How lipids contribute to ion channel function, a fat perspective on direct and indirect interactions

Harayama, 2018, Understanding the diversity of membrane lipid composition, Nat Rev Mol Cell Biol, 1842, 1 Singer, 1972, The fluid mosaic model of the structure of cell membranes, Science, 175, 720, 10.1126/science.175.4023.720 Goñi, 2014, The basic structure and dynamics of cell membranes: an update of the Singer–Nicolson model, BBA Biomembr, 1838, 1467, 10.1016/j.bbamem.2014.01.006 Nielsen, 1998, Energetics of inclusion-induced bilayer deformations, Biophys J, 74, 1966, 10.1016/S0006-3495(98)77904-4 Barden, 2016, n-3 Fatty acid supplementation and proresolving mediators of inflammation, Curr Opin Lipidol, 27, 26, 10.1097/MOL.0000000000000262 Rawicz, 2000, Effect of chain length and unsaturation on elasticity of lipid bilayers, Biophys J, 79, 328, 10.1016/S0006-3495(00)76295-3 Rajamoorthi, 2005, Packing and viscoelasticity of polyunsaturated ω-3 and ω-6 lipid bilayers as seen by 2H NMR and X-ray diffraction, J Am Chem Soc, 127, 1576, 10.1021/ja046453b Dennis, 1991, Role of phospholipase in generating lipid second messengers in signal transduction, FASEB J, 5, 2068, 10.1096/fasebj.5.7.1901288 Khan, 1995, Arachidonic acid and free fatty acids as second messengers and the role of protein kinase C, Cell Signal, 7, 171, 10.1016/0898-6568(94)00089-T Elinder, 2017, Actions and mechanisms of polyunsaturated fatty acids on voltage-gated ion channels, Front Physiol, 8, 10, 10.3389/fphys.2017.00043 Bruno, 2007, Docosahexaenoic acid alters bilayer elastic properties, Proc Natl Acad Sci U S A, 104, 9638, 10.1073/pnas.0701015104 Hardie, 2012, Photomechanical responses in Drosophila photoreceptors, Science, 338, 260, 10.1126/science.1222376 Charalambous, 2012, Engineering de novo membrane-mediated protein–protein communication networks, J Am Chem Soc, 134, 5746, 10.1021/ja300523q Vasquez, 2014, Phospholipids that contain polyunsaturated fatty acids enhance neuronal cell mechanics and touch sensation, Cell Rep, 6, 70, 10.1016/j.celrep.2013.12.012 Caires, 2017, Omega-3 fatty acids modulate TRPV4 function through plasma membrane remodeling, Cell Rep, 21, 246, 10.1016/j.celrep.2017.09.029 Teng, 2015, The force-from-lipid (FFL) principle of mechanosensitivity, at large and in elements, Pflugers Arch, 467, 27, 10.1007/s00424-014-1530-2 Martinac, 1987, Pressure-sensitive ion channel in Escherichia coli, Proc Natl Acad Sci U S A, 84, 2297, 10.1073/pnas.84.8.2297 Paoletti, 2013, NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease, Nat Rev Neurosci, 10.1038/nrn3504 Miller, 1992, Potentiation of NMDA receptor currents by arachidonic acid, Nature, 355, 722, 10.1038/355722a0 Nishikawa, 1994, Facilitatory effect of docosahexaenoic acid on N-methyl-d-aspartate response in pyramidal neurones of rat cerebral cortex, J Physiol (Lond), 475, 83, 10.1113/jphysiol.1994.sp020051 Paoletti, 1994, Mechanosensitivity of NMDA receptors in cultured mouse central neurons, Neuron, 13, 645, 10.1016/0896-6273(94)90032-9 Casado, 1998, Opposite modulation of NMDA receptors by lysophospholipids and arachidonic acid: common features with mechanosensitivity, J Physiol (Lond), 513, 317, 10.1111/j.1469-7793.1998.317bb.x Kloda, 2007, Liposome reconstitution and modulation of recombinant N-methyl-d-aspartate receptor channels by membrane stretch, Proc Natl Acad Sci U S A, 104, 1540, 10.1073/pnas.0609649104 Hardie, 2015, Phototransduction in Drosophila, Curr Opin Neurobiol, 34, 37, 10.1016/j.conb.2015.01.008 Huang, 2010, Activation of TRP channels by protons and phosphoinositide depletion in Drosophila photoreceptors, Curr Biol, 20, 189, 10.1016/j.cub.2009.12.019 Randall, 2015, Speed and sensitivity of phototransduction in Drosophila depend on degree of saturation of membrane phospholipids, J Neurosci, 35, 2731, 10.1523/JNEUROSCI.1150-14.2015 Goodman, 2006, Mechanosensation White, 2016, TRPV4: molecular conductor of a diverse orchestra, Physiol Rev, 96, 911, 10.1152/physrev.00016.2015 Watanabe, 2003, Anandamide and arachidonic acid use epoxyeicosatrienoic acids to activate TRPV4 channels, Nature, 424, 434, 10.1038/nature01807 Berna-Erro, 2017, Structural determinants of 5′,6′-epoxyeicosatrienoic acid binding to and activation of TRPV4 channel, Sci Rep, 7, 10522, 10.1038/s41598-017-11274-1 Barrantes, 2004, Structural basis for lipid modulation of nicotinic acetylcholine receptor function, Brain Res Rev, 47, 71, 10.1016/j.brainresrev.2004.06.008 Sunshine, 1994, Lipid modulation of nicotinic acetylcholine receptor function: the role of membrane lipid composition and fluidity, Biochim Biophys Acta, 1191, 59, 10.1016/0005-2736(94)90233-X Tanaka, 2012, Effects of docosahexaenoic acid on neurotransmission, Biomol Ther, 20, 152, 10.4062/biomolther.2012.20.2.152 Basak, 2017, Crystal structure and dynamics of a lipid-induced potential desensitized-state of a pentameric ligand-gated channel, Elife, 6, e23886, 10.7554/eLife.23886 Antollini, 2016, Fatty acid regulation of voltage- and ligand-gated ion channel function, Front Physiol, 7, 573, 10.3389/fphys.2016.00573 Bouzat, 2008, The interface between extracellular and transmembrane domains of homomeric Cys-loop receptors governs open-channel lifetime and rate of desensitization, J Neurosci, 28, 7808, 10.1523/JNEUROSCI.0448-08.2008 Kaczmarek, 2017, International Union of Basic and Clinical Pharmacology. C. Nomenclature and properties of calcium-activated and sodium-activated potassium channels, Pharmacol Rev, 69, 1, 10.1124/pr.116.012864 Hoshi, 2013, Omega-3 fatty acids lower blood pressure by directly activating large-conductance Ca2+-dependent K+ channels, Proc Natl Acad Sci U S A, 110, 4816, 10.1073/pnas.1221997110 Hoshi, 2013, Mechanism of the modulation of BK potassium channel complexes with different auxiliary subunit compositions by the omega-3 fatty acid DHA, Proc Natl Acad Sci U S A, 110, 4822, 10.1073/pnas.1222003110 Tian, 2016, Atomic determinants of BK channel activation by polyunsaturated fatty acids, Proc Natl Acad Sci U S A, 113, 13905, 10.1073/pnas.1615562113 Bukiya, 2014, Activation of calcium- and voltage-gated potassium channels of large conductance by leukotriene B4, J Biol Chem, 289, 35314, 10.1074/jbc.M114.577825 Bukiya, 2011, The steroid interaction site in transmembrane domain 2 of the large conductance, voltage- and calcium-gated potassium (BK) channel accessory β1 subunit, Proc Natl Acad Sci U S A, 108, 20207, 10.1073/pnas.1112901108 Zhao, 2010, Membrane stretch and cytoplasmic Ca2+ independently modulate stretch-activated BK channel activity, J Biomech, 43, 3015, 10.1016/j.jbiomech.2010.06.018 Julius, 2013, TRP channels and pain, Annu Rev Cell Dev Biol, 29, 355, 10.1146/annurev-cellbio-101011-155833 Tigyi, 2003, Molecular mechanisms of lysophosphatidic acid action, Prog Lipid Res, 42, 498, 10.1016/S0163-7827(03)00035-3 Inoue, 2004, Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling, Nat Med, 10, 712, 10.1038/nm1060 Tigyi, 2012, Lipids: LPA activates TRPV1—and it hurts, Nat Chem Biol, 8, 22, 10.1038/nchembio.738 Nieto-Posadas, 2011, Lysophosphatidic acid directly activates TRPV1 through a C-terminal binding site, Nat Chem Biol, 8, 78, 10.1038/nchembio.712 Morales-Lazaro, 2014, Structural determinants of the transient receptor potential 1 (TRPV1) channel activation by phospholipid analogs, J Biol Chem, 289, 24079, 10.1074/jbc.M114.572503 Zygmunt, 1999, Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide, Nature, 400, 452, 10.1038/22761 Medeiros, 2017, Membrane-mediated action of the endocannabinoid anandamide on membrane proteins: implications for understanding the receptor-independent mechanism, Sci Rep, 7, 1, 10.1038/srep41362 Jordt, 2002, Molecular basis for species-specific sensitivity to “hot” chili peppers, Cell, 108, 421, 10.1016/S0092-8674(02)00637-2 Cao, 2013, TRPV1 structures in distinct conformations reveal activation mechanisms, Nature, 504, 113, 10.1038/nature12823 Cao, 2013, TRPV1 channels are intrinsically heat sensitive and negatively regulated by phosphoinositide lipids, Neuron, 77, 667, 10.1016/j.neuron.2012.12.016 Kahn-Kirby, 2004, Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo, Cell, 119, 889, 10.1016/j.cell.2004.11.005 Denisov, 2016, Nanodiscs for structural and functional studies of membrane proteins, Nat Struct Mol Biol, 23, 481, 10.1038/nsmb.3195 Denisov, 2017, Nanodiscs in membrane biochemistry and biophysics, Chem Rev, 117, 4669, 10.1021/acs.chemrev.6b00690 Laganowsky, 2014, Membrane proteins bind lipids selectively to modulate their structure and function, Nature, 510, 172, 10.1038/nature13419 Liu, 2017, Characterization of membrane protein–lipid interactions by mass spectrometry ion mobility mass spectrometry, J Am Soc Mass Spectrom, 28, 579, 10.1007/s13361-016-1555-1