Characterizing low affinity epibatidine binding to α4β2 nicotinic acetylcholine receptors with ligand depletion and nonspecific binding

BMC Biophysics

Volumn 4, Issue 1, 2011, Pages

  Person, Alexandra M ^a   Wells, Gregg B ^a,b,c  

^a TEXAS A AND M HEALTH SCIENCE CENTER   (United States)

^b TEXAS A AND M UNIVERSITY SYSTEM   (United States)

^c TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84862193977     PISSN: 20461682     EISSN: None     Source Type: Journal    
DOI: 10.1186/2046-1682-4-19     Document Type: Article

References (61)

1. Johnson ML. The analysis of ligand-binding data with experimental uncertainties in the independent variables. Anal Biochem 1985, 148:471-478. 10.1016/0003-2697(85)90254-4, 4061823.
2. Tellinghuisen J. The least-squares analysis of data from binding and enzyme kinetics studies: weights, bias, and confidence intervals in usual and unusual situations. Methods Enzymol 2009, 467:499-529.
3. Carter CM, Leighton-Davies JR, Charlton SJ. Miniaturized receptor binding assays: complications arising from ligand depletion. J Biomol Screen 2007, 12:255-266. 10.1177/1087057106297788, 17259589.
4. Wells JW, Birdsall NJ, Burgen AS, Hulme EC. Competitive binding studies with multiple sites. Effects arising from depletion of the free radioligand. Biochimica et biophysica acta 1980, 632:464-469. 10.1016/0304-4165(80)90242-1, 7417533.
5. Hulme EC, Birdsall NJM. Strategy and tactics in receptor-binding studies. Receptor-Ligand Interactions: A Practical Approach 1992, 63-176. New York, NY: Oxford University Press, Hulme EC, The Practical Approach Series.
6. Munson PJ, Rodbard D. Ligand: a versatile computerized approach for characterization of ligand-binding systems. Anal Biochem 1980, 107:220-239. 10.1016/0003-2697(80)90515-1, 6254391.
7. Motulsky HJ, Christopoulos A. Fitting models to biological data using linear and nonlinear regression. A practical guide to curve fitting 2004, New York, NY: Oxford University Press.
8. Avlani VA, McLoughlin DJ, Sexton PM, Christopoulos A. The impact of orthosteric radioligand depletion on the quantification of allosteric modulator interactions. J Pharmacol Exp Ther 2008, 325:927-934. 10.1124/jpet.108.136978, 18322151.
9. Wang ZX, Jiang RF. A novel two-site binding equation presented in terms of the total ligand concentration. FEBS Lett 1996, 392:245-249. 10.1016/0014-5793(96)00818-6, 8774854.
10. Gnädisch D, London ED, Terry P, Hill GR, Mukhin AG. High affinity binding of [3H]epibatidine to rat brain membranes. Neuroreport 1999, 10:1631-1636. 10.1097/00001756-199906030-00002, 10501548.
11. Eaton JB, Peng JH, Schroeder KM, George AA, Fryer JD, Krishnan C, Buhlman L, Kuo YP, Steinlein O, Lukas RJ. Characterization of human α4β2-nicotinic acetylcholine receptors stably and heterologously expressed in native nicotinic receptor-null SH-EP1 human epithelial cells. Mol Pharmacol 2003, 64:1283-1294. 10.1124/mol.64.6.1283, 14645658.
12. Shafaee N, Houng M, Truong A, Viseshakul N, Figl A, Sandhu S, Forsayeth JR, Dwoskin LP, Crooks PA, Cohen BN. Pharmacological similarities between native brain and heterologously expressed α4β2 nicotinic receptors. Br J Pharmacol 1999, 128:1291-1299. 10.1038/sj.bjp.0702900, 1571746, 10578144.
13. Houghtling RA, Dávila-García MI, Hurt SD, Kellar KJ. [3H]Epibatidine binding to nicotinic cholinergic receptors in brain. Med Chem Res 1994, 4:538-546.
14. Truong A, Xing X, Forsayeth JR, Dwoskin LP, Crooks PA, Cohen BN. Pharmacological differences between immunoisolated native brain and heterologously expressed rat α4β2 nicotinic receptors. Brain Res Mol Brain Res 2001, 96:68-76.
15. Whiteaker P, Sharples CG, Wonnacott S. Agonist-induced up-regulation of α4β2 nicotinic acetylcholine receptors in M10 cells: pharmacological and spatial definition. Mol Pharmacol 1998, 53:950-962.
16. Jett DA, Beckles RA, Navoa RV, McLemore GL. Increased high-affinity nicotinic receptor-binding in rats exposed to lead during development. Neurotoxicol Teratol 2002, 24:805-811. 10.1016/S0892-0362(02)00314-8, 12460663.
17. Karadsheh MS, Shah MS, Tang X, Macdonald RL, Stitzel JA. Functional characterization of mouse α4β2 nicotinic acetylcholine receptors stably expressed in HEK293T cells. J Neurochem 2004, 91:1138-1150. 10.1111/j.1471-4159.2004.02801.x, 15569257.
18. Person AM, Bills KL, Liu H, Botting SK, Lindstrom J, Wells GB. Extracellular domain nicotinic acetylcholine receptors formed by α4 and β2 subunits. J Biol Chem 2005, 280:39990-40002. 10.1074/jbc.M505087200, 16174636.
19. Swillens S. Interpretation of binding curves obtained with high receptor concentrations: practical aid for computer analysis. Mol Pharmacol 1995, 47:1197-1203.
20. Marks MJ, Meinerz NM, Drago J, Collins AC. Gene targeting demonstrates that α4 nicotinic acetylcholine receptor subunits contribute to expression of diverse [3H]epibatidine binding sites and components of biphasic 86Rb+ efflux with high and low sensitivity to stimulation by acetylcholine. Neuropharmacology 2007, 53:390-405. 10.1016/j.neuropharm.2007.05.021, 2577786, 17631923.
21. Nelson ME, Kuryatov A, Choi CH, Zhou Y, Lindstrom J. Alternate stoichiometries of α4β2 nicotinic acetylcholine receptors. Mol Pharmacol 2003, 63:332-341. 10.1124/mol.63.2.332, 12527804.
22. Marks MJ, Whiteaker P, Calcaterra J, Stitzel JA, Bullock AE, Grady SR, Picciotto MR, Changeux J-P, Collins AC. Two pharmacologically distinct components of nicotinic receptor-mediated rubidium efflux in mouse brain require the β2 subunit. J Pharmacol Exp Ther 1999, 289:1090-1103.
23. Butt CM, Hutton SR, Marks MJ, Collins AC. Bovine serum albumin enhances nicotinic acetylcholine receptor function in mouse thalamic synaptosomes. J Neurochem 2002, 83:48-56. 10.1046/j.1471-4159.2002.01135.x, 12358728.
24. Buisson B, Bertrand D. Chronic exposure to nicotine upregulates the human α4β2 nicotinic acetylcholine receptor function. J Neurosci 2001, 21:1819-1829.
25. Zwart R, Vijverberg HP. Four pharmacologically distinct subtypes of α4β2 nicotinic acetylcholine receptor expressed in Xenopus laevis oocytes. Mol Pharmacol 1998, 54:1124-1131.
26. Sidach SS, Fedorov NB, Lippiello PM, Bencherif M. Development and optimization of a high-throughput electrophysiology assay for neuronal α4β2 nicotinic receptors. J Neurosci Methods 2009, 182:17-24. 10.1016/j.jneumeth.2009.05.014, 19481112.
27. Vallejo YF, Buisson B, Bertrand D, Green WN. Chronic nicotine exposure upregulates nicotinic receptors by a novel mechanism. J Neurosci 2005, 25:5563-5572. 10.1523/JNEUROSCI.5240-04.2005, 2246082, 15944384.
28. Moroni M, Zwart R, Sher E, Cassels BK, Bermudez I. α4β2 nicotinic receptors with high and low acetylcholine sensitivity: pharmacology, stoichiometry, and sensitivity to long-term exposure to nicotine. Mol Pharmacol 2006, 70:755-768. 10.1124/mol.106.023044, 16720757.
29. Briggs CA, Gubbins EJ, Putman CB, Thimmapaya R, Meyer MD, Surowy CS. High- and low-sensitivity subforms of α4β2 and α3β2 nAChRs. Journal of Molecular Neuroscience 2006, 30:11-12. 10.1385/JMN:30:1:11, 17192606.
30. Zhou Y, Nelson ME, Kuryatov A, Choi C, Cooper J, Lindstrom J. Human α4β2 acetylcholine receptors formed from linked subunits. J Neurosci 2003, 23:9004-9015.
31. Covernton PJO, Connolly JG. Multiple components in the agonist concentration-response relationships of neuronal nicotinic acetylcholine receptors. J Neurosci Methods 2000, 96:63-70. 10.1016/S0165-0270(99)00185-5, 10704672.
32. Kuryatov A, Luo J, Cooper J, Lindstrom J. Nicotine acts as a pharmacological chaperone to up-regulate human α4β2 acetylcholine receptors. Mol Pharmacol 2005, 68:1839-1851.
33. Zwart R, Broad LM, Xi Q, Lee M, Moroni M, Bermudez I, Sher E. 5-I A-85380 and TC-2559 differentially activate heterologously expressed α4β2 nicotinic receptors. Eur J Pharmacol 2006, 539:10-17. 10.1016/j.ejphar.2006.03.077, 16674940.
34. Tapia L, Kuryatov A, Lindstrom J. Ca2+ permeability of the (α4)3(β2)2 stoichiometry greatly exceeds that of (α4)2(β2)3 human acetylcholine receptors. Mol Pharmacol 2007, 71:769-776.
35. Anderson DJ, Malysz J, Grønlien JH, El Kouhen R, Håkerud M, Wetterstrand C, Briggs CA, Gopalakrishnan M. Stimulation of dopamine release by nicotinic acetylcholine receptor ligands in rat brain slices correlates with the profile of high, but not low, sensitivity alpha4beta2 subunit combination. Biochem Pharmacol 2009, 78:844-851. 10.1016/j.bcp.2009.06.024, 19555668.
36. Carbone AL, Moroni M, Groot-Kormelink PJ, Bermudez I. Pentameric concatenated (α4)2(β2)3 and (α4)3(β2)2 nicotinic acetylcholine receptors: subunit arrangement determines functional expression. Br J Pharmacol 2009, 156:970-981. 10.1111/j.1476-5381.2008.00104.x, 2697715, 19366353.
37. Exley R, Moroni M, Sasdelli F, Houlihan LM, Lukas RJ, Sher E, Zwart R, Bermudez I. Chaperone protein 14-3-3 and protein kinase A increase the relative abundance of low agonist sensitivity human α4β2 nicotinic acetylcholine receptors in Xenopus oocytes. J Neurochem 2006, 98:876-885. 10.1111/j.1471-4159.2006.03915.x, 16787419.
38. Houlihan LM, Slater Y, Guerra DL, Peng JH, Kuo YP, Lukas RJ, Cassels BK, Bermudez I. Activity of cytisine and its brominated isosteres on recombinant human α7, α4β2 and α4β4 nicotinic acetylcholine receptors. J Neurochem 2001, 78:1029-1043. 10.1046/j.1471-4159.2001.00481.x, 11553677.
39. Khiroug SS, Khiroug L, Yakel JL. Rat nicotinic acetylcholine receptor α2β2 channels: comparison of functional properties with α4β2 channels in Xenopus oocytes. Neuroscience 2004, 124:817-822. 10.1016/j.neuroscience.2004.01.017, 15026122.
40. Gotti C, Moretti M, Meinerz NM, Clementi F, Gaimarri A, Collins AC, Marks MJ. Partial deletion of the nicotinic cholinergic receptor α4 or β2 subunit genes changes the acetylcholine sensitivity of receptor-mediated 86Rb+ efflux in cortex and thalamus and alters relative expression of α4 and β2 subunits. Mol Pharmacol 2008, 73:1796-1807. 10.1124/mol.108.045203, 18337473.
41. Li P, Steinbach JH. The neuronal nicotinic α4β2 receptor has a high maximal probability of being open. Br J Pharmacol 2010, 160:1906-1915. 2958637, 20649589.
42. Houghtling RA, Dávila-García MI, Kellar KJ. Characterization of (±)-[3H]epibatidine binding to nicotinic cholinergic receptors in rat and human brain. Mol Pharmacol 1995, 48:280-287.
43. Marks MJ, Whiteaker P, Collins AC. Deletion of the α7, β2, or β4 nicotinic receptor subunit genes identifies highly expressed subtypes with relatively low affinity for [3H]epibatidine. Mol Pharmacol 2006, 70:947-959. 10.1124/mol.106.025338, 16728647.
44. Srivastava S, Hamouda AK, Pandhare A, Duddempudi PK, Sanghvi M, Cohen JB, Blanton MP. [3H]Epibatidine photolabels non-equivalent amino acids in the agonist binding site of Torpedo and α4β2 nicotinic acetylcholine receptors. J Biol Chem 2009, 284:24939-24947. 10.1074/jbc.M109.019083, 2757197, 19620239.
45. Hulme EC, Trevethick MA. Ligand binding assays at equilibrium: validation and interpretation. Br J Pharmacol 2010, 161:1219-1237. 10.1111/j.1476-5381.2009.00604.x, 3000649, 20132208.
46. Chanvorachote B, Nimmannit U, Muangsiri W, Kirsch L. An evaluation of a fluorometric method for determining binding parameters of drug-carrier complexes using mathematical models based on total drug concentration. J Fluoresc 2009, 19:747-753. 10.1007/s10895-009-0471-1, 19353246.
47. Andujar-Sánchez M, Jara-Perez V, Cobos ES, Cámara-Artigas A. A thermodynamic characterization of the interaction of 8-anilino-1-naphthalenesulfonic acid with native globular proteins: the effect of the ligand dimerization in the analysis of the binding isotherms. J Mol Recognit 2011, 24:548-556. 10.1002/jmr.1065, 20687233.
48. Beyer WH. Standard Mathematical Tables 1976, Cleveland, Ohio: CRC Press.
49. Motulsky HJ, Ransnas LA. Fitting curves to data using nonlinear regression: a practical and nonmathematical review. FASEB J 1987, 1:365-374.
50. Cuatrecasas P, Hollenberg MD. Membrane receptors and hormone action. Adv Protein Chem 1976, 30:251-451.
51. Cheng Y, Prusoff WH. Relationship between the inhibition constant (KI) and the concentration of inhibitor which causes 50 per cent inhibition (I50) of an enzymatic reaction. Biochem Pharm 1973, 22:3099-3108. 10.1016/0006-2952(73)90196-2, 4202581.
52. Xiao Y, Kellar KJ. The comparative pharmacology and up-regulation of rat neuronal nicotinic receptor subtype binding sites stably expressed in transfected mammalian cells. J Pharmacol Exp Ther 2004, 310:98-107. 10.1124/jpet.104.066787, 15016836.
53. Mendel CM, Mendel DB. 'Non-specific' binding. The problem, and a solution. Biochem J 1985, 228:269-272. 1144979, 2988517.
54. Reed RG. Spurious cell surface receptors: inadequate correction for saturable, nonspecific binding mimics receptor binding. Anal Biochem 1990, 185:160-163. 10.1016/0003-2697(90)90273-C, 2160778.
55. McLure JA, Miners JO, Birkett DJ. Nonspecific binding of drugs to human liver microsomes. Br J Clin Pharmacol 2000, 49:453-461. 2014956, 10792203.
56. Burnham KP, Anderson DR. Model selection and multimodel inference: A practical information-theoretic approach 2002, New York: Springer, second.
57. Ludden TM, Beal SL, Sheiner LB. Comparison of the Akaike information criterion, the Schwarz criterion and the F test as guides to model selection. J Pharmacokinet Biopharm 1994, 22:431-445. 10.1007/BF02353864, 7791040.
58. Johnson ML, Frasier SG. Nonlinear least-squares analysis. Methods Enzymol 1985, 117:301-342.
59. Kishi M, Steinbach JH. Role of the agonist binding site in up-regulation of neuronal nicotinic α4β2 receptors. Mol Pharmacol 2006, 70:2037-2044. 10.1124/mol.106.029298, 16966476.
60. Sallette J, Pons S, Devillers-Thiery A, Soudant M, Prado de Carvalho L, Changeux J-P, Corringer P-J. Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 2005, 46:595-607. 10.1016/j.neuron.2005.03.029, 15944128.
61. Gahring LC, Vasquez-Opazo GA, Rogers SW. Choline promotes nicotinic receptor α4 + β2 up-regulation. J Biol Chem 2010, 285:19793-19801. 10.1074/jbc.M110.108803, 2888390, 20392695.