N-Glycosylation at the conserved sites ensures the expression of properly folded functional ACh receptors

Molecular Brain Research

Volumn 45, Issue 2, 1997, Pages 219-229

  Gehle, Vaughn M ^a,b   Walcott, Elisabeth C ^a   Nishizaki, Tomoyuki ^a,c   Sumikawa, Katumi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c KOBE UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

ACh receptor; Assembly; N glycosylation; Toxin binding site; Xenopus oocyte

Indexed keywords

ALPHA BUNGAROTOXIN; CARBOHYDRATE; CHOLINERGIC RECEPTOR; ION CHANNEL; MEMBRANE RECEPTOR; MONOCLONAL ANTIBODY; MUTANT PROTEIN; PROTEIN SUBUNIT;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG RECEPTOR BINDING; IMMUNOPRECIPITATION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; SITE DIRECTED MUTAGENESIS; XENOPUS;

ACETYLCHOLINE; AMINO ACID SEQUENCE; ANIMALS; ASPARAGINE; ASPARTIC ACID; BINDING SITES; BUNGAROTOXINS; CLONING, MOLECULAR; CONSERVED SEQUENCE; FEMALE; GLYCOSYLATION; ION CHANNELS; KINETICS; MACROMOLECULAR SUBSTANCES; MEMBRANE POTENTIALS; OOCYTES; PATCH-CLAMP TECHNIQUES; POINT MUTATION; PROTEIN FOLDING; RECEPTORS, CHOLINERGIC; RNA, MESSENGER; XENOPUS LAEVIS;

EID: 0031149753     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(96)00256-2     Document Type: Article

References (39)

1. Anderson, D.J. and Blobel, G., In vitro synthesis, glycosylation, and membrane insertion of the four subunits of Torpedo acetylcholine receptor, Proc. Natl. Acad. Sci. USA, 78 (1981) 5598-5602.
2. Blount, P. and Merlie, J.P., Molecular basis of the two nonequivalent ligand binding sites of the muscle nicotinic acetylcholine receptor, Neuron, 3 (1989) 349-357.
3. Blount, P., Smith, M.M. and Merlie, J.P., Assembly intermediates of the mouse muscle nicotinic acetylcholine receptor in stably transfected fibroblasts, J. Cell Biol., 111 (1990) 2601-2611.
4. Colman, A., Transcription & translation, a practical approach. In S.J. Hames (Ed.), B.D.A.H., IRL Press, Oxford, UK, 1984, pp. 271-302.
5. Conroy, W.G., Saedi, M.S. and Lindstrom, J., TE671 cells express an abundance of a partially mature acetylcholine receptor alpha subunit which has characteristics of an assembly intermediate, J. Biol. Chem., 265 (1990) 21642-21651.
6. Conti-Tronconi, B.M., McLane, K.E., Raftery, M.A., Grando, S.A. and Protti, M.P., The nicotinic acetylcholine receptor: structure and autoimmune pathology, Crit. Rev. Biochem. Mol. Biol., 29 (1994) 69-123.
7. Devillers-Thiery, A., Galzi, J.L., Eisele, J.L., Bertrand, S., Bertrand, D. and Changeux, J.-P., Functional architecture of the nicotinic acetylcholine receptor: A prototype of ligand-gated ion channels, J. Membr. Biol., 136 (1993) 97-112.
8. Dowding, A.J. and Hall, Z.W., Monoclonal antibodies specific for each of the two toxin-binding sites of Torpedo acetylcholine receptor, Biochemistry, 26 (1987) 6372-6381.
9. Fambrough, D.M., Lemas, M.V., Hamrick, M., Emerick, M., Renaud, K.J., Inman, E.M., Hwang, B. and Takeyasu, K., Analysis of subunit assembly of the Na-K-ATPase, Am. J. Physiol., 266 (1994) C579-C589.
10. Garcia-Guzman, M., Sala, F., Sala, S., Campos-Caro, A. and Criado, M., Role of two acetylcholine receptor subunit domains in homomer formation and intersubunit recognition, as revealed by alpha 3 and alpha 7 subunit chimeras, Biochemistry, 33 (1994) 15198-15203.
11. Gehle, V.M. and Sumikawa, K., Site-directed mutagenesis of the conserved N-glycosylation site on the nicotinic acetylcholine receptor subunits, Brain Res. Mol. Brain Res., 11 (1991) 17-25.
12. Gelman, M.S., Chang, W., Thomas, D.Y., Bergeron, J.J. and Prives, J.M., Role of the endoplasmic reticulum chaperone calnexin in subunit folding and assembly of nicotinic acetylcholine receptors, J. Biol. Chem., 270 (1995) 15085-15092.
13. Green, W.N. and Claudio, T., Acetylcholine receptor assembly: Subunit folding and oligomerization occur sequentially, Cell, 74 (1993) 57-69.
14. Green, W.N. and Millar, N.S., Ion-channel assembly, Trends Neurosci., 18 (1995) 280-287.
15. Gu, Y., Forsayeth, J.R., Verrall, S., Yu, X.M. and Hall, Z.W., Assembly of the mammalian muscle acetylcholine receptor in transfected COS cells, J. Cell Biol., 114 (1991) 799-807.
16. Kao, P.N. and Karlin, A., Acetylcholine receptor binding site contains a disulfide cross-link between adjacent half-cystinyl residues, J. Biol. Chem., 261 (1986) 8085-8088.
17. Kellaris, K.V., Ware, D.K., Smith, S. and Kyte, J., Assessment of the number of free cysteines and isolation and identification of cystine-containing peptides from acetylcholine receptor, Biochemistry, 28 (1989) 3469-3482.
18. Merlie, J.P., Hofler, J.G. and Sebbane, R., Acetylcholine receptor synthesis from membrane polysomes, J. Biol. Chem., 256 (1981) 6995-6999.
19. Merlie, J.P. and Lindstrom, J., Assembly in vivo of mouse muscle acetylcholine receptor: Identification of an alpha subunit species that may be an assembly intermediate, Cell, 34 (1983) 747-757.
20. Merlie, J.P. and Smith, M.M., Synthesis and assembly of acetylcholine receptor, a multisubunit membrane glycoprotein, J. Membr. Biol., 91 (1986) 1-10.
21. Nomoto, H., Takahashi, N., Nagaki, Y., Endo, S., Arata, Y. and Hayashi, K., Carbohydrate structures of acetylcholine receptor from Torpedo californica and distribution of oligosaccharides among the subunits, Eur. J. Biochem., 157 (1986) 233-242.
22. Numa, S., Noda, M., Takahashi, H., Tanabe, T., Toyosato, M., Furutani, Y. and Kikyotani, S., Molecular structure of the nicotinic acetylcholine receptor, Cold Spring Harb. Symp. Quant. Biol., 1 (1983) 57-69.
23. Ochoa, E.L., Chattopadhyay, A. and McNamee, M.G., Desensitization of the nicotinic acetylcholine receptor: Molecular mechanisms and effect of modulators, Cell. Mol. Neurobiol., 9 (1989) 141-178.
24. Paulson, H.L., Ross, A.F., Green, W.N. and Claudio, T., Analysis of early events in acetylcholine receptor assembly, J. Cell Biol., 113 (1991) 1371-1384.
25. Ross, A.F., Green, W.N., Hartman, D.S. and Claudio, T., Efficiency of acetylcholine receptor subunit assembly and its regulation by cAMP, J. Cell Biol., 113 (1991) 623-636.
26. Ross, A.F., Rapuano, M., Schmidt, J.H. and Prives, J.M., Phosphorylation and assembly of nicotinic acetylcholine receptor subunits in cultured chick muscle cells, J. Biol. Chem., 262 (1987) 14640-14647.
27. Saedi, M.S., Conroy, W.G. and Lindstrom, J., Assembly of Torpedo acetylcholine receptors in Xenopus oocytes, J. Cell Biol., 112 (1991) 1007-1015.
28. Sakmann, B., Methfessel, C., Mishina, M., Takahashi, T., Takai, T., Kurasaki, M., Fukuda, K. and Numa, S., Role of acetylcholine receptor subunits in gating of the channel, Nature (London), 318 (1985) 538-543.
29. Smith, M.M., Lindstrom, J. and Merlie, J.P., Formation of the α-bungarotoxin binding site and assembly of the nicotinic acetylcholine receptor subunits occur in the endoplasmic reticulum, J. Biol. Chem., 262 (1987) 4367-4376.
30. Sumikawa, K., Sequences on the N-terminus of ACh receptor subunits regulate their assembly, Brain Res. Mol. Brain Res., 13 (1992) 349-353.
31. Sumikawa, K. and Gehle, V.M., Assembly of mutant subunits of the nicotinic acetylcholine receptor lacking the conserved disulfide loop structure, J. Biol. Chem., 267 (1992) 6286-6290.
32. Sumikawa, K. and Miledi, R., Assembly and N-glycosylation of all ACh receptor subunits are required for their efficient insertion into plasma membranes, Brain Res. Mol. Brain Res., 5 (1989) 183-192.
33. Sumikawa, K. and Nishizaki, T., The amino acid residues 1-128 in the alpha subunit of the nicotinic acetylcholine receptor contain assembly signals, Brain Res. Mol. Brain Res., 25 (1994) 257-264.
34. Verrall, S. and Hall, Z.W., The N-terminal domains of acetylcholine receptor subunits contain recognition signals for the initial steps of receptor assembly, Cell, 68 (1992) 23-31.
35. Walcott, E. and Sumikawa, K., A conserved disulfide loop in the subunits of the acetylcholine receptor facilitates correct subunit coupling, Brain Res. Mol. Brain. Res., in press.
36. White, M.M., Mayne, K.M., Lester, H.A. and Davidson, N., Mouse-Torpedo hybrid acetylcholine receptors: Functional homology does not equal sequence homology, Proc. Natl. Acad. Sci. USA, 82 (1985) 4852-4856.
37. Yu, X.M. and Hall, Z.W., Extracellular domains mediating epsilon subunit interactions of muscle acetylcholine receptor, Nature (London), 352 (1991) 64-67.
38. Yu, X.M. and Hall, Z.W., Amino- and carboxyl-terminal domains specify the identity of the delta subunit in assembly of the mouse muscle nicotinic acetylcholine receptor, Mol. Pharmacol., 46 (1994) 964-969.
39. Yu, X.M. and Hall, Z.W., A sequence in the main cytoplasmic loop of the α subunit is required for assembly of mouse muscle nicotinic acetylcholine receptor, Neuron, 13 (1994) 247-255.