Structural insights into the gating mechanisms of TRPV channels

Cell Calcium - Tập 87 - Trang 102168 - 2020
Ruth A. Pumroy1, Edwin C. Fluck1, Tofayel Ahmed1, Vera Y. Moiseenkova-Bell1
1Department of Systems Pharmacology and Translational Therapeutics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, 19104, USA

Tài liệu tham khảo

Nilius, 2011, The transient receptor potential family of ion channels, Genome Biol., 12, 218, 10.1186/gb-2011-12-3-218 Samanta, 2018, Transient receptor potential (TRP) channels, Subcell. Biochem., 87, 141, 10.1007/978-981-10-7757-9_6 Madej, 2018, Dawning of a new era in TRP channel structural biology by cryo-electron microscopy, Pflugers Arch., 470, 213, 10.1007/s00424-018-2107-2 Caterina, 1997, The capsaicin receptor: a heat-activated ion channel in the pain pathway, Nature, 389, 816, 10.1038/39807 Smith, 2002, TRPV3 is a temperature-sensitive vanilloid receptor-like protein, Nature, 418, 186, 10.1038/nature00894 Xu, 2002, TRPV3 is a calcium-permeable temperature-sensitive cation channel, Nature, 418, 181, 10.1038/nature00882 Strotmann, 2000, OTRPC4, a nonselective cation channel that confers sensitivity to extracellular osmolarity, Nat. Cell Biol., 2, 695, 10.1038/35036318 Liedtke, 2000, Vanilloid receptor–Related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor, Cell, 103, 525, 10.1016/S0092-8674(00)00143-4 Kanzaki, 1999, Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I, Nat. Cell Biol., 1, 165, 10.1038/11086 Caterina, 1999, A capsaicin-receptor homologue with a high threshold for noxious heat, Nature, 398, 436, 10.1038/18906 Patapoutian, 2003, ThermoTRP channels and beyond: mechanisms of temperature sensation, Nat. Rev. Neurosci., 4, 529, 10.1038/nrn1141 van Goor, 2017, TRP channels in calcium homeostasis: from hormonal control to structure-function relationship of TRPV5 and TRPV6, Biochim. Biophys. Acta. Mol. Cell Res., 1864, 883, 10.1016/j.bbamcr.2016.11.027 Peng, 2011, TRPV5 and TRPV6 in transcellular Ca(2+) transport: regulation, gene duplication, and polymorphisms in African populations, Adv. Exp. Med. Biol., 704, 239, 10.1007/978-94-007-0265-3_14 Park, 2011, TRP vanilloid 2 knock-out mice are susceptible to perinatal lethality but display normal thermal and mechanical nociception, J. Neurosci., 31, 11425, 10.1523/JNEUROSCI.1384-09.2011 Huang, 2011, TRPV3 and TRPV4 ion channels are not major contributors to mouse heat sensation, Mol. Pain, 7, 37, 10.1186/1744-8069-7-37 Montell, 2005, The TRP superfamily of cation channels, Sci. STKE, 2005, 10.1126/stke.2722005re3 Dang, 2019, Structural insight into TRPV5 channel function and modulation, Proc. Natl. Acad. Sci. U. S. A., 116, 8869, 10.1073/pnas.1820323116 Singh, 2018, Mechanism of calmodulin inactivation of the calcium-selective TRP channel TRPV6, Sci. Adv., 4, 10.1126/sciadv.aau6088 Hughes, 2018, Structural insights on TRPV5 gating by endogenous modulators, Nat. Commun., 9, 4198, 10.1038/s41467-018-06753-6 de Groot, 2011, Molecular mechanisms of calmodulin action on TRPV5 and modulation by parathyroid hormone, Mol. Cell. Biol., 31, 2845, 10.1128/MCB.01319-10 Lau, 2012, Distinct properties of Ca2+-calmodulin binding to N- and C-terminal regulatory regions of the TRPV1 channel, J. Gen. Physiol., 140, 541, 10.1085/jgp.201210810 Bokhovchuk, 2018, The structural basis of calcium-dependent inactivation of the transient receptor potential vanilloid 5 channel, Biochemistry, 57, 2623, 10.1021/acs.biochem.7b01287 Bate, 2018, A novel mechanism for calmodulin-dependent inactivation of transient receptor potential vanilloid 6, Biochemistry, 57, 2611, 10.1021/acs.biochem.7b01286 Kovalevskaya, 2012, The TRPV5/6 calcium channels contain multiple calmodulin binding sites with differential binding properties, J. Struct. Funct. Genomics, 13, 91, 10.1007/s10969-012-9128-4 Cuajungco, 2006, PACSINs bind to the TRPV4 cation channel. PACSIN 3 modulates the subcellular localization of TRPV4, J. Biol. Chem., 281, 18753, 10.1074/jbc.M602452200 D’Hoedt, 2008, Stimulus-specific modulation of the cation channel TRPV4 by PACSIN 3, J. Biol. Chem., 283, 6272, 10.1074/jbc.M706386200 Goretzki, 2018, Structural basis of TRPV4 N terminus interaction with Syndapin/PACSIN1-3 and PIP2, Structure, 26, 1583, 10.1016/j.str.2018.08.002 Cao, 2013, Interplay between calmodulin and phosphatidylinositol 4,5-bisphosphate in Ca2+-induced inactivation of transient receptor potential vanilloid 6 channels, J. Biol. Chem., 288, 5278, 10.1074/jbc.M112.409482 Rohacs, 2007, Regulation of transient receptor potential (TRP) channels by phosphoinositides, Pflugers Arch., 455, 157, 10.1007/s00424-007-0275-6 Rohacs, 2015, Phosphoinositide regulation of TRPV1 revisited, Pflugers Arch., 467, 1851, 10.1007/s00424-015-1695-3 Rohacs, 2014, Phosphoinositide regulation of TRP channels, Handb. Exp. Pharmacol., 223, 1143, 10.1007/978-3-319-05161-1_18 Lukacs, 2007, Dual regulation of TRPV1 by phosphoinositides, J. Neurosci., 27, 7070, 10.1523/JNEUROSCI.1866-07.2007 Klein, 2008, Determinants of molecular specificity in phosphoinositide regulation. Phosphatidylinositol (4,5)-bisphosphate (PI(4,5)P2) is the endogenous lipid regulating TRPV1, J. Biol. Chem., 283, 26208, 10.1074/jbc.M801912200 Cao, 2013, TRPV1 channels are intrinsically heat sensitive and negatively regulated by phosphoinositide lipids, Neuron, 77, 667, 10.1016/j.neuron.2012.12.016 Prescott, 2003, A modular PIP2 binding site as a determinant of capsaicin receptor sensitivity, Science, 300, 1284, 10.1126/science.1083646 Chuang, 2001, Bradykinin and nerve growth factor release the capsaicin receptor from PtdIns(4,5)P2-mediated inhibition, Nature, 411, 957, 10.1038/35082088 Mercado, 2010, Ca2+-dependent desensitization of TRPV2 channels is mediated by hydrolysis of phosphatidylinositol 4,5-bisphosphate, J. Neurosci., 30, 13338, 10.1523/JNEUROSCI.2108-10.2010 Doerner, 2011, Voltage- and temperature-dependent activation of TRPV3 channels is potentiated by receptor-mediated PI(4,5)P2 hydrolysis, J. Gen. Physiol., 137, 271, 10.1085/jgp.200910388 Harraz, 2018, PIP2 depletion promotes TRPV4 channel activity in mouse brain capillary endothelial cells, Elife, 7 Takahashi, 2014, TRPV4 channel activity is modulated by direct interaction of the ankyrin domain to PI(4,5)P(2), Nat. Commun., 5, 4994, 10.1038/ncomms5994 Garcia-Elias, 2013, Phosphatidylinositol-4,5-biphosphate-dependent rearrangement of TRPV4 cytosolic tails enables channel activation by physiological stimuli, Proc. Natl. Acad. Sci. U. S. A., 110, 9553, 10.1073/pnas.1220231110 Saha, 2017, Preferential selection of Arginine at the lipid-water-interface of TRPV1 during vertebrate evolution correlates with its snorkeling behaviour and cholesterol interaction, Sci. Rep., 7, 16808, 10.1038/s41598-017-16780-w Szoke, 2010, Effect of lipid raft disruption on TRPV1 receptor activation of trigeminal sensory neurons and transfected cell line, Eur. J. Pharmacol., 628, 67, 10.1016/j.ejphar.2009.11.052 Liu, 2006, TRPV1, but not P2X, requires cholesterol for its function and membrane expression in rat nociceptors, Eur. J. Neurosci., 24, 1, 10.1111/j.1460-9568.2006.04889.x Morales-Lazaro, 2019, Cholesterol as a key molecule that regulates TRPV1 channel function, Adv. Exp. Med. Biol., 1135, 105, 10.1007/978-3-030-14265-0_6 Liu, 2003, Thermodynamics of heat activation of single capsaicin ion channels VR1, Biophys. J., 85, 2988, 10.1016/S0006-3495(03)74719-5 Jansson, 2013, Effect of cholesterol depletion on the pore dilation of TRPV1, Mol. Pain, 9, 1, 10.1186/1744-8069-9-1 Picazo-Juarez, 2011, Identification of a binding motif in the S5 helix that confers cholesterol sensitivity to the TRPV1 ion channel, J. Biol. Chem., 286, 24966, 10.1074/jbc.M111.237537 Klein, 2014, Cholesterol sensitises the transient receptor potential channel TRPV3 to lower temperatures and activator concentrations, Cell Calcium, 55, 59, 10.1016/j.ceca.2013.12.001 Colton, 2007, 2-Aminoethoxydiphenyl borate as a common activator of TRPV1, TRPV2, and TRPV3 channels, Handb. Exp. Pharmacol., 173, 10.1007/978-3-540-34891-7_10 Singh, 2018, Structural bases of TRP channel TRPV6 allosteric modulation by 2-APB, Nat. Commun., 9, 2465, 10.1038/s41467-018-04828-y Gao, 2016, Selective potentiation of 2-APB-induced activation of TRPV1-3 channels by acid, Sci. Rep., 6, 20791, 10.1038/srep20791 De Petrocellis, 2012, Cannabinoid actions at TRPV channels: effects on TRPV3 and TRPV4 and their potential relevance to gastrointestinal inflammation, Acta Physiol. Oxf., 204, 255, 10.1111/j.1748-1716.2011.02338.x Qin, 2008, TRPV2 is activated by cannabidiol and mediates CGRP release in cultured rat dorsal root ganglion neurons, J. Neurosci., 28, 6231, 10.1523/JNEUROSCI.0504-08.2008 Smart, 2000, The endogenous lipid anandamide is a full agonist at the human vanilloid receptor (hVR1), Br. J. Pharmacol., 129, 227, 10.1038/sj.bjp.0703050 Muller, 2018, Cannabinoid ligands targeting TRP channels, Front. Mol. Neurosci., 11, 487, 10.3389/fnmol.2018.00487 Hughes, 2018, Structural basis of TRPV5 channel inhibition by econazole revealed by cryo-EM, Nat. Struct. Mol. Biol., 25, 53, 10.1038/s41594-017-0009-1 Sanchez-Moreno, 2018, Irreversible temperature gating in trpv1 sheds light on channel activation, Elife, 7, 10.7554/eLife.36372 Luo, 2019, Molecular basis for heat desensitization of TRPV1 ion channels, Nat. Commun., 10, 2134, 10.1038/s41467-019-09965-6 Leffler, 2007, A high-threshold heat-activated channel in cultured rat dorsal root ganglion neurons resembles TRPV2 and is blocked by gadolinium, Eur. J. Neurosci., 26, 12, 10.1111/j.1460-9568.2007.05643.x Fricke, 2019, Oxidation of methionine residues activates the high-threshold heat-sensitive ion channel TRPV2, Proc. Natl. Acad. Sci. U. S. A., 116, 24359, 10.1073/pnas.1904332116 Liu, 2016, Use dependence of heat sensitivity of vanilloid receptor TRPV2, Biophys. J., 110, 1523, 10.1016/j.bpj.2016.03.005 Chung, 2004, 2-aminoethoxydiphenyl borate activates and sensitizes the heat-gated ion channel TRPV3, J. Neurosci., 24, 5177, 10.1523/JNEUROSCI.0934-04.2004 Liu, 2011, Hysteresis of gating underlines sensitization of TRPV3 channels, J. Gen. Physiol., 138, 509, 10.1085/jgp.201110689 Phelps, 2010, Differential regulation of TRPV1, TRPV3, and TRPV4 sensitivity through a conserved binding site on the ankyrin repeat domain, J. Biol. Chem., 285, 731, 10.1074/jbc.M109.052548 Moiseenkova-Bell, 2009, Hot on the trail of TRP channel structure, J. Gen. Physiol., 133, 239, 10.1085/jgp.200810123 Jin, 2006, Structure of the N-terminal ankyrin repeat domain of the TRPV2 ion channel, J. Biol. Chem., 281, 25006, 10.1074/jbc.C600153200 McCleverty, 2006, Crystal structure of the human TRPV2 channel ankyrin repeat domain, Protein Sci., 15, 2201, 10.1110/ps.062357206 Lishko, 2007, The ankyrin repeats of TRPV1 bind multiple ligands and modulate channel sensitivity, Neuron, 54, 905, 10.1016/j.neuron.2007.05.027 Phelps, 2008, Structural analyses of the ankyrin repeat domain of TRPV6 and related TRPV ion channels, Biochemistry, 47, 2476, 10.1021/bi702109w Landoure, 2010, Mutations in TRPV4 cause Charcot-Marie-Tooth disease type 2C, Nat. Genet., 42, 170, 10.1038/ng.512 Inada, 2012, Structural and biochemical consequences of disease-causing mutations in the ankyrin repeat domain of the human TRPV4 channel, Biochemistry, 51, 6195, 10.1021/bi300279b Shi, 2013, Crystal structure of the N-terminal ankyrin repeat domain of TRPV3 reveals unique conformation of finger 3 loop critical for channel function, Protein Cell, 4, 942, 10.1007/s13238-013-3091-0 Moiseenkova-Bell, 2008, Structure of TRPV1 channel revealed by electron cryomicroscopy, Proc. Natl. Acad. Sci. U. S. A., 105, 7451, 10.1073/pnas.0711835105 Liao, 2013, Structure of the TRPV1 ion channel determined by electron cryo-microscopy, Nature, 504, 107, 10.1038/nature12822 Cao, 2013, TRPV1 structures in distinct conformations reveal activation mechanisms, Nature, 504, 113, 10.1038/nature12823 Hellmich, 2014, Structural biology of TRP channels, Handb. Exp. Pharmacol., 223, 963, 10.1007/978-3-319-05161-1_10 Gao, 2016, TRPV1 structures in nanodiscs reveal mechanisms of ligand and lipid action, Nature, 534, 347, 10.1038/nature17964 Zubcevic, 2016, Cryo-electron microscopy structure of the TRPV2 ion channel, Nat. Struct. Mol. Biol., 23, 180, 10.1038/nsmb.3159 Huynh, 2016, Structure of the full-length TRPV2 channel by cryo-EM, Nat. Commun., 7, 11130, 10.1038/ncomms11130 Zubcevic, 2018, Conformational plasticity in the selectivity filter of the TRPV2 ion channel, Nat. Struct. Mol. Biol., 25, 405, 10.1038/s41594-018-0059-z Zubcevic, 2019, Symmetry transitions during gating of the TRPV2 ion channel in lipid membranes, Elife, 8, 10.7554/eLife.45779 Pumroy, 2019, Molecular mechanism of TRPV2 channel modulation by cannabidiol, Elife, 8, 10.7554/eLife.48792 Dosey, 2019, Structures of TRPV2 in distinct conformations provide insight into role of the pore turret, Nat. Struct. Mol. Biol., 26, 40, 10.1038/s41594-018-0168-8 Zubcevic, 2018, Conformational ensemble of the human TRPV3 ion channel, Nat. Commun., 9, 4773, 10.1038/s41467-018-07117-w Singh, 2018, Structure and gating mechanism of the transient receptor potential channel TRPV3, Nat. Struct. Mol. Biol., 25, 805, 10.1038/s41594-018-0108-7 Zubcevic, 2019, Regulatory switch at the cytoplasmic interface controls TRPV channel gating, Elife, 8, 10.7554/eLife.47746 Singh, 2019, Structural basis of temperature sensation by the TRP channel TRPV3, Nat. Struct. Mol. Biol., 26, 994, 10.1038/s41594-019-0318-7 Deng, 2018, Cryo-EM and X-ray structures of TRPV4 reveal insight into ion permeation and gating mechanisms, Nat. Struct. Mol. Biol., 25, 252, 10.1038/s41594-018-0037-5 Hughes, 2019, Structure-based characterization of novel TRPV5 inhibitors, Elife, 8, 10.7554/eLife.49572 Saotome, 2016, Crystal structure of the epithelial calcium channel TRPV6, Nature, 534, 506, 10.1038/nature17975 Singh, 2017, Swapping of transmembrane domains in the epithelial calcium channel TRPV6, Sci. Rep., 7, 10669, 10.1038/s41598-017-10993-9 McGoldrick, 2018, Opening of the human epithelial calcium channel TRPV6, Nature, 553, 233, 10.1038/nature25182 Zheng, 2014, Structure and function of the thermoTRP channel pore, Curr. Top. Membr., 74, 233, 10.1016/B978-0-12-800181-3.00009-9 Munns, 2015, Role of the outer pore domain in transient receptor potential vanilloid 1 dynamic permeability to large cations, J. Biol. Chem., 290, 5707, 10.1074/jbc.M114.597435 van der Wijst, 2017, A gate hinge controls the epithelial calcium channel TRPV5, Sci. Rep., 7, 45489, 10.1038/srep45489 Jara-Oseguera, 2019, The ion selectivity filter is not an activation gate in TRPV1-3 channels, Elife, 8, 10.7554/eLife.51212 Zubcevic, 2019, The role of pi-helices in TRP channel gating, Curr. Opin. Struct. Biol., 58, 314, 10.1016/j.sbi.2019.06.011 Kasimova, 2018, Ion channel sensing: are fluctuations the crux of the matter?, J. Phys. Chem. Lett., 9, 1260, 10.1021/acs.jpclett.7b03396 Kasimova, 2018, A hypothetical molecular mechanism for TRPV1 activation that invokes rotation of an S6 asparagine, J. Gen. Physiol., 150, 1554, 10.1085/jgp.201812124 Nilius, 2003, The carboxyl terminus of the epithelial Ca(2+) channel ECaC1 is involved in Ca(2+)-dependent inactivation, Pflugers Arch., 445, 584, 10.1007/s00424-002-0923-9