2,754
Views
101
CrossRef citations to date
0
Altmetric
Original

Assembly and trafficking of nicotinic acetylcholine receptors (Review)

&
Pages 279-292 | Received 30 Nov 2007, Published online: 09 Jul 2009

References

  • Lester HA, Dibas MI, Dahan DS, Leite JF, Dougherty DA. Cys-loop receptors: new twists and turns. Trends Neurosci 2004; 27: 329–336
  • Millar NS. 2006. Ligand-gated ion channels. Encyclopedia of Life Sciences http://www.els.net/ [doi:10.1038/npg.els.0000154].
  • Sharma G, Vijayaraghavan S. Nicotinic receptor signalling in nonexcitable cells. J Neurobiol 2002; 53: 524–534
  • Lindstrom J. Acetylcholine receptors and myasthenia. Muscle Nerve 2000; 23: 453–477
  • Weiland S, Bertrand D, Leonard S. Neuronal nicotinic acetylcholine receptors: from the gene to the disease. Behavioural Brain Res 2000; 113: 43–56
  • Gotti C, Zoli M, Clementi F. Brain nicotinic acetylcholine receptors: native subtypes and their relevance. Trends Pharmacol Sci 2006; 27: 482–491
  • Jensen AA, Frolund B, Liljefors T, Krogsgaard-Larsen P. Neuronal nicotinic acetylcholine receptors: structural revelations, target identification, and therapeutic inspirations. J Med Chem 2005; 48: 4705–4745
  • Arneric SP, Holladay M, Williams M. Neuronal nicotinic receptors: a perspective on two decades of drug discovery research. Biochem Pharmacol 2007; 74: 1092–1101
  • Raymond Delpech V, Matsuda K, Sattelle BM, Rauh JJ, Sattelle DB. Ion channels: molecular targets of neuroactive insecticides. Invert Neurosci 2005; 5: 119–133
  • Millar NS, Denholm I. Nicotinic acetylcholine receptors: targets for commercially important insecticides. Invert Neurosci 2007; 7: 53–66
  • Popot J-L, Changeux J-P. Nicotinic receptor of acetylcholine: structure of an oligomeric integral membrane protein. Physiol Rev 1984; 64: 1162–1239
  • Weill CL, McNamee MG, Karlin A. Affinity-labeling of purified acetylcholine receptor from Torpedo californica. Biochem Biophys Res Comm 1974; 61: 997–1003
  • Noda M, Takahashi H, Tanabe T, Toyosato M, Furutani Y, Hirose T, Asai M, Inayama S, Miyata T, Numa S. Primary structure of α-subunit precursor of Torpedo californica acetylcholine receptor deduced from cDNA sequence. Nature 1982; 299: 793–797
  • Sumikawa K, Houghton M, Smith JC, Bell L, Richards BM, Barnard EA. The molecular cloning and characterisation of cDNA coding for the α subunit of the acetylcholine receptor. Nucl Acids Res 1982; 10: 5809–5822
  • Sine SM. The nicotinic receptor ligand binding domain. J Neurobiol 2002; 53: 431–446
  • Luetje CW, Patrick J. Both α- and β-subunits contribute to the agonist sensitivity of neuronal nicotinic acetylcholine receptors. J Neurosci 1991; 11: 837–845
  • Le Novère N, Corringer P-J, Changeux J-P. The diversity of subunit composition in nAChRs: evolutionary origins, physiologic and pharmacologic consequences. J Neurobiol 2002; 53: 447–456
  • Millar NS. Assembly and subunit diversity of nicotinic acetylcholine receptors. Biochem Soc Trans 2003; 31: 869–874
  • Lukas RJ, Changeux J-P, Le Novère N, Albuquerque EX, Balfour DJK, Berg DK, Bertrand D, Chiappinelli AA, Clarke PBS, Collins AC, Dani JA, Grady SR, Kellar KJ, Lindstrom JM, Marks MJ, Quik M, Taylor PW, Wonnacott S. International union of pharmacology. XX. current status of the nomenclature for nicotinic acetylcholine receptors and their subunits. Pharmacol Rev 1999; 51: 397–401
  • Luetje CW. Getting past the asterisk: the subunit composition of presynaptic nicotinic receptors that modulate striatal dopamine release. Mol Pharmacol 2004; 65: 1333–1335
  • Mishina M, Kurosaki T, Tobimatsu T, Morimoto Y, Noda M, Yamamoto T, Terao M, Lindstrom J, Takahashi T, Kuno M, Numa S. Expression of functional acetylcholine receptor from cloned cDNAs. Nature 1984; 307: 604–608
  • Claudio T, Green WN, Hartman DS, Hayden D, Paulson HL, Sigworth FJ, Sine SM, Swedlund A. Genetic reconstitution of functional acetylcholine receptor channels in mouse fibroblasts. Science 1987; 238: 1688–1694
  • Unwin N. Refined structure of the nicotinic acetylcholine receptor at 4Å resolution. J Mol Biol 2005; 346: 967–989
  • Kubalek E, Ralston S, Lindstrom J, Unwin N. Location of subunits within the acetylcholine receptor by electron image analysis of tubular crystals from Torpedo marmorata. J Cell Biol 1987; 105: 9–18
  • Beroukhim R, Unwin N. Three-dimensional location of the main immunogenic region of the acetylcholine receptor. Neuron 1995; 15: 323–331
  • Unwin N. Acetylcholine receptor channel imaged in the open state. Nature 1995; 373: 37–43
  • Green WN, Millar NS. Ion-channel assembly. Trends Neurosci 1995; 18: 280–287
  • Green WN. Ion channel assembly: creating structures that function. J Gen Physiol 1999; 113: 163–169
  • Keller ST, Taylor P. Determinants responsible for assembly of the nicotinic acetylcholine receptor. J Gen Physiol 1999; 113: 171–176
  • Blount P, Smith MM, Merlie JP. Assembly intermediates of the mouse muscle nicotinic acetylcholine receptor in stably transfected fibroblasts. J Cell Biol 1990; 111: 2601–2611
  • Gu Y, Forsayeth JR, Verrall S, Yu XM, Hall ZW. Assembly of the mammalian muscle acetylcholine receptor in transfected COS cells. J Cell Biol 1991; 114: 799–807
  • Saedi MS, Conroy WG, Lindstrom J. Assembly of Torpedo acetylcholine receptors in Xenopus oocytes. J Cell Biol 1991; 112: 1007–1015
  • Kreienkamp H-J, Maeda RK, Sine S, Taylor P. Intersubunit contacts governing assembly of the mammalian nicotinic acetylcholine receptor. Neuron 1995; 14: 635–644
  • Green WN, Claudio T. Acetylcholine receptor assembly: subunit folding and oligomerization occur sequentially. Cell 1993; 74: 57–69
  • Green WN, Wanamaker CP. The role of the cystine loop in acetylcholine receptor assembly. J Biol Chem 1997; 272: 20945–20953
  • Green WN, Wanamaker CP. Formation of the nicotinic acetylcholine receptor binding sites. J Neurosci 1998; 18: 5555–5564
  • Harkness PC, Millar NS. Changes in conformation and subcellular distribution of α4β2 nicotinic acetylcholine receptors revealed by chronic nicotine treatment and expression of subunit chimeras. J Neurosci 2002; 22: 10172–10181
  • Ortells MO, Barrantes GE. A model for the assembly of nicotinic receptors based on subunit-subunit interactions. Proteins 2008; 70: 473–488
  • Whiting PJ, Lindstrom JM. Purification and characterization of a nicotinic acetylcholine receptor from chick brain. Biochemistry 1986; 25: 2082–2093
  • Whiting P, Lindstrom J. Purification and characterization of a nicotinic acetylcholine receptor from rat brain. Proc Natl Acad Sci USA 1987; 84: 595–599
  • Whiting PJ, Lindstrom JM. Characterization of bovine and human neuronal nicotinic acetylcholine receptors using monoclonal antibodies. J Neurosci 1988; 8: 3395–3404
  • Halvorsen SW, Berg DK. Affinity labeling of neuronal acetylcholine receptor subunits with an α-neurotoxin that blocks receptor function. J Neurosci 1987; 7: 2547–2555
  • Halvorsen SW, Berg DK. Subunit composition of nicotinic acetylcholine receptors from chick ciliary ganglia. J Neurosci 1990; 10: 1711–1718
  • Anand R, Conroy WG, Schoepfer R, Whiting P, Lindstrom J. Neuronal nicotinic acetylcholine receptors expressed in Xenopus oocytes have a pentameric quaternary structure. J Biol Chem 1991; 266: 11192–11198
  • Cooper E, Couturier S, Ballivet M. Pentameric structure and subunit stoichiometry of a neuronal nicotinic acetylcholine receptor. Nature 1991; 350: 235–238
  • Palma E, Bertrand S, Binzoni T, Bertrand D. Neuronal nicotinic α7 receptor expressed in Xenopus oocytes presents five putative binding sites for methyllycaconitine. J Physiol 1996; 491: 151–161
  • Drisdel RC, Green WN. Neuronal α-bungarotoxin receptors are α7 subunit homomers. J Neurosci 2000; 20: 133–139
  • Boulter J, Connolly J, Deneris E, Goldman D, Heinemann S, Patrick J. Functional expression of two neuronal nicotinic acetylcholine receptors from cDNA clones identifies a gene family. Proc Natl Acad Sci USA 1987; 84: 7763–7767
  • Duvoisin RM, Deneris ES, Patrick J, Heinemann S. The functional diversity of the neuronal nicotinic acetylcholine receptors is increased by a novel subunit: β4. Neuron 1989; 3: 487–496
  • Rogers SW, Gahring LC, Papke RL, Heinemann S. Identification of cultured cells expressing ligand-gated cationic channels. Protein Expr Purif 1991; 2: 108–116
  • Whiting P, Schoepfer R, Lindstrom J, Priestley T. Structural and pharmacological characterization of the major brain nicotinic acetylcholine receptor subtype stably expressed in mouse fibroblasts. Mol Pharmacol 1991; 40: 463–472
  • Wong ET, Holstad SG, Mennerick SJ, Hong SE, Zorumski CF, Isenberg KE. Pharmacological and physiological properties of a putative ganglionic nicotinic receptor α3β4, expressed in transfected eucaryotic cells. Mol Brain Res 1995; 28: 101–109
  • Ragozzino D, Fucile S, Giovannelli A, Grassi F, Mileo AM, Ballivet M, Alemà S, Eusebi F. Functional properties of neuronal nicotinic acetylcholine receptor channels expressed in transfected human cells. Eur J Neurosci 1997; 9: 480–488
  • Cooper ST, Harkness PC, Baker ER, Millar NS. Upregulation of cell-surface α4β2 neuronal nicotinic receptors by lower temperature and expression of chimeric subunits. J Biol Chem 1999; 274: 27145–27152
  • Boorman JPB, Groot-Kormelink PJ, Sivilotti LG. Stoichiometry of human recombinant neuronal nicotinic receptors containing the β3 subunit expressed in Xenopus oocytes. J Physiol 2000; 529: 565–577
  • Zwart R, Vijverberg HPM. Four pharmacologically distinct subtypes of α4β2 nicotinic acetylcholine receptor expressed in Xenopus laevis oocytes. Mol Pharmacol 1998; 54: 1124–1131
  • Nelson ME, Kuryatov A, Choi CH, Zhou Y, Lindstrom J. Alternate stoichiometries of α4β2 nicotinic acetylcholine receptors. Mol Pharmacol 2003; 63: 332–341
  • Zhou Y, Nelson ME, Kuryatov A, Choi CH, Cooper J, Lindstrom J. Human α4β2 acetylcholine receptors formed from linked subunits. J Neurosci 2003; 23: 9004–9015
  • Tapia L, Kuryatov A, Lindstrom J. Ca2 +  permeability of the (α4)3(β2)2 stoichiometry greatly exceeds that of (α4)2(β2)3 human acetylcholine receptors. Mol Pharmacol 2007; 71: 769–776
  • Deneris ES, Boulter J, Swanson LW, Patrick J, Heinemann S. β3: a new member of nicotinic acetylcholine receptor gene family is expressed in brain. J Biol Chem 1989; 264: 6268–6272
  • Couturier S, Erkman L, Valera S, Rungger D, Bertrand S, Boulter J, Ballivet M, Bertrand D. α5, α3, and non-α3. Three clustered avian genes encoding neuronal nicotinic acetylcholine receptor-related subunits. J Biol Chem 1990; 265: 17560–17567
  • Wang F, Gerzanich V, Wells GB, Anand R, Peng X, Keyser K, Lindstrom J. Assembly of human neuronal nicotinic receptor α5 subunit with α3, β2, and β4 subunits. J Biol Chem 1996; 271: 17656–17665
  • Gerzanich V, Wang F, Kuryatov A, Lindstrom J. α5 subunit alters desensitization, pharmacology, Ca+ +  permeability and Ca+ +  modulation of human neuronal α3 nicotinic receptors. J Pharm Exper Ther 1998; 286: 311–320
  • Fucile S, Barabino B, Palma E, Grassi F, Limatola C, Mileo AM, Alemà S, Ballivet M, Eusebi F. α5 subunit forms functional α3β4α5 nAChRs in transfected human cells. Neuroreport 1997; 8: 2433–2436
  • Ramirez-Latorre J, Yu CR, Qu F, Perin F, Karlin A, Role L. Functional contributions of α5 subunit to neuronal acetylcholine receptor channels. Nature 1996; 380: 347–351
  • Groot-Kormelink PJ, Luyten WHML, Colquhoun D, Sivilotti LG. A reporter mutation approach shows incorporation of the “orphan” subunit β3 into a functional nicotinic receptor. J Biol Chem 1998; 273: 15317–15320
  • Kuryatov A, Olale F, Cooper J, Choi C, Lindstrom J. Human α6 AChR subtypes: subunit composition, assembly, and pharmacological responses. Neuropharmacol 2000; 39: 2570–2590
  • Tumkosit P, Kuryatov A, Luo J, Lindstrom J. β3 subunits promote expression and nicotine-induced up-regulation of human nicotinic α6* nicotinic acetylcholine receptors expressed in transfected cell lines. Mol Pharmacol 2006; 70: 1358–1368
  • Gotti C, Moretti M, Clementi F, Riganti L, McIntosh JM, Collins AC, Marks MJ, Whiteaker P. Expression of nigrostriatal α6-containing nicotinic acetylcholine receptors is selectively reduced, but not eliminated, by β3 subunit gene deletion. Mol Pharmacol 2005; 67: 2007–2015
  • Broadbent S, Groot-Kormelink PJ, Krashia PA, Harkness PC, Millar NS, Beato M, Sivilotti LG. Incorporation of the β3 subunit has a dominant-negative effect on the function of recombinant central-type neuronal nicotinic receptors. Mol Pharmacol 2006; 70: 1350–1356
  • Groot-Kormelink PJ, Broadbent S, Boorman JP, Sivilotti LG. Incomplete incorporation of tandem subunits in recombinant neuronal nicotinic receptors. J Gen Physiol 2004; 123: 697–708
  • Groot-Kormelink PJ, Broadbent S, Beato M, Sivilotti LG. Constraining the expression of nicotinic acetylcholine receptors by using pentameric constructs. Mol Pharmacol 2006; 69: 558–563
  • Ericksen SS, Boileau AJ. Tandem couture: Cys-loop receptor concatamer insights and caveats. Mol Neurobiol 2007; 35: 113–128
  • Conroy WG, Vernallis AB, Berg DK. The α5 gene product assembles with multiple acetylcholine receptor subunits to form distinctive receptor subtypes in brain. Neuron 1992; 9: 679–691
  • Vernallis AB, Conroy WG, Berg DK. Neurons assemble acetylcholine receptors with as many as three kinds of subunits while maintaining subunit segregation among receptor subtypes. Neuron 1993; 10: 451–464
  • Conroy WG, Berg DK. Neurons can maintain multiple classes of nicotinic acetylcholine receptors distinguished by different subunit compositions. J Biol Chem 1995; 270: 4424–4431
  • Balestra B, Vailati S, Moretti M, Hanke W, Clementi F, Gotti C. Chick optic lobe contains a developmentally regulated α2α5β2 nicotinic receptor subtype. Mol Pharmacol 2000; 58: 300–311
  • Conroy WG, Berg DK. Nicotinic receptor subtypes in the developing chick brain: appearance of a species containing the α4, β2 and α5 gene products. Mol Pharmacol 1998; 53: 392–401
  • Zoli M, Moretti M, Zanardi A, McIntosh JM, Clementi F, Gotti C. Identification of the nicotinic receptor subtypes expressed on dopaminergic terminals in the rat striatum. J Neurosci 2002; 22: 8785–8789
  • Yu CR, Role LW. Functional contribution of the α5 subunit to neuronal nicotinic channels expressed by chick sympathetic ganglion neurones. J Physiol 1998; 509: 667–681
  • Gerzanich V, Kuryatov A, Anand R, Lindstrom J. "Orphan” α6 nicotinic AChR subunit can form a functional heteromeric acetylcholine receptor. Mol Pharmacol 1997; 51: 320–327
  • Fucile S, Matter J-M, Erkman L, Ragozzino D, Barabino B, Grassi F, Alemà S, Ballivet M, Eusebi F. The neuronal α6 subunit forms functional heteromeric acetylcholine receptors in human transfected cells. Eur J Neurosci 1998; 10: 172–178
  • Vailati S, Hanke W, Bejan A, Barabino B, Longhi R, Balestra B, Moretti M, Clementi F, Gotti C. Functional α6-containing nicotinic receptors are present in chick retina. Mol Pharmacol 1999; 56: 11–19
  • Champtiaux N, Gotti C, Cordero-Erausquin M, David DJ, Przybylski C, Léna C, Clementi F, Moretti M, Rossi FM, Le Novère N, McIntosh JM, Gardier AM, Changeux JP. Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J Neurosci 2003; 23: 7820–7829
  • Moretti M, Vailati S, Zoli M, Lippi G, Riganti L, Longhi R, Viegi A, Clementi F, Gotti C. Nicotinic acetylcholine receptor subtypes expressed during rat retina development and their regulation by visual experience. Mol Pharmacol 2004; 66: 85–96
  • Drenan RM, Nashmi R, Imoukhuede P, Just H, McKinney S, Lester HA. Subcellular trafficking, pentameric assembly and subunit stoichiometry of neuronal nicotinic acetylcholine receptors containing fluorescently labeled α6 and β3 subunits. Mol Pharmacol 2008; 73: 27–41
  • Couturier S, Bertrand D, Matter JM, Hernandez MC, Bertrand S, Millar N, Valera S, Barkas T, Ballivet M. A neuronal nicotinic acetylcholine receptor subunit (α7) is developmentally regulated and forms a homo-oligomeric channel blocked by α-BTX. Neuron 1990; 5: 847–856
  • Schoepfer R, Conroy WG, Whiting P, Gore M, Lindstrom J. Brain α-bungarotoxin binding protein cDNAs and mAbs reveal subtypes of this branch of the ligand-gated ion channel gene superfamily. Neuron 1990; 5: 35–48
  • Gerzanich V, Anand R, Lindstrom J. Homomers of α8 and α7 subunits of nicotinic receptors exhibit similar channels but contrasting binding site properties. Mol Pharmacol 1994; 45: 212–220
  • Gotti C, Hanke W, Maury K, Moretti M, Ballivet M, Clementi F, Bertrand D. Pharmacology and biophysical properties of α7 and α7-α8 α-bungarotoxin receptor subtypes immunopurified from the chick optic lobe. Eur J Neurosci 1994; 6: 1281–1291
  • Keyser KT, Britto LR, Schoepfer R, Whiting P, Cooper J, Conroy W, Brozozowska-Prechtl A, Karten HJ, Lindstrom J. Three subtypes of α-bungarotoxin-sensitive nicotinic acetylcholine receptors are expressed in chick retina. J Neurosci 1993; 13: 442–454
  • Anand R, Peng X, Ballesta JJ, Lindstrom J. Pharmacological characterization of α-bungarotoxin-sensitive acetylcholine receptors immunoisolated from chick retina: contrasting properties of α7 and α8 subunit-containing subtypes. Mol Pharmacol 1993; 44: 1046–1050
  • Gotti C, Ogando AE, Hanke W, Schlue R, Moretti M, Clementi F. Purification and characterization of an α-bungarotoxin receptor that forms a functional nicotinic channel. Proc Natl Acad Sci USA 1991; 88: 3258–3262
  • Gotti C, Hanke W, Schlue W-R, Briscini L, Moretti M, Clementi F. A functional α-bungarotoxin receptor is present in chick cerebellum: purification and characterization. Neurosci 1992; 50: 117–127
  • Gotti C, Moretti M, Maggi R, Longhi R, Hanke W, Klinke N, Clementi F. α7 and α8 nicotinic receptor subtypes immunoprecipitated from chick retina have different immunological, pharmacological and functional properties. Eur J Neurosci 1997; 9: 1201–1211
  • Norman RI, Mehraban F, Barnard EA, Dolly JO. Nicotinic acetylcholine receptor from chick optic lobe. Proc Natl Acad Sci USA 1982; 79: 1321–1325
  • Pugh PC, Corriveau RA, Conroy WG, Berg DK. Novel subpopulation of neuronal acetylcholine receptors among those binding α-bungarotoxin. Mol Pharmacol 1995; 47: 717–725
  • Yu CR, Role LW. Functional contribution of the α7 subunit to multiple subtypes of nicotinic receptors in embryonic chick sympathetic neurones. J Physiol 1998; 509: 651–665
  • Chen D, Patrick JW. The α-bungarotoxin-binding nicotinic acetylcholine receptor from rat brain contains only the α7 subunit. J Biol Chem 1997; 272: 24024–24029
  • Shao Z, Yakel JL. Single channel properties of neuronal nicotinic ACh receptors in stratum radiatum interneurons of rat hippocampal slices. J Physiol 2000; 527: 507–513
  • Sudweeks SN, Yakel JL. Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons. J Physiol 2000; 527: 515–528
  • Khiroug SS, Harkness PC, Lamb PW, Sudweeks SN, Khiroug L, Millar NS, Yakel JL. Rat nicotinic receptor α7 and β2 subunits co-assemble to form functional heteromeric nicotinic receptor channels. J Physiol 2002; 540: 425–434
  • Elgoyhen AB, Johnson DS, Boulter J, Vetter DE, Heinemann S. α9: an acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells. Cell 1994; 18: 705–715
  • Elgoyhen AB, Vetter DE, Katz E, Rothlin CV, Heineman SF, Boulter J. α10: a determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells. Proc Natl Acad Sci USA 2001; 98: 3501–3506
  • Vetter DE, Liberman MC, Mann J, Barhanin J, Boulter J, Brown MC, Saffiote-Kolman J, Heinemann SF, Elgoyhen AB. Role of α9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation. Neuron 1999; 23: 93–103
  • Baker ER, Zwart R, Sher E, Millar NS. Pharmacological properties of α9α10 nicotinic acetylcholine receptors revealed by heterologous expression of subunit chimeras. Mol Pharmacol 2004; 65: 453–460
  • Kassner PD, Berg DK. Differences in the fate of neuronal acetylcholine receptor protein expressed in neurons and stably transfected cells. J Neurobiol 1997; 33: 968–982
  • Cooper ST, Millar NS. Host cell-specific folding and assembly of the neuronal nicotinic acetylcholine receptor α7 subunit. J Neurochem 1997; 68: 2140–2151
  • Rangwala F, Drisdel RC, Rakhilin S, Ko E, Atluri P, Harkins AB, Fox AP, Salman SB, Green WN. Neuronal α-bungarotoxin receptors differ structurally from other nicotinic acetylcholine receptors. J Neurosci 1997; 17: 8201–8212
  • Castillo M, Mulet J, Gutiérrez LM, Ortiz JA, Castelán F, Gerber S, Sala S, Sala F, Criado M. Dual role of the RIC-3 protein in trafficking of serotonin and nicotinic acetylcholine receptors. J Biol Chem 2005; 280: 27062–27068
  • Lansdell SJ, Gee VJ, Harkness PC, Doward AI, Baker ER, Gibb AJ, Millar NS. RIC-3 enhances functional expression of multiple nicotinic acetylcholine receptor subtypes in mammalian cells. Mol Pharmacol 2005; 68: 1431–1438
  • Williams ME, Burton B, Urrutia A, Shcherbatko A, Chavez-Noriega LE, Cohen CJ, Aiyar J. Ric-3 promotes functional expression of the nicotinic acetylcholine receptor α7 subunit in mammalian cells. J Biol Chem 2005; 280: 1257–1263
  • Halevi S, McKay J, Palfreyman M, Yassin L, Eshel M, Jorgensen E, Treinin M. The C. elegans ric-3 gene is required for maturation of nicotinic acetylcholine receptors. EMBO J 2002; 21: 1012–1020
  • Halevi S, Yassin L, Eshel M, Sala F, Sala S, Criado M, Treinin M. Conservation within the RIC-3 gene family: effectors of mammalian nicotinic acetylcholine receptor expression. J Biol Chem 2003; 278: 34411–34417
  • Harkness PC, Millar NS. Inefficient cell-surface expression of hybrid complexes formed by the co-assembly of neuronal nicotinic acetylcholine receptor and serotonin receptor subunits. Neuropharmacol 2001; 41: 79–87
  • Yu XM, Hall ZW. Extracellular domains mediating ε subunit interactions of muscle acetylcholine receptor. Nature 1991; 352: 64–67
  • Sumikawa K. Sequences on the N-terminus of ACh receptor subunits regulate their assembly. Brain Res Mol Brain Res 1992; 13: 349–353
  • Eiselé J-L, Bertrand S, Galzi J-L, Devillers-Thiéry A, Changeux J-P, Bertrand D. Chimaeric nicotinic-serotonergic receptor combines distinct ligand binding and channel specificities. Nature 1993; 366: 479–483
  • García-Guzmán M, Sala F, Sala S, Campos-Caro A, Criado M. Role of two acetylcholine receptor subunit domains in homomer formation and intersubunit recognition, as revealed by α3 and α7 subunit chimeras. Biochem 1994; 33: 15198–15203
  • Vicente-Agulló F, Rovira JC, Campos-Caro A, Rodríguez-Ferrer C, Ballesta JJ, Sala S, Sala F, Criado M. Acetylcholine receptor subunit homomer formation requires compatibility between amino acid residues of the M1 and M2 transmembrane segments. FEBS Lett 1996; 399: 83–86
  • Cooper ST, Millar NS. Host cell-specific folding of the neuronal nicotinic receptor α8 subunit. J Neurochem 1998; 70: 2585–2593
  • Dineley KT, Patrick JW. Amino acid determinants of α7 nicotinic acetylcholine receptor surface expression. J Biol Chem 2000; 275: 13974–13985
  • Gee VJ, Kracun S, Cooper ST, Gibb AJ, Millar NS. Identification of domains influencing assembly and ion channel properties in α7 nicotinic receptor and 5-HT3 receptor subunit chimaeras. Br J Pharmacol 2007; 152: 501–512
  • Ren X-Q, Cheng S-B, Treuil MW, Mukherjee J, Rao J, Braunewell KH, Lindstrom J, Anand R. Structural determinants of α4β2 nicotinic acetylcholine receptor trafficking. J Neurosci 2005; 25: 6676–6686
  • Drisdel RC, Manzana E, Green WN. The role of palmitoylation in the functional expression of nicotinic α7 receptors. J Neurosci 2004; 24: 10502–10510
  • Mishina M, Tobimatsu T, Tanaka K, Fujita Y, Fukuda K, Kurasake M, Takahashi H, Morimoto Y, Hirose T, Inayama S, Takahasi T, Kuno M, Numa S. Location of functional regions of acetylcholine receptor α-subunit by site-directed mutagenesis. Nature 1985; 313: 364–369
  • Blount P, Merlie JP. Mutational analysis of muscle nicotinic acetylcholine receptor subunit assembly. J Cell Biol 1990; 111: 2613–2622
  • Chen D, Dang H, Patrick JW. Contributions of N-linked glycosylation to the expression of a functional α7-nicotinic receptor in Xenopus oocytes. J Neurochem 1998; 70: 349–357
  • Wanamaker CP, Green WN. N-linked glycosylation is required for nicotinic receptor assembly but not for subunit associations with calnexin. J Biol Chem 2005; 280: 33800–33810
  • Sumikawa K, Gehle VM. Assembly of mutant subunits of the nicotinic acetylcholine receptor lacking the conserved disulfide loop structure. J Biol Chem 1992; 267: 6286–6290
  • Gelman MS, Prives JM. Arrest of subunit folding and assembly of nicotinic acetylcholine receptors in cultured muscle cells by dithiothreitol. J Biol Chem 1996; 271: 10709–10714
  • Rakhilin S, Drisdel RC, Sagher D, McGehee DS, Vallejo Y, Green W, N. bungarotoxin receptors contain α7 subunits in two different disulfide-bonded conformations. J Cell Biol 1999; 146: 203–217
  • Helekar SA, Char D, Neff S, Patrick J. Prolyl isomerase requirement for the expression of functional homo-oligomeric ligand-gated ion channels. Neuron 1994; 12: 179–189
  • Helekar SA, Patrick J. Peptidyl prolyl cis-trans isomerase activity of cyclophilin A in functional homo-oligomeric receptor expression. Proc Natl Acad Sci USA 1997; 94: 5432–5437
  • Blumenthal EM, Conroy WG, Romano SJ, Kassner PD, Berg DK. Detection of functional nicotinic receptors blocked by α-bungarotoxin on PC12 cells and dependence of their expression on post-translational events. J Neurosci 1997; 17: 6094–6104
  • Paulson HL, Ross AF, Green WN, Claudio T. Analysis of early events in acetylcholine receptor assembly. J Cell Biol 1991; 113: 1371–1384
  • Blount P, Merlie JP. BIP associates with newly synthesized subunits of the mouse muscle nicotinic receptor. J Cell Biol 1991; 113: 1125–1132
  • Gelman MS, Chang W, Thomas DY, Bergeron JJM, Prives JM. Role of the endoplasmic reticulum chaperone calnexin in subunit folding and assembly of nicotinic acetylcholine receptors. J Biol Chem 1995; 270: 15085–15092
  • Keller SH, Lindstrom J, Yaylor P. Involvement of the chaperone protein calnexin and the acetylcholine receptor β-subunit in the assembly and cell surface expression of the receptor. J Biol Chem 1996; 271: 22871–22877
  • Jeanclos EM, Lin L, Treuil MW, Rao J, DeCoster MA, Anand R. The chaperone protein 14-3-3η interacts with the nicotinic acetylcholine receptor α4 subunit. J Biol Chem 2001; 276: 28281–28290
  • Lin L, Jeanclos EM, Treuil MW, Braunewell K-H, Gundelfinger ED, Anand R. The calcium sensor protein visinin-like protein-1 modulates the surface expression and agonist-sensitivity of the α4β2 nicotinic acetylcholine receptor. J Biol Chem 2002; 277: 41872–41878
  • Millar NS. 2008. RIC-3: a nicotinic acetylcholine receptor chaperone. Br J Pharmacol 153:5177–5183.
  • Nguyen M, Alfonso A, Johnson CD, Rand JB. Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 1995; 140: 527–535
  • Miller KG, Alfonso A, Nguyen M, Crowell JA, Johnson CD, Rand JB. A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc Natl Acad Sci USA 1996; 93: 12593–12598
  • Cheng A, McDonald NA, Connolly CN. Cell surface expression of 5-hydroxytryptamine type 3 receptors is promoted by RIC-3. J Biol Chem 2005; 280: 22502–22507
  • Lansdell SJ, Collins T, Yabe A, Gee VJ, Gibb AJ, Millar NS.2008. Host-cell specific effects of the nicotinic acetylcholine receptor chaperone RIC-3 revealed by a comparison of human and Drosophila RIC-3 homologues. J Neurochem [published on-line: doi: 10.1111/j.1471-4159.2008.05235.x].
  • Eimer S, Gottschalk A, Hengartner M, Horvitz HR, Ricmond J, Schafer WR, Bessereau J-L. Regulation of nicotinic receptor trafficking by the transmembrane Golgi protein UNC-50. EMBO J 2007; 26: 4313–4323
  • Lewis JA, Wu C-H, Berg H, Levine J. The genetics of levamisole resistance in the nematode Caenorhabditis elegans. Genetics 1980; 95: 905–928
  • Lewis JA, Elmer JS, Skimming J, McLafferty S, Fleming JT, McGee T. Cholinergic receptor mutants of the nematode Caenorhabditis elegans. J Neurosci 1987; 7: 3059–3071
  • Fitzgerald J, Kennedy D, Viseshakul N, Cohen BN, Mattick J, Bateman JF, Forsayeth JR. UCNL, the mammalian homologue of UNC-50, is an inner nuclear membrane RNA-binding protein. Brain Res 2000; 877: 110–123
  • Froehner SC, Luetje CW, Scotland PB, Patrick J. The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron 1990; 5: 403–410
  • Phillips WD, Kopta C, Blount P, Gardner PD, Steinbach JH, Merlie JP. ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kilodalton protein. Science 1991; 251: 568–570
  • Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 1995; 377: 232–236
  • Colledge M, Froehner SC. To muster a cluster: anchoring neurotransmitter receptors at synapses. Proc Natl Acad Sci USA 1998; 95: 3341–3343
  • Sanes JR, Lichtman JW. Development of the vertebrate neuromuscular junction. Annu Rev Neurosci 1999; 22: 389–442
  • Yang S-H, Armson PF, Cha J, Phillips WD. Clustering of GABAA receptors by rapsyn/43kD protein in vitro. Mol Cell Neurosci 1997; 8: 430–438
  • Feng G, Steinbach JH, Sanes JR. Rapsyn clusters neuronal acetylcholine receptors but is inessential for formation of an interneuronal cholinergic synapse. J Neurosci 1998; 18: 4166–4176
  • Burns AL, Benson D, Howard MJ, Margiotta JF. Chick ciliary ganglion neurons contain transcripts coding for acetylcholine receptor-associated protein at synapses (rapsyn). J Neurosci 1997; 17: 5016–5026
  • Conroy WG, Berg DK. Rapsyn variants in ciliary ganglia and their possible effects on clustering of nicotinic receptors. J Neurochem 1999; 73: 1399–1408
  • Kassner PD, Conroy WG, Berg DK. Organizing effects of rapsyn on neuronal nicotinic acetylcholine receptors. Mol Cell Neurosci 1998; 10: 258–270
  • Liu Q-S, Berg DK. Actin filaments and the opposing actions of CaM kinase II and calcineurin in regulating α7-containing nicotinic receptors on chick ciliary ganglion neurons. J Neurosci 1999; 19: 10280–10288
  • Shoop RD, Yamada N, Berg DK. Cytoskeletal links of neuronal acetylcholine receptors containing α7 subunits. J Neurosci 2000; 20: 4021–4029
  • Roth AL, Berg DK. Large clusters of α7-containing nicotinic acetylcholine receptors on chick spinal cord neurons. J Comp Neurol 2003; 465: 195–204
  • Conroy WG, Liu Z, Nai Q, Coggan JS, Berg DK. PDZ-containing proteins provide a functional postsynaptic scaffold for nicotinic receptors in neurons. Neuron 2003; 38: 759–771
  • Parker MJ, Zhao S, Bredt DS, Sanes JR, Feng G. PSD93 regulates synaptic stability at neuronal cholinergic synapses. J Neurosci 2004; 24: 378–388
  • Baer K, Bürli T, Huh K-H, Wiesner A, Erb-Vögtli S, Göckeritz-Dujmovic D, Moransard M, Nishimune A, Rees MI, Henley JM, Fritschy J-M, Fuhrer C. PICK1 interacts with α7 neuronal nicotinic acetylcholine receptors and controls their clustering. Mol Cell Neurosci 2007; 35: 339–355
  • Wang J, Jing Z, Zhang L, Zhou G, Braun J, Yao Y, Wang Z-Z. Regulation of acetylcholine receptor clustering by the tumor suppressor APC. Nature Neurosci 2003; 6: 1017–1018
  • Temburni MK, Rosenberg MM, Pathak N, McConnell R, Jacob MH. Neuronal nicotinic synapse assembly requires the adenomatous polyposis coli tumor suppressor protein. J Neurosci 2004; 24: 6776–6784
  • Farías GG, Vallés AS, Colombres M, Godoy JA, Toledo EM, Lukas RJ, Barrantes FJ, Inestrosa NC. Wnt-7a induces presynaptic colocalization of α7-nicotinic acetylcholine receptors and adenomatous polyposis coli in hippocampal neurons. J Neurosci 2007; 27: 5313–5325
  • Kabbani N, Woll M, Levenson R, Lindstrom JM, Changeux J-P. Intracellular complexes of the β2 subunit of the nicotinic acetylcholine receptor in brain identified by proteomics. Proc Natl Acad Sci USA 2007; 104: 20570–20575
  • Marks MJ, Stitzel JA, Collins AC. Time course study of the effects of chronic nicotine infusion on drug response and brain function. J Pharmacol Exp Ther 1985; 235: 619–628
  • Schwartz RD, Kellar KJ. In vivo regulation of [3H]acetylcholine recognition sites in brain by nicotinic cholinergic drugs. J Neurochem 1985; 45: 427–433
  • Benwell MEM, Balfour DJK, Anderson JM. Evidence that tobacco smoking increases the density of (−)-[3H]nicotine binding sites in human brain. J Neurochem 1988; 50: 1243–1247
  • Marks MJ, Pauly JR, Gross SD, Deneris ES, Hermans-Borgmeyer I, Heinemann SF, Collins AC. Nicotine binding and nicotine receptor subunit RNA after chronic nicotine treatment. J Neurosci 1992; 12: 2765–2784
  • Peng X, Gerzanich V, Anand R, Whiting PJ, Lindstrom J. Nicotine-induced increase in neuronal nicotinic receptors results from a decrease in the rate of receptor turnover. Mol Pharmacol 1994; 46: 523–530
  • Zhang X, Gong Z-H, Hellstrom-Lindahl E, Nordberg A. Regulation of α4β2 nicotinic acetylcholine receptors in M10 cells following treatment with nicotinic agents. Neuroreport 1994; 6: 313–317
  • Bencherif M, Fowler K, Lukas R, Lippiello PM. Mechanisms of up-regulation of neuronal nicotinic acetylcholine receptors in clonal cell lines and primary cultures of fetal rat brain. J Pharmacol Exp Ther 1995; 275: 987–994
  • Gopalakrishnan M, Monteggia LM, Anderson DJ, Molinari EJ, Piattoni-Kaplan M, Donnelly-Roberts D, Arneric SP, Sullivan JP. Stable expression, pharmacologic properties and regulation of the human neuronal nicotinic acetylcholine α4β2 receptor. J Pharm Exp Ther 1996; 276: 289–297
  • Nashmi R, Dickinson ME, McKinney S, Jareb M, Labarca C, Fraser SE, Lester HA. Assembly of α4β2 nicotinic acetylcholine receptors assessed with functional fluorescently labeled subunits: effects of localization, trafficking, and nicotine-induced upregulation in clonal mammalian cells and in cultured midbrain neurons. J Neurosci 2003; 23: 11554–11567
  • Kuryatov A, Luo J, Cooper J, Lindstrom J. Nicotine acts as a pharmacological chaperone to up-regulate human α4β2 acetylcholine receptors. Mol Pharmacol 2005; 68: 1839–1851
  • Sallette J, Pons S, Devillers-Thiery A, Soudant M, Prado de Carvalho L, Changeux J-P, Corringer PJ. Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 2005; 46: 595–607
  • Kishi M, Steinbach JH. Role of agonist binding site in up-regulation of neuronal nicotinic α4β2 receptors. Mol Pharmacol 2006; 70: 2037–2044
  • Corringer P-J, Sallette J, Changeux J-P. Nicotine enhances intracellular nicotinic receptor maturation: a novel mechanism of neuronal plasticity?. J Physiol (Paris) 2006; 99: 162–171
  • Gaimarri A, Moretti M, Riganti L, Zanardi A, Clementi F, Gotti C. Regulation of neuronal nicotinic receptor traffic and expression. Brain Res Rev 2007; 55: 134–143
  • Nashmi R, Xiao C, Deshpande P, McKinney S, Grady SR, Whiteaker P, Huang Q, McClure-Begley T, Lindstrom JM, Labarca C, Collins AC, Marks MJ, Lester HA. Chronic nicotine cell specifically upregulates functional α4* nicotinic receptors: basis for both tolerance in midbrain and enhance long-term potentiation in perforant path. J Neurosci 2007; 27: 8202–8218
  • Wang F, Nelson ME, Kuryatov A, Olale F, Cooper J, Keyser K, Lindstrom J. Chronic nicotine treatment up-regulates human α3β2 but not α3β4 acetylcholine receptors stably transfected in human embryonic kidney cells. J Biol Chem 1998; 273: 28721–28732
  • Ridley DL, Rogers A, Wonnacott S. Differential effects of chronic drug treatment on α3* and α7 nicotinic receptor binding sites, in hippocampal neurones and SH-SY5Y cells. Br J Pharmacol 2001; 133: 1286–1295
  • Sallette J, Bohler S, Benoit P, Soudant M, Pons S, Le Novère N, Changeux J-P, Corringer PJ. An extracellular protein microdomain controls up-regulation of neuronal nicotinic acetylcholine receptors by nicotine. J Biol Chem 2004; 279: 18767–18775
  • Perry DC, Mao D, Gold AB, McIntosh JM, Pezzullo JC, Kellar KJ. Chronic nicotine differentially regulates α6- and β3-containing nicotinic cholinergic receptors in rat brain. J Pharm Exp Ther 2007; 322: 306–315
  • Mao D, Perry DC, Yasuda RP, Wolfe BB, Kellar KJ. The α4β2α5 nicotinic cholinergic receptor in rat brain is resistant to up-regulation by nicotine in vivo. J Neurochem 2007; 104: 446–456
  • Walsh H, Govind AP, Mastro R, Hoda JC, Bertrand D, Vallejo Y, Green WN. 2008. Upregulation of nicotinic receptors by nicotine varies with receptor subtype. J Biol Chem 283:6022–6032.
  • Cho C-H, Song W, Leitzell K, Teo E, Meleth AD, Quick MW, Lester RAJ. Rapid upregulation of α7 nicotinic acetylcholine receptors by tyrosine dephosphorylation. J Neurosci 2005; 25: 3712–2723
  • Massey KA, Zago WM, Berg DK. BDNF up-regulates α7 nicotinic acetylcholine receptor levels on subpopulations of hippocampal interneurons. Mol Cell Neurosci 2006; 33: 381–388
  • Liu Z, Tearle AW, Nai Q, Berg DK. Rapid activity-driven SNARE-dependent trafficking of nicotinic receptors on somatic spines. J Neurosci 2005; 25: 1159–1168
  • Wonnacott S. Presynaptic nicotinic ACh receptors. Trends Neurosci 1997; 20: 92–98
  • MacDermott AB, Role LW, Sigelbaum SA. Presynaptic ionotropic receptors and the control of transmitter release. Annu Rev Neurosci 1999; 22: 443–485
  • Berg DK, Shoop RD, Chang KT, Cuevas J, Nicotinic acetylcholine receptors in ganglionic transmission, in Handbook of Experimental Pharmacology, Vol. 144, Neuronal Nicotinic Receptors, Clementi F, Fornasari D, Gotti C,. Springer: Berlin, 2000; pp 247–267.
  • Jones S, Sudweeks S, Yakel JL. Nicotinic receptors in the brain: correlating physiology with function. Trends Neurosci 1999; 22: 555–561
  • Williams BM, Temburni MK, Levey MS, Bertrand S, Bertrand D, Jacob MH. The long internal loop of the α3 subunit targets nAChRs to subdomains within individual synapses on neurones in vivo. Nature Neurosci 1998; 1: 557–562
  • Temburni MK, Blitzblau RC, Jacob MH. Receptor targeting and heterogeneity at interneuronal nicotinic cholinerigic synapses in vivo. J Physiol 2000; 525: 21–29
  • Xu J, Zhu Y, Heinemann SF. Identification of sequence motifs that target neuronal nicotinic receptors to dendrites and axons. J Neurosci 2006; 26: 9780–9793
  • Kracun S, Harkness PC, Gibb AJ, Millar NS. 2008. Influence of M3-M4 intracellular domain upon nicotinic acetylcholine receptor assembly targeting and function. Br J Pharmacol [published on-line: doi: 10.1038/sj.bjp.0707676].
  • Wang J-M, Zhang L, Yao Y, Viroonchatapan N, Rothe E, Wang Z-Z. A transmembrane motif governs the surface trafficking of nicotinic acetylcholine receptors. Nature Neurosci 2002; 5: 963–970

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.