic currents evoked by chemical or thermal activation of the heat-gated ion channel, TRPV3. J Biol Chem 280: 15928-15941.
17. Chung MK, Guler AD, Caterina MJ, (2008) TRPV1 shows dynamic ionic selectivity during agonist stimulation. Nat Neurosci 11: 555-564.
18. Salazar H, Llorente I, Jara-Oseguera A, Garcia-Villegas R, Munari M, et al. (2008) A single N-terminal cysteine in TRPV1 determines activation by pungent compounds from onion and garlic. Nat Neurosci 11: 255-261.
19. Akabas MH, Stauffer DA, Xu M, Karlin A, (1992) Acetylcholine receptor channel structure probed in cysteine-substitution mutants. Science 258: 307-310.
20. Jordt SE, Tominaga M, Julius D, (2000) Acid potentiation of the capsaicin receptor determined by a key extracellular site. Proc Natl Acad Sci U S A 97: 8134-8139.
21. Salazar H, Jara-Oseguera A, Hernandez-Garcia E, Llorente I, Arias OII, et al. (2009) Structural determinants of gating in the TRPV1 channel. Nat Struct Mol Biol 16: 704-710.
22. Yao J, Liu B, Qin F (2010) Pore turret of thermal TRP channels is not essential for temperature sensing. Proc Natl Acad Sci U S A 107: E125; author reply E126-E127.
23. Cui Y, Yang F, Cao X, Yarov-Yarovoy V, Wang K, et al. (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.
24. Clapham DE, Miller C, (2011) A thermodynamic framework for understanding temperature sensing by transient receptor potential (TRP) channels. Proc Natl Acad Sci U S A 108: 19492-19497.
25. Latorre R, Brauchi S, Orta G, Zaelzer C, Vargas G, (2007) ThermoTRP channels as modular proteins with allosteric gating. Cell Calcium 42: 427-438.
26. Bhave G, Zhu W, Wang H, Brasier DJ, Oxford GS, et al. (2002) cAMP-dependent protein kinase regulates desensitization of the capsaicin receptor (VR1) by direct phosphorylation. Neuron 35: 721-731.
27. Xu H, Ramsey IS, Kotecha SA, Moran MM, Chong JA, et al. (2002) TRPV3 is a calcium-permeable temperature-sensitive cation channel. Nature 418: 181-186.
28. Peier AM, Reeve AJ, Andersson DA, Moqrich A, Earley TJ, et al. (2002) A heat-sensitive TRP channel expressed in keratinocytes. Science 296: 2046-2049.
29. Aneiros E, Cao L, Papakosta M, Stevens EB, Phillips S, et al. (2011) The biophysical and molecular basis of TRPV1 proton gating. EMBO J 30: 994-1002.
30. Aghajanian S, Hovsepyan M, Geoghegan KF, Chrunyk BA, Engel PC, (2003) A thermally sensitive loop in clostridial glutamate dehydrogenase detected by limited proteolysis. J Biol Chem 278: 1067-1074.
31. Nelson SW, Iancu CV, Choe JY, Honzatko RB, Fromm HJ, (2000) Tryptophan fluorescence reveals the conformational state of a dynamic loop in recombinant porcine fructose-1,6-bisphosphatase. Biochemistry 39: 11100-11106.
32. Jung Y, Bayley H, Movileanu L, (2006) Temperature-responsive protein pores. J Am Chem Soc 128: 15332-15340.