Antibodies as tools to study the structure of membrane proteins: The case of the nicotinic acetylcholine receptor

Annual Review of Biophysics and Biomolecular Structure

Volumn 25, Issue , 1996, Pages 197-229

  Conti Fine, Bianca M ^a   Lei, Sijin ^a   McLane, Kathryn E ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA DULUTH   (United States)

Author keywords

cholinergic receptor; ton channel superfamily; transmembrane topology

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; EPITOPE; GLUTAMATE RECEPTOR; GLYCINE RECEPTOR; NICOTINIC RECEPTOR; RECEPTOR ANTIBODY; RECEPTOR SUBUNIT;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; MODEL; PEPTIDE MAPPING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; RECEPTOR BINDING; REVIEW;

EID: 0029974176     PISSN: 10568700     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.bb.25.060196.001213     Document Type: Review

References (112)

1. Akabas MH, Kaufman K, Archdeacon P, Karlin A. 1994. Identification of acetylcholine receptor channel-lining residues in the entire M2 segment of the α subunit. Neuron 13:919-27
2. Akabas MH, Stauffer DA, Xu M, Karlin A. 1992. Acetylcholine receptor channel structure probed in cysteine-substitution mutants. Science 258:307-10
3. Albuquerque EX, Pereira EFR, Castro NG, Alkondon M. 1995. Neuronal nicotinic receptors: function, modulation and structure. Neuroscience 7:91-101
4. Anand R, Bason L, Saedi MS, Gerzanich V, Peng X, Lindstrom J. 1993. Reporter epitopes: a novel approach to examine transmembrane topology of integral membrane proteins applied to the alpha 1 subunit of the nicotinic acetylcholine receptor. Biochemistry 32:9975-84
5. Anderson DJ, Walter P, Blobel G. 1982. Signal recognition protein is required for the integration of acetylcholine receptor δ subunit, a transmembrane glycoprotein, into the endoplasmic reticulum membrane. J. Cell Biol. 93:501-6
6. Appel JR, Pinilla C, Niman H, Houghten R. 1990. Elucidation of discontinuous linear determinants in peptides. J. Immunol. 144:976-83
7. Bahouth SW, Wang H-Y, Malbon CC. 1991. Immunological approaches for probing receptor structure and function. Trends Biochem. Sci. 12:338-43
8. Barlow DJ, Edwards MS, Thornton JM. 1986. Continuous and discontinuous protein antigenic determinants. Nature 322:747-48
9. Bennett JA, Dingledine R. 1995. Topology profile for a glutamate receptor: three transmembrane domains and a channel-lining reentrant membrane loop. Neuron 14:373-84
10. Beroukhim R, Unwin N. 1995. Three-dimensional location of the main immunogenic region of the acetylcholine receptor. Neuron 15:1-20
11. Bertrand D, Devillers-Thiery A, Revah F, Galzi J-L, Hussy N, et al. 1992. Unconventional pharmacology of a neuronal nicotinic receptor mutated in the channel domain. Proc. Natl. Acad. Sci. USA 89:1261-65
12. Bertrand D, Galzi JL, Devillers-Thiery A, Bertrand S, Changeux JP. 1993. Mutations at two distinct sites within the channel domain M2 after calcium permeability of neuronal α7 nicotinic receptor. Proc. Natl. Acad. Sci. USA 90:6971-75
13. Betz H. 1990. Homology and analogy in transmembrane receptor design: lessons from synaptic membrane proteins. Biochemistry 29: 3591-99
14. Betz H. 1992. Structure and function of inhibitory glycine receptors. Q. Rev. Biophys. 25:381-94
15. Blanton MP, Cohen JB. 1994. Identifying the lipid-prptein interface of the Torpedo nicotinic acetylcholine receptor: secondary structure implications. Biochemistry 33:2859-72
16. Blanton MP, Raja SK, Lala AK, Cohen JB. 1995. Photolabeling Torpedo californica nicotinic acetylcholine receptor membranes with the hydrophobic probe [3H]diazofluorene. Biochemistry. Submitted
17. Brisson A, Unwin PNT. 1984. Tubular crystals of acetylcholine receptor. J. Cell Biol. 99:1202-11
18. Buller AL, Hastings GA, Kirkness EF, Fraser CM. 1994. Site-directed mutagensis of N-lnked glycosylation sites on the γ-aminobutyric acid type A receptor α1 subunit. Mol. Pharmacol. 46:858-65
19. A receptor subunits in label-fracture replicas of cultured rat cerebellar granule cells. Recept. Channels 2:143-53
20. Charnet P, Labarca C, Leonard R, Vogelaar NJ, Czyzk L, et al. 1990. An open channel blocker interacts with adjacent turns of α-helices in the nicotinic acetylcholine receptor. Neuron 4:87-95
21. Chaturvedi V, Donnelly-Roberts DL, Lentz TL. 1992. Substitution of Torpedo acetylcholine receptor α1-subunit residues with snake α1- and rat nerve α3-subunit residues in recombinant fusion proteins: effect on α-bungarotoxin binding. Biochemistry 31:1370-75
22. Chavez RA, Hall ZW. 1991. The transmembrane topology of the amino terminus of the a subunit of the nicotinic acetylcholine receptor. J. Biol. Chem. 266:15532-38
23. Chavez RA, Hall ZW. 1992. Expression of fusion proteins of the nicotinic acetylcholine receptor from mammalian muscle identifies the membrane-spanning regions in the α and δ subunits. J. Cell Biol. 116: 385-93
24. Cheetham JC, Raleigh DP, Griest RE, Redfield C, Dobson CM, Rees AR. 1991. Antigen mobility in the combining site of an anti-peptide antibody. Proc. Natl. Acad. Sci. USA 88:7968-72
25. Claudio T. 1989. Molecular genetics of acetylcholine receptor-channels. In Frontiers in Molecular Biology, ed. DM Glover, BD Hammes, pp. 63-142. Oxford, UK: IRL Press
26. Conti-Tronconi BM, McLane KE, Raftery MA, Grando SA, Protti MP, 1994. The nicotinic acetylcholine receptor: structure and autoimmune pathology. Crit. Rev. Biochem. Mol. Biol. 19:69-123
27. Corringer PJ, Galzi JL, Eisele JL, Bertrand S, Changeux J-P, Bertrand D. 1995. Identification of a new component of the agonist binding site of the nicotinic α1 homooligomeric receptor. J. Biol. Chem. 270:11749-52
28. Criado M, Hochschwender S, Sarin V, Fox VL, Lindstrom J. 1985. Evidence for unpredicted transmembrane domains in acetylcholine receptor subunits. Proc. Natl. Acad. Sci. USA 82:2004-8
29. Davies DR, Padlan EA, Sheriff S. 1990. Antibody-antigen complexes. Annu. Rev. Biochem. 59:439-73
30. Dennis M, Giraudat J, Kotzba-Hibert F, Goeldner M, Hirth C, et al. 1988. Amino acids of the Torpedo marmorata acetylcholine receptor a subunit labeled by a photoaffinity ligand for the acetylcholine binding site. Biochemistry 27:2346-57
31. 3H]quinacrine azide in the active state of the nicotinic acetylcholine receptor. J. Biol. Chem. 265:11017-29
32. Dougherty DA, Stauffer DA. 1990. Acetylcholine binding by a synthetic receptor: implications for biological recognition. Science 250:1558-60
33. Dwyer BP. 1991. Topological dispositions of lysine α380 and lysine γ486 in the acetylcholine receptor from Torpedo californica. Biochemistry 30:4105-12
34. Ebert B, Wafford KA, Whiting P. Krogsgaard-Larsen P, Kemp JA. 1994. Molecular pharmacology of γ-aminobutyric acid type A receptor agonists and partial agonists in oocytes injected with different α, β and γ receptor subunit combinations. Mol. Pharmacol. 46:957-63
35. Eisele J-L, Bertrand S, Galzi J-L, Devillers-Thiery A, Changeux J-P, Bertrand D. 1993. Chimaeric nicotinic-serotonergic receptor combines distinct ligand binding and channel specificities. Nature 366:479-83
36. Fairclough RH, Finer-Moore J, Love RA, Kristofferson D, Desmeules PJ, Stroud RM. 1983. Subunit organization and structure of an acetylcholine receptor. Cold Spring Harbor Symp. Quant. Biol. 68:9-20
37. Finer-Moore J, Stroud R. 1984. Amphipathic analysis and possible formation of the ion channel in an acetylcholine receptor. Proc. Natl. Acad. Sci. USA 81:155-59
38. Galzi J-L, Devillers-Thiery A, Hussy N, Bertrand S, Changeux J-P, Bertrand D. 1992. Mutations in the channel domain of a neuronal nicotinic receptor convert ion selectivity from cationic to anionic. Nature 359: 500-5
39. Galzi J-L, Revah F. Bessis A, Changeux J-P. 1991. Functional architecture of the nicotinic acetylcholine receptor: from electric organ to brain. Annu. Rev. Pharmacol. 31: 37-72
40. Ghosh P, Stroud RM. 1991. Ion channels formed by a highly charged peptide. Biochemistry 30:3551-57
41. Gorne-Tschelnokow U, Strecker A, Kaduk C, Naumann D, Hucho F. 1994. The transmembrane domains of the nicotinic acetylcholine receptor contain α-helical and β structures. EMBO J. 13:338-41
42. Hartman DS, Claudio T. 1990. Coexpression of two distinct muscle acetylcholine receptor a subunits during development. Nature 343:372-73
43. Helekar SA, Char D, Neff S, Patrick J. 1994. Prolyl isomerase requirement for the expression of functional homo-oligomeric ligand-gated ion channels. Neuron 12:179-89
44. Hollmann M, Heinemann S. 1994. Cloned glutamate receptors. Annu. Rev. Neurosci. 17:31-108
45. Hollmann M, Maron C, Heinemann S. 1994. N-glycosylation site tagging suggests a three transmembrane domain topology for the glutamate receptor GluR1. Neuron 13:1331-43
46. Imoto K, Busch C, Sakmann B, Mishina M, Konno T, et al. 1988. Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance. Nature 335: 645-48
47. Imoto KJ, Konno T, Nakai J, Wang F, Misha M, Numa S. 1991. A ring of uncharged polar amino acids as a component of channel constriction in the nicotinic acetylcholine receptor. FEBS Lett. 289:193-200
48. Karlin A. 1993. Structure of nicotinic acetylcholine receptors. Curr. Opin. Neurobiol. 3:299-309
49. A/benzodiazepine receptor from rat cerebellum. J. Neurochem. 63:371-74
50. Konno T, Busch C, Von Kitzing E, Imoto K, Wang F, et al. 1991. Rings of anionic amino acids as structural determinants of ion selectivity in the acetylcholine receptor channel. Proc. R. Soc. London Ser. B 244:69-79
51. Kuhse J, Laube B, Magalei D, Betz H. 1993. Assembly of the inhibitory glycine receptor: identification of amino acid sequence motifs governing subunit stoichiometry. Neuron 11:1049-56
52. Kuryatov A, Laube B, Betz H, Kuhse J. 1994. Mutational analysis of the glycine-binding site of the NMDA receptor: structural similarity with bacterial amino acid-binding proteins. Neuron 12:1291-1300
53. Langosch D, Hartung K, Grell E, Bamberg E, Betz H. 1991. Ion channel formation by synthetic transmembrane segments of the inhibitory glycine receptor - a model study. Biochim. Biophys. Acta 1063:35-44
54. Langosch D, Laube B, Rundstrom N, Schmieden V, Bormann J, Betz H. 1994. Decreased agonist affinity and chloride conductance of mutant glycine receptors associated with human hereditary hyperekplexia. EMBO J. 13:4223-28
55. Lei S, Raftery MA, Conti-Tronconi BM. 1993. Monoclonal antibodies against synthetic sequences of the nicotinic receptor cross-react fully with the native receptor and reveal the transmembrane disposition of their epitopes. Biochemistry 32:91-100
56. Lentz TL, Wilson PT. 1988. Neurotoxin-binding site on the acetylcholine receptor. Int. Rev. Neurobiol. 29: 117-60
57. Leonard RJ, Labarca CG, Charnet P, Davidson N, Lester HA. 1988. Evidence that the M2 membrane-spanning region lines the ion channel pore of the nicotinic receptor. Science 242:1578-81
58. Liddington RC, Yan Y, Moulai J, Sahli R, Benjamin TL, Harrison SC. 1991. Structure of simian virus 40 at 3.8-Å resolution. Nature 354:278-84
59. Lindstrom J, Anand R, Peng X, Gerzanich V, Wang F, Yuebing L. 1995. Neuronal nicotinic receptor subtypes. Ann. NY Acad. Sci. 757:100-16
60. MacDonald RL. 1995. Ethanol, γ-aminobutyrate type A receptors, and protein kinase C phosphorylation. Proc. Natl. Acad. Sci. USA 92: 3633-35
61. A receptor channels. Annu. Rev. Neurosci. 17:569-602
62. MacKinnon R. 1995. Pore loops: an emerging theme in ion channel structure. Neuron 14:889-92
63. McLane KE, Wahlsten JL, Conti-Tronconi BM. 1993. Use of synthetic sequences of the nicotinic acetylcholine receptor to identify structural determinants of binding sites for neurotoxins and antibodies to the main immunogenic region. Methods: Companion Methods Enzymol. 5: 201-11
64. Mihic SJ, Whiting PJ, Klein RL, Wafford KA, Harris RA. 1994. A single amino acid of the human γ-aminobutyric acid type A receptor γ2 subunit determines benzodiazepine efficacy. J. Biol. Chem. 269: 32768-73
65. Molnar E, McIlhinney J, Baude A, Nusser Z, Somogyi P. 1994. Membrane topology of the GluR1 glutamate receptor subunit: epitope mapping by site-directed antipeptide antibodies. J. Neurochem. 63: 683-93
66. Moore CR, Yates JR III, Griffin PR, Shabanowitz J, Martino PA, et al. 1989. Proteolytic fragments of the nicotinic acetylcholine receptor identified by mass spectrometry: implications for receptor topography. Biochemistry 28:9184-91
67. Mulac-Jericevic B, Kurisaki J, Atassi MZ. 1987. Profile of the continuous antigenic regions on the extracellular part of the a chain of an acetylcholine receptor. Proc. Natl. Acad. Sci. USA 84:3633-37
68. A receptor determined by electron microscopic image analysis. J. Neurochem. 62: 815-18
69. Ohno K, Hutchinson DO, Milone M, Brengman JM, Bouzat C, et al. 1995. Congenital myasthenic syndrome caused by prolonged acetylcholine receptor channel openings due to a mutation in the M2 mutation in the e subunit. Proc. Natl. Acad. Sci. USA 92:758-62
70. O'Leary ME, Filatov GN, White MM. 1994. Characterization of δ-tubocurarine binding site of Torpedo acetylcholine receptor. Am. J. Physiol. 266:C648-53
71. Quirk K, Gillard NP, Ragan CI, Whiting P, McKernan K.M. 1994. Model of subunit composition of γ-aminobutyric acid A receptor subtypes expressed in rat cerebellum with respect to their a and γ/δ subunits. J. Biol. Chem. 269:16020-28
72. Rajendra S, Lynch JW, Pierce KD, French CR, Barry PH, Schofield PR. 1994. Startle disease mutations reduce the agonist sensitivity of the human inhibitory glycine receptor. J. Biol. Chem. 269:18739-42
73. Rajendra S, Lynch JW, Pierce KD, French CR, Barry PH, Schofield PR. 1995. Mutation of an arginine residue in the human glycine receptor transforms β-alanine and taurine from agonists in competitive antagonists. Neuron 14:169-75
74. Ratnam M, Manohar, Le Nguyen D, Rivier J, Sargent PB, Lindstrom J. 1986. Transmembrane topography of nicotinic acetylcholine receptor: immunochemical tests contradict theoretical predictions based on hydrophobicity profiles. Biochemistry 25: 2633-43
75. Reddy GL, Iwamoto T, Tomich JM, Montai M. 1993. Synthetic peptides and four-helix bundel proteins as model systems for the pore-forming structure of channel proteins. II. transmembrane segment M2 of the brain glycine receptor is a plausible candidate for the pore-lining structure. J. Biol. Chem. 268:14608-15
76. Revah F, Bertrand D, Galzi J-L, Devillers-Thiery A, Mulle C, et al. 1991. Mutations in the channel domain after desensitization of a neuronal nicotinic receptor. Nature 353: 846-49
77. Rini JM, Schulze-Gahmen U, Wilson IA. 1992. Structural evidence for induced fit as a mechanism for antibody-antigen recognition. Science 255:959-65
78. Roche KW, Raymond LA, Blackstone C, Huganir RL. 1994. Transmembrane topology of the glutamate receptor subunit GluR6. Proc. Natl. Acad. Sci. USA 269:11679-82
79. Roche KW, Tingley WG, Huganir RL. 1994. Glutamate receptor phosphorylation and synaptic plasticity. Curr. Opin. Neurobiol. 4:383-88
80. Roth B, Schwendimann B, Hughes CJ, Tzartos SJ, Barkas T. 1987. A modified nicotinic acetylcholine receptor lacking the ion channel amphipatic helices. FEBS Lett. 221:172-78
81. Ruiz-Gomez A, Vaello M-L, Valdivieso F, Mayor F Jr. 1991. Phosphorylation of the 48-kDa subunit of the glycine receptor by protein kinase C. J. Biol. Chem. 266:559-66
82. Sargent PB. 1993. The diversity of neuronal nicotinic acetylcholine receptors. Annu. Rev. Neurosci. 16: 403-43
83. Saul B, Schmieden V, Kling C, Mulhardt C, Gass P, et al. 1994. Point mutation of glycine receptor α1 subunit in the spasmodic mouse affects agonist responses. FEBS Lett. 350: 71-76
84. Schmieden V, Kuhse J, Betz H. 1993. Mutation of glycine receptor subunit creates β-alanine receptor responsive to GABA. Science 262:256-58
85. Schroeder B, Reinhardt-Maelicke S, Schrattenholz A, McLane KE, Conti-Tronconi BM, Maelicke A. 1994. Monoclonal antibodies WF6 and FK1 define two neighboring ligand binding sites on Torpedo acetylcholine receptor α polypeptide. J. Biol. Chem. 269:10407-16
86. Schroder S, Hoch W, Beacker C-M, Grenningloh G, Betz H. 1991. Mapping of antigenic epitopes on the α1 subunit of the inhibitory glycine receptor. Biochemistry 30:42-47
87. Smith GB, Olsen RW. 1994. Identification of a [3H]muscimol photoaffinity substrate in the bovine γ-aminobutyric acid A receptor α subunit. J. Biol. Chem. 268:20380-87
88. Spangler BD. 1991. Binding to native proteins by antipeptide monoclonal antibodies. J. Immunol. 146:1591-95
89. Stern-Bach Y, Bettler B, Hartley M, Sheppard PO, O'Hara PJ, Heinemann S. 1994. Agonist selectivity of glutamate receptors is specified by two domains structurally related to bacterial amino acid-binding proteins. Neuron 13:1345-57
90. Stroud RM, McCarthy MP, Shuster M. 1990. Nicotinic acetylcholine receptor superfamily of ligand-gated ion channels. Biochemistry 29: 11009-23
91. Sussman JL, Harel M, Frolow F, Oefner C, Goldman A, et al. 1991. Atomic structure of acetylcholinesterase from Torpedo californica: a prototypic acetylcholine-binding protein. Science 253:872-79
92. Taverna FA, Wang L-Y, MacDonald JF, Hampson DR. 1994. A transmembrane model for an ionotropic glutamate receptor predicted on the basis of the location of asparagine-linked oligosaccharides. J. Biol. Chem. 269: 14159-64
93. Tomaselli GF, McLaughlin JT, Jurman ME, Hawrot E, Yellen G. 1991. Mutations affecting agonist sensitivity of the nicotinic acetylcholine receptor. Biophys. J. 60:721-24
94. Twyman RE, Gahring LC, Spiess J, Rogers SW. 1995. Glutamate receptor antibodies activate a subset of receptors and reveal an agonist binding site. Neuron 14:755-62
95. Tzartos SJ, Kokla H, Walgrave S, Conti-Tronconi BM. 1988. The main immunogenic region of human muscle acetylcholine receptor is localized within residues 67-76 of the α subunit. Proc. Natl. Acad. Sci. USA 85: 2899-903
96. Tzartos SJ, Kouvatsou R, Tzartos E. 1995. Monoclonal antibodies as site-specific probes for the acetylcholine receptor δ subunit tyrosine and serine phosphorylation sites. Eur. J. Biochem. 228:463-72
97. Tzartos SJ, Loutrari HV, Tang F, Kokla A, Walgrave SL, et al. 1990. Main immunogenic region of Torpedo electroplax and human muscle acetylcholine receptor: localization and microheterogeneity revealed by the use of synthetic peptides. J. Neurochem. 54:51-61
98. Tzartos SJ, Remoundos MS. 1990. Fine localization of the major α-bungarotoxin binding site to residues α189-195 of the Torpedo acetylcholine receptor: residues 189, 190, and 195 are indispensable for binding. J. Biol. Chem. 265:21462-67
99. Tzartos, SJ, Tzartos E, Kouvatsou, R. 1995. Acetylcholine receptor tyrosine and serine phosphorylation. Monoclonal antibodies as site-specific tools for phosphorylation and channel function. Proc. Int. Symp. Cholinergic Synapse: Structure, Function, and Regulation Site, p. S16
100. Tzartos SJ, Valcana C, Kouvatsou R, Kokla A. 1993. The tyrosine phosphorylation site of the acetylcholine receptor β subunit is located in a highly immunogenic epitope implicated in channel function: antibody probes for β subunit phosphorylation and function. EMBO J. 12:5141-49
101. Uchino S, Sakimura K, Naganari K, Mishina M. 1992. Mutations in a putative agonist binding region of the AMPA-selective glutamate receptor channel. FEBS Lett. 308:253-57
102. Unwin N. 1993. Nicotinic acetylcholine receptor at 9Å resolution. J. Mol. Biol. 229:1101-24
103. Unwin N. 1995. Acetylcholine receptor channel imaged in the open state. Nature 373:37-43
104. Van Regenmortel MHV. 1989. Structural and functional approaches to the study of protein antigenicity. Immunol. Today 10:266-72
105. Vandenberg RJ, Rajendra S, French CR, Barry PH, Scofield PR. 1993. The extracellular disulfide loop motif of the inhibitory glycine receptor does not form the agonist binding site. Mol. Pharmacol. 44:198-203
106. Wang T-L, Guggino WB, Cutting GR. 1994. A novel γ-aminobutyric acid receptor subunit (ρ2) cloned from human retina forms bicuculline-insensitive homooligomeric receptors in Xenopus oocytes. J. Neurosci. 14:6524-31
107. A receptors is essential for benzodiazepine agonist binding. J. Biol. Chem. 267:1426-29
108. Wennogle LP, Changeux J-P. 1980. Transmembrane orientation of proteins present in acetylcholine receptor rich membranes from Torpedo marmorata studied by selective proteolysis. Eur. J. Biochem. 106: 381-93
109. White BH, Cohen JB. 1992. Agonist-induced changes in the structure of the acetylcholine receptor M2 regions revealed by photoincorporation of an uncharged nicotinic noncompetitive antagonist. J. Biol. Chem. 267: 15770-83
110. Wingrove PB, Wafford KA, Bain C, Whiting PJ. 1994. The modulatory action of loreclezole at the γ-aminobutyric acid type A receptor is determined by a single amino acid in the β2 and β3 subunit. Proc. Natl. Acad. Sci. USA 91:4569-73
111. A receptor channels: from subunits to functional entities. Curr. Opin. Neurobiol. 2:263-69
112. Wisden W, Seeburg PH. 1993. Mammalian ionotropic glutamate receptors. Curr. Opin. Neurobiol. 3: 291-98