α 4β2Nicotinic Acetylcholine Receptors; relationships between subunit stoichiometry and function at the single channel level

Journal of Biological Chemistry

Volumn 292, Issue 7, 2017, Pages 2729-2740

  Mazzaferro, Simone ^a   Bermudez, Isabel ^d   Sine, Steven M ^a,c   Stephenson, F Anne ^a,b,c  

^a Receptor Biology Laboratory   (United States)

^b Mayo Clinic College of Medicine   (United States)

^c MAYO GRADUATE SCHOOL   (United States)

^d OXFORD BROOKES UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC COMPOUNDS;

ACETYLCHOLINE RECEPTOR; ALLOSTERIC MODULATORS; MACROSCOPIC CURRENTS; MEASUREMENTS OF; NEUROLOGICAL DISORDERS; NICOTINIC ACETYLCHOLINE RECEPTORS; PHARMACOLOGICAL PROPERTIES; SINGLE CHANNELS;

STOICHIOMETRY;

3 [3 (3 PYRIDINYL) 1,2,4 OXADIAZOL 5 YL]BENZONITRILE; BENZONITRILE; NICOTINIC RECEPTOR ALPHA4BETA2; UNCLASSIFIED DRUG; 3-(3-(PYRIDINE-3-YL)-1,2,4-OXADIAZOL-5-YL)BENZONITRILE; NICOTINIC AGENT; NICOTINIC RECEPTOR; OXADIAZOLE DERIVATIVE; PYRIDINE DERIVATIVE;

ANIMAL CELL; ARTICLE; BINDING SITE; CONTROLLED STUDY; DESENSITIZATION; DRUG POTENTIATION; EXPRESSION VECTOR; HISTOGRAM; HUMAN; HUMAN CELL; LIGAND BINDING; MEMBRANE CONDUCTANCE; MEMBRANE POTENTIAL; NONHUMAN; PATCH CLAMP TECHNIQUE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; STOICHIOMETRY; XENOPUS LAEVIS; ANIMAL; CELL LINE; CHEMISTRY; METABOLISM;

ANIMALS; CELL LINE; HUMANS; NICOTINIC AGONISTS; OXADIAZOLES; PATCH-CLAMP TECHNIQUES; PYRIDINES; RECEPTORS, NICOTINIC;

EID: 85013356417     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.764183     Document Type: Article

References (44)

1. Millar, N. S., and Gotti, C. (2009) Diversity of vertebrate nicotinic acetylcholine receptors. Neuropharmacology 56, 237-246
2. Albuquerque, E. X., Pereira, E. F., Alkondon, M., and Rogers, S. W. (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol. Rev. 89, 73-120
3. Marubio, L. M., del Mar Arroyo-Jimenez, M., Cordero-Erausquin, M., Léna, C., Le Novère, N., de Kerchove d'Exaerde, A., Huchet, M., Damaj, M. I., and Changeux, J. P. (1999) Reduced antinociception in mice lacking neuronal nicotinic receptor subunits. Nature 398, 805- 810
4. Picciotto, M. R., Zoli, M., Léna, C., Bessis, A., Lallemand, Y., Le Novère, N., Vincent, P., Pich, E. M., Brûlet, P., and Changeux, J. P. (1995) Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain. Nature 374, 65-67
5. Ross, S. A., Wong, J. Y., Clifford, J. J., Kinsella, A., Massalas, J. S., Horne, M. K., Scheffer, I. E., Kola, I., Waddington, J. L., Berkovic, S. F., and Drago, J. (2000) Phenotypic characterization of an α4 neuronal nicotinic acetylcholine receptor subunit knock-out mouse. J. Neurosci. 20, 6431- 6441
6. Zoli, M., Léna, C., Picciotto, M. R., and Changeux, J. P. (1998) Identification of four classes of brain nicotinic receptors using β2 mutant mice. J. Neurosci. 18, 4461- 4472
7. Zwart, R., and Vijverberg, H. P. (1998) Four pharmacologically distinct subtypes of α4β2 nicotinic acetylcholine receptor expressed in Xenopus laevis oocytes. Mol. Pharmacol. 54, 1124-1131
8. Moroni, M., Zwart, R., Sher, E., Cassels, B. K., and Bermudez, I. (2006) α4β2 nicotinic receptors with high and low acetylcholine sensitivity: pharmacology, stoichiometry, and sensitivity to long-term exposure to nicotine. Mol. Pharmacol. 70, 755-768
9. Nelson, M. E., Kuryatov, A., Choi, C. H., Zhou, Y., and Lindstrom, J. (2003) Alternate stoichiometries of α4β2 nicotinic acetylcholine receptors. Mol. Pharmacol. 63, 332-341
10. Moroni, M., Vijayan, R., Carbone, A., Zwart, R., Biggin, P. C., and Bermudez, I. (2008) Non-agonist-binding subunit interfaces confer distinct functional signatures to the alternate stoichiometries of the α4β2 nicotinic receptor: an α4- α4 interface is required for Zn 2β potentiation. J. Neurosci. 28, 6884- 6894
11. Timmermann, D. B., Sandager-Nielsen, K., Dyhring, T., Smith, M., Jacobsen, A.-M., Nielsen, E. ∅., Grunnet, M., Christensen, J. K., Peters, D., Kohlhaas, K., Olsen, G. M., and Ahring, P. K. (2012) Augmentation of cognitive function by NS9283, a stoichiometry-dependent positive allosteric modulator of β2- and α4-containing nicotinic acetylcholine receptors. Br. J. Pharmacol. 167, 164-182
12. Tapia, L., Kuryatov, A., and Lindstrom, J. (2007) Ca 2β permeability of the ( α4)3(β2)2 stoichiometry greatly exceeds that of ( α4)2 (β2)3 human acetylcholine receptors. Mol. Pharmacol. 71, 769-776
13. Benallegue, N., Mazzaferro, S., Alcaino, C., and Bermudez, I. (2013) The additional ACh binding site at the α4(β)/ α4(β) interface of the ( α4β2)2 α4 nicotinic ACh receptor contributes to desensitization. Br. J. Pharmacol. 170, 304-316
14. Mazzaferro, S., Gasparri, F., New, K., Alcaino, C., Faundez, M., Iturriaga Vasquez, P., Vijayan, R., Biggin, P. C., and Bermudez, I. (2014) Non-equivalent ligand selectivity of agonist sites in ( α4β2)2 β4 nicotinic acetylcholine receptors: a key determinant of agonist efficacy. J. Biol. Chem. 289, 21795-21806
15. Mazzaferro, S., Benallegue, N., Carbone, A., Gasparri, F., Vijayan, R., Biggin, P. C., Moroni, M., and Bermudez, I. (2011) Additional acetylcholine (ACh) binding site at α4/ α4 interface of ( α4β2)2 α4 nicotinic receptor influences agonist sensitivity. J. Biol. Chem. 286, 31043-31054
16. Harpsøe, K., Ahring, P. K., Christensen, J. K., Jensen, M. L., Peters, D., and Balle, T. (2011) Unraveling the high- and low-sensitivity agonist responses of nicotinic acetylcholine receptors. J. Neurosci. 31, 10759-10766
17. Lucero, L. M., Weltzin, M. M., Eaton, J. B., Cooper, J. F., Lindstrom, J. M., Lukas, R. J., and Whiteaker, P. (2016) Differential α4(β)/(β)β2 agonistbinding site contributions to α4β2 nicotinic acetylcholine receptor function within and between isoforms. J. Biol. Chem. 291, 2444-2459
18. Carbone, A.-L., Moroni, M., Groot-Kormelink, P.-J., and Bermudez, I. (2009) Pentameric concatenated ( α4)2 ( α2)3 and ( α4)3 (β2)2 nicotinic acetylcholine receptors: subunit arrangement determines functional expression. Br. J. Pharmacol. 156, 970-981
19. Zwart, R., Carbone, A. L., Moroni, M., Bermudez, I., Mogg, A. J., Folly, E. A., Broad, L. M., Williams, A. C., Zhang, D., Ding, C., Heinz, B. A., and Sher, E. (2008) Sazetidine-A is a potent and selective agonist at native and recombinant α4β2 nicotinic acetylcholine receptors. Mol. Pharmacol. 73, 1838-1843
20. Carignano, C., Barila, E. P., and Spitzmaul, G. (2016) Analysis of neuronal nicotinic acetylcholine receptor α4β2 activation at the single-channel level. Biochim. Biophys. Acta 1858, 1964-1973
21. Chen, Y., Sharples, T. J., Phillips, K. G., Benedetti, G., Broad, L. M., Zwart, R., and Sher, E. (2003) The nicotinic α4β2 receptor selective agonist, TC-2559, increases dopamine neuronal activity in the ventral tegmental area of rat midbrain slices. Neuropharmacology 45, 334-344
22. Ragozzino, D., Fucile, S., Giovannelli, A., Grassi, F., Mileo, A. M., Ballivet, M., Alemà, S., and Eusebi, F. (1997) Functional properties of neuronal nicotinic acetylcholine receptor channels expressed in transfected human cells. Eur. J. Neurosci. 9, 480-488
23. Ibañez-Tallon, I., Miwa, J. M., Wang, H.-L., Adams, N. C., Crabtree, G. W., Sine, S. M., and Heintz, N. (2002) Novel modulation of neuronal nicotinic acetylcholine receptors by association with the endogenous prototoxin lynx1. Neuron. 33, 893-903
24. Hansen, S. B., Wang, H.-L., Taylor, P., and Sine, S. M. (2008) An ion selectivity filter in the extracellular domain of Cys-loop receptors reveals determinants for ion conductance. J. Biol. Chem. 283, 36066-36070
25. Imoto, K., Busch, C., Sakmann, B., Mishina, M., Konno, T., Nakai, J., Bujo, H., Mori, Y., Fukuda, K., and Numa, S. (1988) Rings of negatively charged amino acids determine the acetylcholine receptor channel conductance. Nature 335, 645-648
26. Mukhtasimova, N., Lee, W. Y., Wang, H.-L., and Sine, S. M. (2009) Detection and trapping of intermediate states priming nicotinic receptor channel opening. Nature 459, 451-454
27. Lape, R., Colquhoun, D., and Sivilotti, L. G. (2008) On the nature of partial agonism in the nicotinic receptor superfamily. Nature 454, 722-727
28. Sakmann, B., Patlak, J., and Neher, E. (1980) Single acetylcholine-activated channels show burst-kinetics in presence of desensitizing concentrations of agonist. Nature 286, 71-73
29. Olsen, J. A., Kastrup, J. S., Peters, D., Gajhede, M., Balle, T., and Ahring, P. K. (2013) Two distinct allosteric binding sites at α4β2 nicotinic acetylcholine receptors revealed by NS206 and NS9283 give unique insights to binding activity-associated linkage at Cys-loop receptors. J. Biol. Chem. 288, 35997-36006
30. Unwin, N. (2005) Refined structure of the nicotinic acetylcholine receptor at 4A resolution. J. Mol. Biol. 346, 967-989
31. Morales-Perez, C. L., Noviello, C. M., and Hibbs, R. E. (2016) X-ray structure of the human β4β2 nicotinic receptor. Nature 538, 411-415
32. Jeanclos, E. M., Lin, L., Treuil, M. W., Rao, J., DeCoster, M. A., and Anand, R. (2001) The chaperone protein 14-3-3β interacts with the nicotinic acetylcholine receptor β4 subunit. J. Biol. Chem. 276, 28281-28290
33. Pear, W. S., Nolan, G. P., Scott, M. L., and Baltimore, D. (1993) Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. U.S.A. 90, 8392-8396
34. Sine, S. M. (1993) Molecular dissection of subunit interfaces in the acetylcholine receptor: identification of residues that determine curare selectivity. Proc. Natl. Acad. Sci. U.S.A. 90, 9436-9440
35. Sine, S. M., Quiram, P., Papanikolaou, F., Kreienkamp, H. J., and Taylor, P. (1994) Conserved tyrosines in the β subunit of the nicotinic acetylcholine receptor stabilize quaternary ammonium groups of agonists and curariform antagonists. J. Biol. Chem. 269, 8808- 8816
36. Bouzat, C., Bren, N., and Sine, S. M. (1994) Structural basis of the different gating kinetics of fetal and adult acetylcholine receptors. Neuron. 13, 1395-1402
37. Cooper, S. T., Harkness, P. C., Baker, E. R., and Millar, N. S. (1999) Upregulation of cell-surface β4β2 neuronal nicotinic receptors by lower temperature and expression of chimeric subunits. J. Biol. Chem. 274, 27145-27152
38. Hamill, O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch. 391, 85-100
39. Rayes, D., Spitzmaul, G., Sine, S. M., and Bouzat, C. (2005) Single-channel kinetic analysis of chimeric β7-5HT3A receptors. Mol. Pharmacol. 68, 1475-1483
40. Bouzat, C., Bartos, M., Corradi, J., and Sine, S. M. (2008) The interface between extracellular and transmembrane domains of homomeric Cysloop receptors governs open-channel lifetime and rate of desensitization. J. Neurosci. 28, 7808-7819
41. Sine, S. M., Claudio, T., and Sigworth, F. J. (1990) Activation of Torpedo acetylcholine receptors expressed in mouse fibroblasts. Single channel current kinetics reveal distinct agonist binding affinities. J. Gen. Physiol. 96, 395-437
42. Mukhtasimova, N., daCosta, C. J., and Sine, S. M. (2016) Improved resolution of single channel dwell times reveals mechanisms of binding, priming, and gating in muscle AChR. J. Gen. Physiol. 148, 43-63
43. Colquhoun, D., and Sigworth, F. L. (1983) Fitting and statistical analysis of single-channel records, in Single-Channel Recording (Sakmann, B., and Neher, E., eds) pp. 483-587, Springer US, Boston
44. Sigworth, F. J., and Sine, S. M. (1987) Data transformations for improved display and fitting of single-channel dwell time histograms. Biophys. J. 52, 1047-1054