Physicochemical and immunological studies of the N-terminal domain of the Torpedo acetylcholine receptor α-subunit expressed in Escherichia coli

European Journal of Biochemistry

Volumn 259, Issue 1-2, 1999, Pages 310-319

  Alexeev, Timophey ^a   Krivoshein, Arcadius ^a   Shevalier, Alexander ^a   Kudelina, Irina ^a   Telyakova, Olga ^a   Vincent, Angela ^b   Utkin, Yuri ^a   Hucho, Ferdinand ^c   Tsetlin, Victor ^a  

^a SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^c FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Expression in E. coli; MALDI mass spectrometry; Nicotimc acetylcholine receptor; Torpedo subunit domain

Indexed keywords

CHOLINERGIC RECEPTOR; RECEPTOR SUBUNIT;

AMINO TERMINAL SEQUENCE; ARTICLE; CONTROLLED STUDY; ELECTRIC ORGAN; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DETERMINATION; PROTEIN DOMAIN; TORPEDO CALIFORNICA;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; BUNGAROTOXINS; CHOLINERGIC AGENTS; CIRCULAR DICHROISM; DECAMETHONIUM COMPOUNDS; ELECTRIC ORGAN; ESCHERICHIA COLI; MOLECULAR SEQUENCE DATA; NICOTINIC ANTAGONISTS; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, NICOTINIC; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TORPEDO; TUBOCURARINE;

ESCHERICHIA COLI; MAMMALIA; TORPEDO CALIFORNICA;

EID: 0033555679     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1999.00041.x     Document Type: Article

References (61)

1. Changeux, J.-P. (1990) Functional architecture and dynamics of the nicotinic acetylcholine receptor: a ligand-gated ion channel. In: Fidia Research Foundation Neurosience Award Lectures, 4. Raven, New York, pp. 21-168.
2. Karlin, A. & Akabas, M.H. (1995) Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron 15, 1231-1244.
3. Hucho, F., Tsetlin, V.I. & Machold, J. (1996) The emerging three-dimensional structure of a receptor. The nicotinic acetylcholine receptor. Eur. J. Biochem. 239, 539-557.
4. Yu, X.M. & Hall, Z.W. (1994) The role of the cytoplasmic domains of individual subunits of the acetylcholine receptor in 43 kDa protein-induced clustering in COS cells. J. Neurosci. 14, 785-795.
5. Hucho, F., Oberthür, W. & Lottspeich, F. (1986) The ion channel of the nicotinic acetylcholine receptor is formed by the homologous helices M II of the receptor subunits. FEBS Lett. 205, 137-142.
6. 3H]chlorpromazine. Proc. Natl Acad. Sci. USA 83, 2719-2723.
7. 3H]quinacrine azide in the active site of the nicotinic acetylcholine receptor. J. Biol. Chem. 265, 11017-11029.
8. Akabas, M.H. & Karlin, A. (1995) Identification of acetyclholine receptor channel-lining residues in the M1 segment of the α-subunit. Biochemistry 34, 12496-12500.
9. Pedersen, S.E. & Cohen, J.B. (1990) d-Tubocurarine binding sites are located at α-γ and α-δ subunit interfaces of the nicotinic acetylcholine receptor. Proc. Natl Acad. Sci. USA 87, 2785-2789.
10. Blount, P. & Merlie, J.P. (1989) Molecular basis of the two nonequivalent ligand binding sites of the muscle nicotinic acetylcholine receptor. Neuron 3, 349-357.
11. Kreienkamp, H.-J., Utkin, Y.N., Weise, C., Machold, J., Tsetlin, V.I. & Hucho, F. (1992) Investigation of ligand binding sites of the acetylcholine receptor using photoactivable derivatives of neurotoxin II from Naja naja oxiana. Biochemistry 31, 8239-8244.
12. Utkin, Y.N., Kobayashi, Y., Hucho, F. & Tsetlin, V.I. (1994) Relationships between the binding sites for an α-conotoxin and snake venom toxins in the nicotinic acetylcholine receptor from Torpedo californica. Toxicon 32, 1153-1157.
13. Hann, R.M., Pagan, O.R. & Eteruvic, V.A. (1994) The α-conotoxins GI and MI distinguish between the nicotinic acetylcholine receptor agonist sites while SI does not. Biochemistry 33, 14058-14063.
14. Klymkowsky, M.W. & Stroud, R.M. (1979) Immunospecific identification and three-dimensional structure of a membrane-bound acetylcholine receptor from Torpedo californica. J. Mol. Biol. 128, 319-334.
15. Unwin, N. (1993) Nicotinic acetylcholine receptor at 9 Å resolution. J. Mol. Biol. 229, 1101-1124.
16. Unwin, N. (1996) Projection structure of the nicotinic acetylcholine receptor: distinct conformation of the α subunits. J. Mol. Biol. 257, 586-596.
17. Gershoni, J.M., Hawrot, E. & Lentz, T.L. (1983) Binding of α-bungarutoxin to isolated α-subunit of the acetylcholine receptor of Torpedo californica: quantitative analysis with protein blots. Proc. Natl Acad. Sci. USA 80, 4973-4977.
18. Neumann, D., Barchan, D., Fridkin, M. & Fuchs, S. (1986) Analysis of ligand binding to the synthetic dodecapeptide 185-196 of the acetylcholine receptor α-subunit. Proc. Natl Acad. Sci. USA 83, 9250-9253.
19. Wilson, P.T., Lentz, T.L. & Hawrot, E. (1985) Determination of the primary amino acid sequence specifying the α-bingarotoxin binding site on the α subunit of the acetylcholine receptor from Torpedo californica. Proc. Natl Acad. Sci. USA 82, 8790-8794.
20. Barkas, T., Mauron, A., Roth, B., Alliod, C., Tzartos, S.J. & Ballivet, M. (1987) Mapping the main immunogenic and toxin-binding site of the nicotinic acetylcholine receptor. Science 235, 77-80.
21. Telyakova, O.V., Utkin, Yu. N., Tsetlin, V.I., Severtsova, I.V. & Zvonok, N.M. (1994) Expression of a fragment of the Torpedo californica acetylcholine receptor α-subunit gene in Saccharomyces cerevisiae. Bioorg. Khim. 20, 546-550.
22. Aronheim, A., Eshel, Y., Mosckovitz, R. & Gershoni, J.M. (1988) Characterization of the binding of α-bungarotoxin to bacterially expressed cholinergic binding sites. J. Biol. Chem. 263, 9933-9937.
23. West, A.P., Jr, Bjorkman, P.J., Dougherty, D.A. & Lester, H.A. (1997) Expression and circular dichroism studies of the extracellular domain of the α-subunit of the nicotinic acetylcholine receptor. J. Biol. Chem. 272, 25468-25473.
24. Klukas, O., Peshenko, I.A., Rodionov, I.L., Telyakova, O.V., Utkin, Yu.N. & Tsetlin, V.I. (1995) Fragments 183-196 and 125-145 of the α-subunit of the nicotinic acetylcholine receptor from Torpedo californica bind α-bungarotoxin and neurotoxin II Naja naja oxiana. Bioorg. Khim. 21, 152-155.
25. Schiebler, W., Lauffer, L. & Hucho, F. (1977) Acetylcholine receptor enriched membranes: acetylcholine binding and exitability after reduction in vitro. FEBS Lett. 81, 39-42.
26. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
27. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
28. Mach, H., Middaugh, C.R. & Lewis, R.V. (1992) Statistical determination of the average values of the extinction coefficients of tryptophan and tyrosine in native proteins. Anal. Biochem. 200, 74-80.
29. Whitaker, J.R. & Granum, P.E. (1980) An absolute method for protein determination based on difference in absorbance at 235 and 280 nm. Anal Biochem. 109, 156-159.
30. Provencher, S.W. (1982) A constrained regularization method for inverting data represented by linear algebraic or integral equations. Comput. Phys. Commun. 27, 213-227.
31. Provencher, S.W. (1982) CONTIN: a general purpose constrained regularization program for inverting noisy linear algebraic and integral equations. Comput. Phys. Commun. 27, 229-242.
32. Schmidt, J. & Raftery, M.A. (1973) A simple assay for the study of solubilized acetylcholine receptors. Anal. Biochem. 52, 349-354.
33. Kachalsky, S.G., Jensen, B.S., Barchan, D. & Fuchs, S. (1995) Two subsites in the binding domain of the acetylcholine receptor: an aromatic subsite and a proline subsite. Proc. Natl Acad. Sci. USA 7, 10801-10805.
34. Utkin, Yu. N., Mund, M., Hucho, F. & Tsetlin, V.I. (1996) Efficient binding of α-bungarotoxin by a solubilized α-subunit of the Torpedo californica acetylcholine receptor. Bioorg. Khim. 22, 387-389.
35. 125I-α-bungarotoxin binding activity to the α-subunit of Torpedo acetylcholine receptor isolated by gel electrophoresis in sodium dodecyl sulfate. J. Biol. Chem. 256, 8294-8297.
36. Tzartos, S.J. & Changeux, J.-P. (1983) High affinity binding of α-bungarotoxin to the purified α-subunit and to its 27000-dalton proteolytic peptide from Torpedo marmorata acetylcholine receptor. Requirement for sodium dodecyl sulfate. EMBO J. 2, 381-387.
37. Shtrom, S.S. & Hall, Z.W. (1996) Formation of a ligand-binding site for the acetylcholine receptor in vitro. J. Biol. Chem. 271, 25506-25514.
38. Tzartos, S.J. & Changeux, J.-P. (1984) Lipid-dependent recovery of alpha-bungarotoxin and monoclonal antibody binding to the purified alpha-subunit from Torpedo marmorata acetylcholine receptor. Enhancement by noncompetitive channel blockers. J. Biol. Chem. 259, 11512-11519.
39. Kasheverov, I., Utkin, Yu.N., Weise, C., Franke, P., Hucho, F. & Tsetlin, V. (1998) Reverse-phase chromatography isolation and MALDI mass spectrometry of the acetylcholine receptor subinits. Protein Expression Purification 12, 226-232.
40. Wonnacott, S., Harrison, R. & Lunt, G.G. (1980) Interrelationship of carbohydrate and the α-toxin binding site on the acetylcholine receptor from Torpedo marmorata. Life Sci. 27, 1769-1775.
41. Zeghlout, S., Marchot, P., Bougis, P.E. & Ronin, C. (1988) Selective loss of binding sites for the iodinated α-neurotoxin I from Naja mossambica mossambica venom upon enzymatic deglycosylation of Torpedo electric organ membranes. Eur. J. Biochem. 174, 543-550.
42. Gehle, V.M. & Sumikawa, K. (1991) Site-directed mutagenesis of the conserved N-glycosylation site on the nicotinic acetylcholine receptor subunits. Brain Res. Mol. Brain Res. 11, 17-25.
43. Fraenkel, Y., Navon, G., Aronheim, A. & Gershoni, J.M. (1990) Direct measurement of agonist binding to genetically engineered peptides of the acetylcholine receptor by selective T1 NMR relaxation. Biochemistry 29, 2617-2622.
44. Oblas, B., Boyd, N.D. & Singer, R.H. (1983) Analysis of receptor-ligand interactions using nitrocellulose gel transfer: application to Torpedo acetylcholine receptor and α-bungarotoxin. Anal. Biochem. 130, 1-8.
45. Whiting, P., Vincent, A. & Newsom-Davis, J. (1985) Monoclonal antibodies to Torpedo acetylcholine receptor. Characterization of antigenic determinants within the cholinergic binding site. Eur. J. Biochem. 150, 533-539.
46. Whiting, P. (1984) A study of the antigenic determinants on the acetylcholine receptor from Torpedo marmorata and human skeletal muscle using monoclonal antibodies. PhD Thesis, University of London.
47. Fasman, G.D. (1995) The measurement of transmembrane helices by the deconvolution of CD spectra of membrane proteins: a review. Biopolymers (Peptide Sci.) 37, 339-362.
48. Sivaraman, T., Kumar, T.K. & Yu, C. (1996) Destabilization of native tertiary structural interactions is linked to helix-induction by 2,2,2-trifluoroethanol in proteins. Int. J. Biol. Macromol. 19, 235-239.
49. Donelly-Roberts, D.L. & Lentz, T.L. (1993) Sodium dodecyl sulfate-and carbamylcholine-induced changes in circular dichroism spectra of acetylcholine receptor synthetic peptides. Mol. Brain Res. 19, 55-61.
50. Finer-Moore, J. & Stroud, R.M. (1984) Amphiphatic analysis and possible formation of the ion channel in an acetylcholine receptor. Proc. Natl Acad. Sci. USA 81, 155-159.
51. Tsigelny, I., Sugiyama, N., Sine, S.M. & Taylor, P. (1997) A model of the nicotinic receptor extracellular domain based on sequence identity and residue location. Biophys. J. 73, 52-66.
52. Naumann, D., Schultz, C., Goeme-Tschelnokow, U. & Hucho, F. (1993) Secondary structure and temperature behavior of the acetylcholine receptor by Fourier Transform Infrared Spectroscopy. Biochemistry 32, 3162-3168.
53. Wu, C.-S.C., Sun, X.H. & Yang, J.T. (1990) Conformation of acetylcholine receptor in the presence of agonists and antagonists. J. Prot. Chem. 9, 119-126.
54. Baenziger, J.E. & Methot, N. (1995) Fourier transform infrared and hydrogen/deuterium exchange reveal an exchange-resistant core of α-helical peptide hydrogens in the nicotinic acetylcholine receptor. J. Biol. Chem. 270, 29129-29137.
55. Goerne-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, 338-341.
56. Tsetlin, V., Shevalier, A., Alexeev, A., Telyakova, O., Krivoshein, A., Utkin, Yu.N., Vincent, A., Beeson, D. & Methfessel, C. (1997) Purification of the acetylcholine receptor α-subunit domains expressed in E. coli. J. Neurochem. 69, S121.
57. Ptitsyn, O.B. & Uversky, V.N. (1994) The molten globule is a third thermodynamical state of protein molecules. FEBS Lett. 341, 15-18.
58. Chen, G.-Q. & Gouaux (1997) Overexpression of a glutamate receptor (GtuR2) ligand binding domain in Escherichia coli: application of a novel protein folding screen. Proc. Natl Acad. Sci. USA 94, 13431-13436.
59. Barchan, D., Asher, O., Tzartos, S.J., Fuchs, S. & Souroujon, M.C. (1998) Modulation of the anti-acetylcholine receptor response and experimental autoimmune myasthenia gravis by recombinant fragments of the acetylcholine receptor. Eur. J. Immunol. 28, 616-624.
60. Wells, G.B., Anand, R., Wang, F. & Lindstrom, J. (1998) Water-soluble nicotinic acetylcholine receptor formed by α subunit extracellular domains. J. Biol. Chem. 273, 964-973.
61. Kreusch, A., Pfaffinger, P.J., Stevens, C.F. & Choe, S. (1998) Crystal structure of the tetramerization domain of the Shaker potassium channel. Nature 392, 945-948.