Untangling Direct and Domain-Mediated Interactions Between Nicotinic Acetylcholine Receptors in DHA-Rich Membranes
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Albuquerque EX, Pereira EFR, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89(1):73–120. https://doi.org/10.1152/physrev.00015.2008
Althoff T, Hibbs RE, Banerjee S, Gouaux E (2014) X-ray structures of glucl in apo states reveal a gating mechanism of cys-loop receptors. Nature 512(7514):333–337. https://doi.org/10.1038/nature13669
Anholt R, Lindstrom J, Montal M (1980) Functional equivalence of monomeric and dimeric forms of purified acetylcholine receptors from torpedo californica in reconstituted lipid vesicles. Eur J Biochem 109:481–487
Antollini SS, Barrantes FJ (2016) Fatty acid regulation of voltage- and ligand-gated ion channel function. Front Physiol 7:573. https://doi.org/10.3389/fphys.2016.00573
Baaden M, Marrink SJ (2013) Coarse-grain modelling of protein–protein interactions. Curr Opin Struct Biol 23(6):878–886. https://doi.org/10.1016/j.sbi.2013.09.004
Baenziger JE, Corringer PJ (2011) 3D structure and allosteric modulation of the transmembrane domain of pentameric ligand-gated ion channels. Neuropharmacology 60(1):116–125. https://doi.org/10.1016/j.neuropharm.2010.08.007
Baenziger JE, Hénault CM, Therien JPD, Sun J (2015) Nicotinic acetylcholine receptor-lipid interactions: mechanistic insight and biological function. Biochimica Biophysica Acta 1848(9):1806–1817. https://doi.org/10.1016/j.bbamem.2015.03.010
Baenziger JE, Domville JA, Therien JPD (2017) The role of cholesterol in the activation of nicotinic acetylcholine receptors. Curr Topics Memb 80:95–137. https://doi.org/10.1016/bs.ctm.2017.05.002
Barrantes FJ (2007) Cholesterol effects on nicotinic acetylcholine receptor. J Neurochem 103(s1):72–80
Barrantes FJ, Antollini SS, Blanton MP, Prieto M (2000) Topography of nicotinic acetylcholine receptor membrane-embedded domains. J Biol Chem 275(48):37333–37339
Barrantes FJ, Bermudez V, Borroni MV, Antollini SS, Pediconi MF, Baier JC, Bonini I, Gallegos C, Roccamo AM, Valles AS, Ayala V, Kamerbeek C (2010) Boundary lipids in the nicotinic acetylcholine receptor microenvironment. J Mol Neurosci 40:87–90. https://doi.org/10.1007/s12031-009-9262-z
Bermudez V, Antollini SS, Nievas GAF, AveldaÒo MI, Barrantes FJ (2010) Partition profile of the nicotinic acetylcholine receptor in lipid domains upon reconstitution. J Lipid Res 51(9):2629–2641
Bond PJ, Sansom MSP (2006) Insertion and assembly of membrane proteins via simulation. J Am Chem Soc 128(8):2697–2704. https://doi.org/10.1021/ja0569104
Borroni MV, Vallés AS, Barrantes FJ (2016) The lipid habitats of neurotransmitter receptors in brain. Biochimica Biophysica Acta 1858:2662–2670. https://doi.org/10.1016/j.bbamem.2016.07.005
Bouzat CB, Barrantes FJ (1993) Effects of long-chain fatty acids on the channel activity of the nicotinic acetylcholine receptor. Recept Channels 1:251–258
Brannigan G, Hénin J, Law R, Eckenhoff R, Klein ML (2008) Embedded cholesterol in the nicotinic acetylcholine receptor. Proc Natl Acad Sci 105(38):14418–14423
Breckenridge W, Gombos G, Morgan I (1972) The lipid composition of adult rat brain synaptosomal plasma membranes. Biochimica Biophysica Acta (BBA) 266(3):695–707. https://doi.org/10.1016/0005-2736(72)90365-3
Brusés JL, Chauvet N, Rutishauser U (2001) Membrane lipid rafts are necessary for the maintenance of the (alpha)7 nicotinic acetylcholine receptor in somatic spines of ciliary neurons. J Neurosci 21(2):504–512
Butler DH, McNamee MG (1993) FTIR analysis of nicotinic acetylcholine receptor secondary structure in reconstituted membranes. Biochimica Biophysica Acta (BBA) 1150(1):17–24. https://doi.org/10.1016/0005-2736(93)90116-h
Campagna J, Fallon J (2006) Lipid rafts are involved in c95 (4, 8) agrin fragment-induced acetylcholine receptor clustering. Neuroscience 138(1):123–132
Carswell CL, Hénault CM, Murlidaran S, Therien J, Juranka PF, Surujballi JA, Brannigan G, Baenziger JE (2015) Role of the fourth transmembrane helix in the allosteric modulation of pentameric Ligand-Gated ion channels. Structure 23(9):1655–64. https://doi.org/10.1016/j.str.2015.06.020
Chang HW, Bock E (1977) Molecular forms of acetylcholine receptor: effects of calcium ions and a sulfhydryl reagent on the occurrence of oligomers. Biochemistry 16:4513–4520
Cheng MH, Xu Y, Tang P (2009) Anionic lipid and cholesterol interactions with $$\alpha 4 \beta 2$$ nachr: insights from md simulations. J Phys Chem B 113(19):6964–6970
Corringer PJ, Poitevin F, Prevost MS, Sauguet L, Delarue M, Changeux JP (2012) Structure and pharmacology of pentameric receptor channels: from bacteria to brain. Structure 20(6):941–956. https://doi.org/10.1016/j.str.2012.05.003
Criado M, Eibl H, Barrantes FJ (1982) Effects of lipids on acetylcholine receptor: essential need of cholesterol for maintenance of agonist-induced state transitions in lipid vesicles. Biochemistry 21(15):3622–3629. https://doi.org/10.1021/bi00258a015
daCosta CJB, Ogrel AA, McCardy EA, Blanton MP, Baenziger JE (2001) Lipid–protein interactions at the nicotinic acetylcholine receptor. J Biol Chem 277(1):201–208. https://doi.org/10.1074/jbc.m108341200
Feller SE (2008) Acyl chain conformations in phospholipid bilayers: a comparative study of docosahexaenoic acid and saturated fatty acids. Chem Phys Lipids 153(1):76–80. https://doi.org/10.1016/j.chemphyslip.2008.02.013
Fong T, McNamee M (1986) Correlation between acetylcholine receptor function and structural properties of membranes. Biochemistry 25(4):830–840
Fong T, McNamee M (1987) Stabilization of acetylcholine receptor secondary structure by cholesterol and negatively charged phospholipids in membranes. Biochemistry. https://doi.org/10.1021/bi00387a020
Gahbauer S, Böckmann RA (2016) Membrane-mediated oligomerization of g protein coupled receptors and its implications for gpcr function. Front Physiol 7:494. https://doi.org/10.3389/fphys.2016.00494
Georgieva R, Chachaty C, Hazarosova R, Tessier C, Nuss P, Momchilova A, Staneva G (2015) Docosahexaenoic acid promotes micron scale liquid-ordered domains: a comparison study of docosahexaenoic versus oleic acid containing phosphatidylcholine in raft-like mixtures. Biochimica Biophysica Acta (BBA) 1848(6):1424–1435. https://doi.org/10.1016/j.bbamem.2015.02.027
Goose JE, Sansom MS (2013) Reduced lateral mobility of lipids and proteins in crowded membranes. PLoS Comput Biol 9(4):1003033. https://doi.org/10.1371/journal.pcbi.1003033
Gotti C, Fornasari D, Clementi F (1997) Human neuronal nicotinic receptors. Prog Neurobiol 53(2):199–237
Hénin J, Salari R, Murlidaran S, Brannigan G (2014) A predicted binding site for cholesterol on the GABAA receptor. Biophys J 106(9):1938–1949. https://doi.org/10.1016/j.bpj.2014.03.024
Hibbs RE, Gouaux E (2011) Principles of activation and permeation in an anion-selective cys-loop receptor. Nature 474(7349):54–60
Ingólfsson HI, Melo MN, Van Eerden FJ, Arnarez C, Lopez CA, Wassenaar TA, Periole X, De Vries AH, Tieleman DP, Marrink SJ (2014) Lipid organization of the plasma membrane. J Am Chem Soc 136(41):14554–14559. https://doi.org/10.1021/ja507832e
Iyer SS, Tripathy M, Srivastava A (2018) Fluid phase coexistence in biological membrane: insights from local nonaffine deformation of lipids. Biophys J 115(1):117–128. https://doi.org/10.1016/j.bpj.2018.05.021
Lavandera JV, Saín J, Fariña AC, Bernal CA, González MA (2017) N-3 fatty acids reduced trans fatty acids retention and increased docosahexaenoic acid levels in the brain. Nutr Neurosci 20(7):424–435
Laverty D, Thomas P, Field M, Andersen OJ, Gold MG, Biggin PC, Gielen M, Smart TG (2017) Crystal structures of a GABAA-receptor chimera reveal new endogenous neurosteroid-binding sites. Nat Struct Mol Biol. https://doi.org/10.1038/nsmb.3477
Laverty D, Desai R, Uchański T, Masiulis S, Stec WJ, Malinauskas T, Zivanov J, Pardon E, Steyaert J, Miller KW, Aricescu AR (2019) Cryo-em structure of the human 1 3 2 gaba, javax.xml.bind.jaxbelement@18520d8a, receptor in a lipid bilayer. Nature 565:516–520. https://doi.org/10.1038/s41586-018-0833-4
Levental K, Lorent J, Lin X, Skinkle A, Surma M (2016) Polyunsaturated lipids regulate membrane domain stability by tuning membrane order. Biophys J. https://doi.org/10.1016/j.bpj.2016.03.012
Marchand S, Devillers-Thiéry A, Pons S, Changeux JP, Cartaud J (2002) Rapsyn escorts the nicotinic acetylcholine receptor along the exocytic pathway via association with lipid rafts. J Neurosci 22(20):8891–8901
Marrink SJ, Risselada HJ, Yefimov S, Tieleman DP, de Vries AH (2007) The martini force field: coarse grained model for biomolecular simulations. J Phys Chem B 111(27):7812–7824. https://doi.org/10.1021/jp071097f
Masiulis S, Desai R, Uchañski T, Serna Martin I, Laverty D, Karia D, Malinauskas T, Zivanov J, Pardon E, Kotecha A, Steyaert J, Miller KW, Aricescu AR (2019) Gabaa receptor signalling mechanisms revealed by structural pharmacology. Nature 565:454–459. https://doi.org/10.1038/s41586-018-0832-5
Morales-Perez CL, Noviello CM, Hibbs RE (2016a) X-ray structure of the human $$\alpha 4 \beta 2$$ nicotinic receptor. Nature 538(7625):411–415. https://doi.org/10.1038/nature19785
Morales-Perez CL, Noviello CM, Hibbs RE (2016b) X-ray structure of the human [alpha]4[beta]2 nicotinic receptor. Nature 538(7625):411–415
Nemecz A, Prevost MS, Menny A, Corringer PJ (2016) Review: emerging molecular mechanisms of signal transduction in pentameric ligand-gated ion channels. Neuron 90:452–470
Oshikawa J, Toya Y, Fujita T, Egawa M, Kawabe J, Umemura S, Ishikawa Y (2003) Nicotinic acetylcholine receptor alpha 7 regulates cAMP signal within lipid rafts. Am J Physiol Cell Physiol 285(3):C567–74. https://doi.org/10.1152/ajpcell.00422.2002
Parton D, Tek A, Baaden M, Sansom M (2013) Formation of raft-like assemblies within clusters of influenza hemagglutinin observed by md simulations. PLoS Comput Biol 9(4):e1003034
Pato C, Stetzkowski-Marden F, Gaus K, Recouvreur M, Cartaud A, Cartaud J (2008) Role of lipid rafts in agrin-elicited acetylcholine receptor clustering. Chemico-Biol Interactions 175(1–3):64–67. https://doi.org/10.1016/j.cbi.2008.03.020
Perillo VL, Peñalva DA, Vitale AJ, Barrantes FJ, Antollini SS (2016) Transbilayer asymmetry and sphingomyelin composition modulate the preferential membrane partitioning of the nicotinic acetylcholine receptor in Lo domains. Arch Biochem Biophys 591:76–86. https://doi.org/10.1016/j.abb.2015.12.003
Prevost MS, Sauguet L, Nury H, Van Renterghem C, Huon C, Poitevin F, Baaden M, Delarue M, Corringer PJ (2012) A locally closed conformation of a bacterial pentameric proton-gated ion channel. Nat Struct Mol Biol 19(6):642–649
Pronk S, Páll S, Schulz R, Larsson P, Bjelkmar P et al (2013) Gromacs 4.5: a high-throughput and highly parallel open source molecular simulation toolkit. Bioinformatics. https://doi.org/10.1093/bioinformatics/btt055
Ramarao MK, Cohen JB (1998) Mechanism of nicotinic acetylcholine receptor cluster formation by rapsyn. Proc Natl Acad Sci USA 95(7):4007–4012. https://doi.org/10.1073/pnas.95.7.4007
Rüchel R, Watters D, Maelicke A (1981) Molecular forms and hydrodynamic properties of acetylcholine receptor from electric tissue. Eur J Biochem 119:215–223
Sauguet L, Shahsavar A, Poitevin F, Huon C, Menny A, Nemecz A, Haouz A, Changeux JP, Corringer PJ, Delarue M (2014) Crystal structures of a pentameric ligand-gated ion channel provide a mechanism for activation. Proc Natl Acad Sci 111(3):966–971
Schindler H, Spillecke F, Neumann E (1984) Different channel properties of torpedo acetylcholine receptor monomers and dimers reconstituted in planar membranes. Proc Natl Acad Sci USA 81:6222–6226
Scott KA, Bond PJ, Ivetac A, Chetwynd AP, Khalid S, Sansom MSP (2008) Coarse-grained MD simulations of membrane protein-bilayer self-assembly. Structure 16(4):621–630. https://doi.org/10.1016/j.str.2008.01.014
Shaikh SR, Dumaual AC, Castillo A, Locascio D, Siddiqui RA, Stillwell W, Wassall SR (2004) Oleic and docosahexaenoic acid differentially phase separate from lipid raft molecules: a comparative nmr, dsc, afm, and detergent extraction study. Biophys J 87(3):1752–1766. https://doi.org/10.1529/biophysj.104.044552
Sharp L, Salari R, Brannigan G (2019) Boundary lipids of the nicotinic acetylcholine receptor: spontaneous partitioning via coarse-grained molecular dynamics simulation. Biochimica Biophysica. https://doi.org/10.1016/j.bbamem.2019.01.005
Sodt AJ, Sandar ML, Gawrisch K, Pastor RW, Lyman E (2014) The molecular structure of the liquid-ordered phase of lipid bilayers. J Am Chem Soc 136(2):725–732. https://doi.org/10.1021/ja4105667
Stetzkowski-Marden F, Gaus K, Recouvreur M, Cartaud A, Cartaud J (2006) Agrin elicits membrane lipid condensation at sites of acetylcholine receptor clusters in c2c12 myotubes. J Lipid Res 47(10):2121–2133
Sunshine C, McNamee MG (1992) Lipid modulation of nicotinic acetylcholine receptor function: the role of neutral and negatively charged lipids. Biochim Biophys Acta 1108(2):240–246. https://doi.org/10.1016/0005-2736(92)90031-G
Turk HF, Chapkin RS (2013) Membrane lipid raft organization is uniquely modified by n-3 polyunsaturated fatty acids. Prostaglandins Leukotrienes Essential Fatty Acids. https://doi.org/10.1016/j.plefa.2012.03.008
Unwin N (2005) Refined structure of the nicotinic acetylcholine receptor at 4 Å resolution. J Mol Biol 346(4):967–989. https://doi.org/10.1016/j.jmb.2004.12.031
Unwin N (2017) Segregation of lipids near acetylcholine-receptor channels imaged by cryo-em. IUCrJ 4:393–399. https://doi.org/10.1107/S2052252517005243
Wassall SR, Stillwell W (2008) Docosahexaenoic acid domains: the ultimate non-raft membrane domain. Chem Phys Lipids 153:57–63
Wenz JJ, Barrantes FJ (2005) Nicotinic acetylcholine receptor induces lateral segregation of phosphatidic acid and phosphatidylcholine in reconstituted membranes. Biochemistry 44(1):398–410
Willmann R, Pun S, Stallmach L, Sadasivam G, Santos AF et al (2006) Cholesterol and lipid microdomains stabilize the postsynapse at the neuromuscular junction. EMBO J 25(17):4050–4060
Yadav RS, Tiwari NK (2014) Lipid integration in neurodegeneration: an overview of Alzheimer’s Disease. Mol Neurobiol 50:168–76
Zhu D, Xiong WC, Mei L (2006) Lipid rafts serve as a signaling platform for nicotinic acetylcholine receptor clustering. J Neurosci 26(18):4841–4851. https://doi.org/10.1523/JNEUROSCI.2807-05.2006
Zingsheim HP, Neugebauer DC, Frank J, Hänicke W, Barrantes FJ (1982) Dimeric arrangement and structure of the membrane-bound acetylcholine receptor studied by electron microscopy. EMBO J 1:541–547