Tethered agonist analogs as site-specific probes for domains of the human α7 nicotinic acetylcholine receptor that differentially regulate activation and desensitization

Molecular Pharmacology

Volumn 78, Issue 6, 2010, Pages 1012-1025

  Wang, Jingyi ^a   Horenstein, Nicole A ^a   Stokes, Clare ^b   Papke, Roger L ^b  

^a University of Florida ^*  (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; AMMONIA; BUNGAROTOXIN RECEPTOR; CYSTEINE; LIGAND; MUTANT PROTEIN; N(5 CHLORO 2,4 DIMETHOXYPHENYL)N(5 METHYL 3 ISOXAZOLYL 3 ISOXAZOLYL)UREA; PNU 120596; THIOL GROUP; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; COMPETITIVE INHIBITION; CONTROLLED STUDY; FEMALE; HUMAN; LIGAND BINDING; MOLECULAR MODEL; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; FEMALE; HUMANS; ISOXAZOLES; MOLECULAR PROBES; MOLECULAR SEQUENCE DATA; MUTATION; NICOTINIC AGONISTS; OOCYTES; PHENYLUREA COMPOUNDS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, NICOTINIC; XENOPUS LAEVIS;

EID: 78649954378     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.110.066662     Document Type: Article

References (34)

1. Barron SC, McLaughlin JT, See JA, Richards VL, and Rosenberg RL (2009) An allosteric modulator of alpha7 nicotinic receptors, N-(5-chloro-2,4- dimethoxyphenyl)- N′-(5-methyl-3-isoxazolyl)-urea (PNU-120596), causes conformational changes in the extracellular ligand binding domain similar to those caused by acetylcholine. Mol Pharmacol 76:253-263.
2. Bertrand D, Bertrand S, Cassar S, Gubbins E, Li J, and Gopalakrishnan M (2008) Positive allosteric modulation of the alpha7 nicotinic acetylcholine receptor: ligand interactions with distinct binding sites and evidence for a prominent role of the M2-M3 segment. Mol Pharmacol 74:1407-1416.
3. Brejc K, van Dijk WJ, Klaassen RV, Schuurmans M, van Der Oost J, Smit AB, and Sixma TK (2001) Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors. Nature 411:269-276. (Pubitemid 32467026)
4. Celie PH, van Rossum-Fikkert SE, van Dijk WJ, Brejc K, Smit AB, and Sixma TK (2004) Nicotine and carbamylcholine binding to nicotinic acetylcholine receptors as studied in AChBP crystal structures. Neuron 41:907-914.
5. 125I-alpha-bungarotoxin-labeled nicotinic receptors in the interpeduncular nucleus of rats. II. Effects of habenular deafferentation. J Comp Neurol 251:407-413.
6. de Jonge WJ and Ulloa L (2007) The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation. Br J Pharmacol 151:915-929.
7. Gahring LC and Rogers SW (2005) Neuronal nicotinic acetylcholine receptor expression and function on nonneuronal cells. AAPS J 7:E885-E894.
8. Giebelen IA, van Westerloo DJ, LaRosa GJ, de Vos AF, and van der Poll T (2007) Local stimulation of alpha7 cholinergic receptors inhibits LPS-induced TNF-alpha release in the mouse lung. Shock 28:700-703.
9. Gotti C, Moretti M, Gaimarri A, Zanardi A, Clementi F, and Zoli M (2007) Heterogeneity and complexity of native brain nicotinic receptors. Biochem Pharmacol 74:1102-1111.
10. Grønlien JH, Håkerud M, Ween H, Thorin-Hagene K, Briggs CA, Gopalakrishnan M, and Malysz J (2007) Distinct profiles of alpha7 nAChR positive allosteric modulation revealed by structurally diverse chemotypes. Mol Pharmacol 72:715-724.
11. Hansen SB, Sulzenbacher G, Huxford T, Marchot P, Taylor P, and Bourne Y (2005) Structures of Aplysia AChBP complexes with nicotinic agonists and antagonists reveal distinctive binding interfaces and conformations. EMBO J 24:3635-3646.
12. Higgins DG, Thompson JD, and Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 266:383-402.
13. Horenstein NA, Leonik FM, and Papke RL (2008) Multiple pharmacophores for the selective activation of nicotinic alpha7-type acetylcholine receptors. Mol Pharmacol 74:1496-1511.
14. Karlin A and Akabas MH (1998) Substituted-cysteine accessibility method. Methods Enzymol 293:123-145.
15. Li Y, Papke RL, He YJ, Millard WJ, and Meyer EM (1999) Characterization of the neuroprotective and toxic effects of α7 nicotinic receptor activation in PC12 cells. Brain Res 830:218-225.
16. Millar NS and Gotti C (2009) Diversity of vertebrate nicotinic acetylcholine receptors. Neuropharmacology 56:237-246.
17. Miyazawa A, Fujiyoshi Y, and Unwin N (2003) Structure and gating mechanism of the acetylcholine receptor pore. Nature 423:949-955.
18. Papke RL, Kem WR, Soti F, López-Hernández GY, and Horenstein NA (2009) Activation and desensitization of nicotinic alpha7-type acetylcholine receptors by benzylidene anabaseines and nicotine. J Pharmacol Exp Ther 329:791-807.
19. Papke RL, Meyer E, Nutter T, and Uteshev VV (2000) alpha7 receptor-selective agonists and modes of alpha7 receptor activation. Eur J Pharmacol 393:179-195.
20. Papke RL and Porter Papke JK (2002) Comparative pharmacology of rat and human alpha7 nAChR conducted with net charge analysis. Br J Pharmacol 137:49-61.
21. Papke RL, Stokes C, Williams DK, Wang J, and Horenstein NA (2010) Cysteine accessibility analysis of the human alpha7 nicotinic acetylcholine receptor ligand binding domain identifies L119 as a gatekeeper. J Neuropharmacol doi: 10.1016/j.neuropharm.2010.07.014.
22. Pavlov VA, Ochani M, Yang LH, Gallowitsch-Puerta M, Ochani K, Lin X, Levi J, Parrish WR, Rosas-Ballina M, Czura CJ, Larosa GJ, Miller EJ, Tracey KJ, and Al-Abed Y (2007) Selective alpha7-nicotinic acetylcholine receptor agonist GTS-21 improves survival in murine endotoxemia and severe sepsis. Crit Care Med 35:1139-1144.
23. Roberts DD, Lewis SD, Ballou DP, Olson ST, and Shafer JA (1986) Reactivity of small thiolate anions and cysteine-25 in papain toward methyl methanethiosulfonate. Biochemistry 25:5595-5601.
24. Sixma TK and Smit AB (2003) Acetylcholine binding protein (AChBP): a secreted glial protein that provides a high-resolution model for the extracellular domain of pentameric ligand-gated ion channels. Annu Rev Biophys Biomol Struct 21:21.
25. Smit AB, Syed NI, Schaap D, van Minnen J, Klumperman J, Kits KS, Lodder H, van der Schors RC, van Elk R, Sorgedrager B, Brejc K, Sixma TK, and Geraerts WP (2001) A glia-derived acetylcholine-binding protein that modulates synaptic transmission. Nature 411:261-268.
26. Spura A, Russin TS, Freedman ND, Grant M, McLaughlin JT, and Hawrot E (1999) Probing the agonist domain of the nicotinic acetylcholine receptor by cysteine scanning mutagenesis reveals residues in proximity to the alpha-bungarotoxin binding site. Biochemistry 38:4912-4921. (Pubitemid 129514760)
27. Stewart DS, Chiara DC, and Cohen JB (2006) Mapping the structural requirements for nicotinic acetylcholine receptor activation by using tethered alkyltrimethylammonium agonists and antagonists. Biochemistry 45:10641-10653.
28. Sullivan D, Chiara DC, and Cohen JB (2002) Mapping the agonist binding site of the nicotinic acetylcholine receptor by cysteine scanning mutagenesis: antagonist footprint and secondary structure prediction. Mol Pharmacol 61:463-472.
29. Svensson AL and Nordberg A (1999) Beta-estradiol attenuate amyloid beta-peptide toxicity via nicotinic receptors. Neuroreport 10:3485-3489.
30. Unwin N, Miyazawa A, Li J, and Fujiyoshi Y (2002) Activation of the nicotinic acetylcholine receptor involves a switch in conformation of the alpha subunits. J Mol Biol 319:1165-1176.
31. van Maanen MA, Papke RL, Koepke J, Bevaart L, Clark R, Lamppu D, Vervoordeldonk MJ, LaRosa GJ and Tak PP (2009) Therapeutic Effect of Stimulating the Nicotinic Acetylcholine Receptor in the Collagen-Induced Model of Rheumatoid Arthritis: a Role for Ion Channel Activity and Penetration of the Central Nervous System. Thesis, pp 77-97, University of Amsterdam, Amsterdam, Netherlands.
32. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, Al-Abed Y, Czura CJ, and Tracey KJ (2003) Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421:384-388.
33. Young GT, Zwart R, Walker AS, Sher E, and Millar NS (2008) Potentiation of alpha7 nicotinic acetylcholine receptors via an allosteric transmembrane site. Proc Natl Acad Sci USA 105:14686-14691.
34. Young JW, Finlayson K, Spratt C, Marston HM, Crawford N, Kelly JS, and Sharkey J (2004) Nicotine improves sustained attention in mice: evidence for involvement of the alpha7 nicotinic acetylcholine receptor. Neuropsychopharmacology 29:891-900.