Specificity determinants of allosteric modulation in the neuronal nicotinic acetylcholine receptor: A fine line between inhibition and potentiation

Molecular Pharmacology

Volumn 81, Issue 2, 2012, Pages 239-249

  Cesa, Laura C ^a   Higgins, Colin A ^a   Sando, Steven R ^a   Kuo, Dennis W ^a   Levandoski, Mark M ^a  

^a GRINNELL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 ALKYL 2 ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; ACETYLSALICYLIC ACID; BETAINE; BIOLOGICAL MARKER; BRAIN NATRIURETIC PEPTIDE; C REACTIVE PROTEIN; CHOLINE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LIPID; NUCLEOTIDE; PHOSPHATIDYLCHOLINE; PROTEOME; SUGAR; TRANSCRIPTOME; TRIMETHYLAMINE OXIDE; TROPONIN T;

ACCURACY; ACUTE HEART INFARCTION; ANGIOGRAPHY; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; BIOASSAY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CLINICAL EVALUATION; CORONARY ARTERY DISEASE; DIET SUPPLEMENTATION; GENE EXPRESSION; GENOME; HEART FAILURE; HEART STRESS; HUMAN; MASS SPECTROMETRY; METABOLITE; METABOLOMICS; METRIC SYSTEM; MOLECULAR MODEL; MORTALITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIMARY PREVENTION; PRIORITY JOURNAL; PROGNOSIS; PROTEIN ANALYSIS; RISK ASSESSMENT; RISK FACTOR; SCREENING; SENSITIVITY AND SPECIFICITY; VASCULAR DISEASE;

ALLOSTERIC REGULATION; ALLOSTERIC SITE; ANIMALS; ANTHELMINTICS; DRUG DESIGN; MORANTEL; MUTATION; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; PROTEIN SUBUNITS; PYRANTEL; RATS; RECEPTORS, NICOTINIC;

EID: 84856076106     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.111.076059     Document Type: Article

References (45)

1. Albuquerque EX, Pereira EF, Alkondon M, and Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89:73-120.
2. Arias HR (2000) Localization of agonist and competitive antagonist binding sites on nicotinic acetylcholine receptors. Neurochem Int 36:595-645.
3. Arias HR, Bhumireddy P, and Bouzat C (2006) Molecular mechanisms and binding site locations for noncompetitive antagonists of nicotinic acetylcholine receptors. Int J Biochem Cell Biol 38:1254-1276.
4. Bartos M, Rayes D, and Bouzat C (2006) Molecular determinants of pyrantel selectivity in nicotinic receptors. Mol Pharmacol 70:1307-1318. (Pubitemid 44435983)
5. Bartos M, Price KL, Lummis SC, and Bouzat C (2009) Glutamine 57 at the complementary binding-site face is a key determinant of morantel selectivity for α7 nicotinic receptors. J Biol Chem 284:21478-21487.
6. Bertrand D and Gopalakrishnan M (2007) Allosteric modulation of nicotinic acetylcholine receptors. Biochem Pharmacol 74:1155-1163. (Pubitemid 47417931)
7. Birks J (2006) Cholinesterase inhibitors for Alzheimer's disease. Cochrane Database Syst Rev (1):CD005593.
8. Boulter J, Connolly J, Deneris E, Goldman D, Heinemann S, and Patrick J (1987) Functional expression of two neuronal nicotinic acetylcholine receptors from cDNA clones identifies a gene family. Proc Natl Acad Sci USA 84:7763-7767.
9. 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 ligandbinding domain of nicotinic receptors. Nature 411:269-276. (Pubitemid 32467026)
10. Broad LM, Zwart R, Pearson KH, Lee M, Wallace L, McPhie GI, Emkey R, Hollinshead SP, Dell CP, Baker SR, et al. (2006) Identification and pharmacological profile of a new class of selective nicotinic acetylcholine receptor potentiators. J Pharmacol Exp Ther 318:1108-1117. (Pubitemid 44268317)
11. Buisson B and Bertrand D (1998) Open-channel blockers at the human α4β2 neuronal nicotinic acetylcholine receptor. Mol Pharmacol 53:555-563. (Pubitemid 28162880)
12. Cohen BN, Figl A, Quick MW, Labarca C, Davidson N, and Lester HA (1995) Regions of β2 and β4 responsible for differences between the steady state dose-response relationships of the α3β2 and α3β4 neuronal nicotinic receptors. J Gen Physiol 105:745-764.
13. Collins T and Millar NS (2010) Nicotinic acetylcholine receptor transmembrane mutations convert ivermectin from a positive to a negative allosteric modulator. Mol Pharmacol 78:198-204.
14. Colquhoun D (1998) Binding, gating, affinity and efficacy: the interpretation of structure-activity relationships for agonists and of the effects of mutating receptors. Br J Pharmacol 125:924-947.
15. Corringer PJ, Baaden M, Bocquet N, Delarue M, Dufresne V, Nury H, Prevost M, and Van Renterghem C (2010) Atomic structure and dynamics of pentameric ligand-gated ion channels: new insight from bacterial homologues. J Physiol 588: 565-572.
16. Dani JA and Bertrand D (2007) Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu Rev Pharmacol Toxicol 47:699-729.
17. Gonzales D, Rennard SI, Nides M, Oncken C, Azoulay S, Billing CB, Watsky EJ, Gong J, Williams KE, Reeves KR, et al. (2006) Varenicline, an alpha4beta2 nicotinic acetylcholine receptor partial agonist, vs sustained-release bupropion and placebo for smoking cessation: a randomized controlled trial. JAMA 296: 47-55.
18. Gotti C, Clementi F, Fornari A, Gaimarri A, Guiducci S, Manfredi I, Moretti M, Pedrazzi P, Pucci L, and Zoli M (2009) Structural and functional diversity of native brain neuronal nicotinic receptors. Biochem Pharmacol 78:703-711.
19. Hanson SM, Morlock EV, Satyshur KA, and Czajkowski C (2008) Structural requirements for eszopiclone and zolpidem binding to the γ-aminobutyric acid type-A (GABAA) receptor are different. J Med Chem 51:7243-7252.
20. Harpsøe K, Ahring PK, Christensen JK, Jensen ML, Peters D, and Balle T (2011) Unraveling the high- and low-sensitivity agonist responses of nicotinic acetylcholine receptors. J Neurosci 31:10759-10766.
21. Henderson BJ, Pavlovicz RE, Allen JD, González-Cestari TF, Orac CM, Bonnell AB, Zhu MX, Boyd RT, Li C, Bergmeier SC, et al. (2010) Negative allosteric modulators that target human α4β2 neuronal nicotinic receptors. J Pharmacol Exp Ther 334:761-774.
22. Hsiao B, Mihalak KB, Repicky SE, Everhart D, Mederos AH, Malhotra A, and Luetje CW (2006) Determinants of zinc potentiation on the α4 subunit of neuronal nicotinic receptors. Mol Pharmacol 69:27-36. (Pubitemid 43048890)
23. Hsiao B, Mihalak KB, Magleby KL, and Luetje CW (2008) Zinc potentiates neuronal nicotinic receptors by increasing burst duration. J Neurophysiol 99:999-1007. (Pubitemid 351253252)
24. Hurst RS, Hajós M, Raggenbass M, Wall TM, Higdon NR, Lawson JA, Rutherford- Root KL, Berkenpas MB, Hoffmann WE, Piotrowski DW, et al. (2005) A novel allosteric modulator of the α7 neuronal nicotinic acetylcholine receptor: in vitro and in vivo characterization. J Neurosci 25:4396-4405. (Pubitemid 40628784)
25. Jensen AA, Frølund B, Liljefors T, and Krogsgaard-Larsen P (2005) Neuronal nicotinic acetylcholine receptors: structural revelations, target identifications, and therapeutic inspirations. J Med Chem 48:4705-4745. (Pubitemid 41038456)
26. Karlin A and Akabas MH (1998) Substituted-cysteine accessibility method. Methods Enzymol 293:123-145. (Pubitemid 29342485)
27. Krause RM, Buisson B, Bertrand S, Corringer PJ, Galzi JL, Changeux JP, and Bertrand D (1998) Ivermectin: a positive allosteric effector of the α7 neuronal nicotinic acetylcholine receptor. Mol Pharmacol 53:283-294. (Pubitemid 28099739)
28. Kucken AM, Wagner DA, Ward PR, Teissére JA, Boileau AJ, and Czajkowski C (2000) Identification of benzodiazepine binding site residues in the γ2 subunit of the γ-aminobutyric acid A receptor. Mol Pharmacol 57:932-939. (Pubitemid 30253376)
29. Maelicke A and Albuquerque EX (2000) Allosteric modulation of nicotinic acetylcholine receptors as a treatment strategy for Alzheimer's disease. Eur J Pharmacol 393:165-170. (Pubitemid 30193413)
30. 2α4 nicotinic receptor influences agonist sensitivity. J Biol Chem 286:31043-31054.
31. Miller PS and Smart TG (2010) Binding, activation and modulation of Cys-loop receptors. Trends Pharmacol Sci 31:161-174.
32. 2+ potentiation. J Neurosci 28:6884-6894.
33. Mukhtasimova N and Sine SM (2007) An intersubunit trigger of channel gating in the muscle nicotinic receptor. J Neurosci 27:4110-4119. (Pubitemid 46597150)
34. Nirthanan S, Garcia G 3rd, Chiara DC, Husain SS, and Cohen JB (2008) Identifi- cation of binding sites in the nicotinic acetylcholine receptor for TDBzl-etomidate, a photoreactive positive allosteric effector. J Biol Chem 283:22051-22062.
35. Rang HP (1981) Drugs and ionic channels: mechanism and implications. Postgrad Med J 57:89-97.
36. Rayes D, De Rosa MJ, Sine SM, and Bouzat C (2009) Number and locations of agonist binding sites required to activate homomeric Cys-loop receptors. J Neurosci 29:6022-6032.
37. Rucktooa P, Smit AB, and Sixma TK (2009) Insight in nAChR subtype selectivity from AChBP crystal structures. Biochem Pharmacol 78:777-787.
38. Sallette J, Bohler S, Benoit P, Soudant M, Pons S, Le Novère N, Changeux JP, and Corringer PJ (2004) An extracellular protein microdomain controls up-regulation of neuronal nicotinic acetylcholine receptors by nicotine. J Biol Chem 279:18767-18775. (Pubitemid 38623302)
39. Schrattenholz A, Pereira EF, Roth U, Weber KH, Albuquerque EX, and Maelicke A (1996) Agonist responses of neuronal nicotinic acetylcholine receptors are potentiated by a novel class of allosterically acting ligands. Mol Pharmacol 49:1-6. (Pubitemid 26036779)
40. Seo S, Henry JT, Lewis AH, Wang N, and Levandoski MM (2009) The positive allosteric modulator morantel binds at noncanonical subunit interfaces of neuronal nicotinic acetylcholine receptors. J Neurosci 29:8734-8742.
41. Sine SM and Engel AG (2006) Recent advances in Cys-loop receptor structure and function. Nature 440:448-455.
42. Teissére JA and Czajkowski C (2001) A β-strand in the γ2 subunit lines the benzodiazepine binding site of the GABAA receptor: structural rearrangements detected during channel gating. J Neurosci 21:4977-4986. (Pubitemid 32622923)
43. Wu TY, Smith CM, Sine SM, and Levandoski MM (2008) Morantel allosterically enhances channel gating of neuronal nicotinic acetylcholine α3β2 receptors. Mol Pharmacol 74:466-475.
44. Young GT, Broad LM, Zwart R, Astles PC, Bodkin M, Sher E, and Millar NS (2007) Species selectivity of a nicotinic acetylcholine receptor agonist is conferred by two adjacent extracellular β4 amino acids that are implicated in the coupling of binding to channel gating. Mol Pharmacol 71:389-397. (Pubitemid 46147905)
45. Zwart R and Vijverberg HP (1998) Four pharmacologically distinct subtypes of α4β2 nicotinic acetylcholine receptor expressed in Xenopus laevis oocytes. Mol Pharmacol 54:1124-1131. (Pubitemid 29002058)