Nicotine-induced upregulation of native neuronal nicotinic receptors is caused by multiple mechanisms

Journal of Neuroscience

Volumn 32, Issue 6, 2012, Pages 2227-2238

  Govind, Anitha P ^a   Walsh, Heather ^a   Green, William N ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA4BETA2; PROTEASOME; PROTEASOME INHIBITOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BIOTINYLATION; BRAIN CELL; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FEMALE; IMMUNOCYTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR UPREGULATION;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; FEMALE; HEK293 CELLS; HUMANS; MALE; NICOTINE; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RECEPTORS, NICOTINIC; UP-REGULATION;

EID: 84856978299     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5438-11.2012     Document Type: Article

References (60)

1. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89:73-120.
2. Alexander JK, Govind AP, Drisdel RC, Blanton MP, Vallejo Y, Lam TT, Green WN (2010) Palmitoylation of nicotinic acetylcholine receptors. J Mol Neurosci 40:12-20.
3. Barrantes FJ (2010) Cholesterol effects on nicotinic acetylcholine receptor: cellular aspects. Subcell Biochem 51:467-487.
4. Benwell ME, Balfour DJ, Anderson JM (1988) Evidence that tobacco smoking increases the density of (-)-[3H]nicotine binding sites in human brain. J Neurochem 50:1243-1247.
5. Bermudez I, Moroni M (2006) Phosphorylation and function of alpha4beta2 receptor. J Mol Neurosci 30:97-98.
6. Breese CR, Marks MJ, Logel J, Adams CE, Sullivan B, Collins AC, Leonard S (1997) Effect of smoking history on [3H]nicotine binding in human postmortem brain. J Pharmacol Exp Ther 282:7-13.
7. Buisson B, Bertrand D (2001) Chronic exposure to nicotine upregulates the human α4β2 nicotinic acetylcholine receptor function. J Neurosci 21:1819-1829.
8. Christianson JC, GreenWN (2004) Regulation of nicotinic receptor expression by the ubiquitin-proteasome system. EMBO J 23:4156-4165.
9. Clarke PB, Schwartz RD, Paul SM, Pert CB, Pert A (1985) Nicotinic binding in rat brain: autoradiographic comparison of [3H]acetylcholine, [3H]nicotine, and [125I]-β-bungarotoxin. J Neurosci 5:1307-1315.
10. Collins AC, Romm E, Wehner JM (1990) Dissociation of the apparent relationship between nicotine tolerance and up-regulation of nicotinic receptors. Brain Res Bull 25:373-379.
11. Collins AC, Luo Y, Selvaag S, Marks MJ (1994) Sensitivity to nicotine and brain nicotinic receptors are altered by chronic nicotine and mecamylamine infusion. J Pharmacol Exp Ther 271:125-133.
12. Conroy WG, Berg DK (1998) Nicotinic receptor subtypes in the developing chick brain: appearance of a species containing the alpha4, beta2, and alpha5 gene products. Mol Pharmacol 53:392-401.
13. Cui C, Booker TK, Allen RS, Grady SR, Whiteaker P, Marks MJ, Salminen O, Tritto T, Butt CM, Allen WR, Stitzel JA, McIntosh JM, Boulter J, Collins AC, Heinemann SF (2003) The β3 nicotinic receptor subunit: a component of α-conotoxin MII-binding nicotinic acetylcholine receptors that modulate dopamine release and related behaviors. J Neurosci 23:11045-11053.
14. Darsow T, Booker TK, Piña-Crespo JC, Heinemann SF (2005) Exocytic trafficking is required for nicotine-induced up-regulation of alpha 4 beta 2 nicotinic acetylcholine receptors. J Biol Chem 280:18311-18320.
15. De Biasi M, Dani JA (2011) Reward, addiction, withdrawal to nicotine. Annu Rev Neurosci 34:105-130.
16. Drisdel RC, Green WN (2000) Neuronal alpha-bungarotoxin receptors are α7 subunit homomers. J Neurosci 20:133-139.
17. Drisdel RC, Manzana E, GreenWN (2004) The role of palmitoylation in functional expression of nicotinic α7 receptors. J Neurosci 24:10502-10510.
18. Fenster CP, Whitworth TL, Sheffield EB, Quick MW, Lester RA (1999) Upregulation of surface α4β2 nicotinic receptors is initiated by receptor desensitization after chronic exposure to nicotine. J Neurosci 19:4804-4814.
19. Ficklin MB, Zhao S, Feng G (2005) Ubiquilin-1 regulates nicotine-induced up-regulation of neuronal nicotinic acetylcholine receptors. J Biol Chem 280:34088-34095.
20. Fong TM, McNamee MG (1986) Correlation between acetylcholine receptor function and structural properties of membranes. Biochemistry 25:830-840.
21. Gotti C, Moretti M, Clementi F, Riganti L, McIntosh JM, Collins AC, Marks MJ, Whiteaker P (2005) Expression of nigrostriatal alpha 6-containing nicotinic acetylcholine receptors is selectively reduced, but not eliminated, by beta 3 subunit gene deletion. Mol Pharmacol 67:2007-2015.
22. Govind AP, Vezina P, Green WN (2009) Nicotine-induced upregulation of nicotinic receptors: underlying mechanisms and relevance to nicotine addiction. Biochem Pharmacol 78:756-765.
23. Grailhe R, de Carvalho LP, Paas Y, Le Poupon C, Soudant M, Bregestovski P, Changeux JP, Corringer PJ (2004) Distinct subcellular targeting of fluorescent nicotinic alpha 3 beta 4 and serotoninergic 5-HT3A receptors in hippocampal neurons. Eur J Neurosci 19:855-862.
24. Green WN, Claudio T (1993) Acetylcholine receptor assembly: subunit folding and oligomerization occur sequentially. Cell 74:57-69.
25. Härfstrand A, Adem A, Fuxe K, Agnati L, Andersson K, Nordberg A (1988) Distribution of nicotinic cholinergic receptors in the rat tel-and diencephalon: a quantitative receptor autoradiographical study using [3H]-acetylcholine, [alpha-125I]bungarotoxin and [3H]nicotine. Acta Physiol Scand 132:1-14.
26. Harkness PC, Millar NS (2002) Changes in conformation and subcellular distribution ofα4β2 nicotinic acetylcholine receptors revealed by chronic nicotine treatment and expression of subunit chimeras. J Neurosci 22:10172-10181.
27. Hsu YN, Amin J, Weiss DS, Wecker L (1996) Sustained nicotine exposure differentially affects alpha 3 beta 2 and alpha 4 beta 2 neuronal nicotinic receptors expressed in Xenopus oocytes. J Neurochem 66:667-675.
28. Hulihan-Giblin BA, Lumpkin MD, Kellar KJ (1990) Effects of chronic administration of nicotine on prolactin release in the rat: inactivation of prolactin response by repeated injections of nicotine. J Pharmacol Exp Ther 252:21-25.
29. Jeanclos EM, Lin L, Treuil MW, Rao J, DeCoster MA, Anand R (2001) The chaperone protein 14-3-3eta interacts with the nicotinic acetylcholine receptor alpha 4 subunit. Evidence for a dynamic role in subunit stabilization. J Biol Chem 276:28281-28290.
30. Karlin A, Akabas MH (1995) Towards a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron 15:1231-1244.
31. Klink R, de Kerchove d'Exaerde A, Zoli M, Changeux JP (2001) Molecular and physiological diversity of nicotinic acetylcholine receptors in the midbrain dopaminergic nuclei. J Neurosci 21:1452-1463.
32. Marks MJ, Burch JB, Collins AC (1983) Effects of chronic nicotine infusion on tolerance development and nicotinic receptors. J Pharmacol Exp Ther 226:817-825.
33. Marks MJ, Stitzel JA, Collins AC (1985) Time course study of the effects of chronic nicotine infusion on drug response and brain receptors. J Pharmacol Exp Ther 235:619-628.
34. Marks MJ, McClure-Begley TD, Whiteaker P, Salminen O, Brown RW, Cooper J, Collins AC, Lindstrom JM (2011) Increased nicotinic acetylcholine receptor protein underlies chronic nicotine-induced up-regulation of nicotinic agonist binding sites in mouse brain. J Pharmacol Exp Ther 337:187-200.
35. McGehee DS, Role LW (1995) Physiological diversity of nicotinic acetylcholine receptors expressed by vertebrate neurons. Annu Rev Physiol 57:521-546.
36. Merlie JP, Lindstrom J (1983) Assembly in vivo of mouse muscle acetylcholine receptor: identification of an alpha subunit species that may be an assembly intermediate. Cell 34:747-757.
37. Moroni M, Zwart R, Sher E, Cassels BK, Bermudez I (2006) alpha4beta2 nicotinic receptors with high and low acetylcholine sensitivity: pharmacology, stoichiometry, and sensitivity to long-term exposure to nicotine. Mol Pharmacol 70:755-768.
38. Nashmi R, Dickinson ME, McKinney S, Jareb M, Labarca C, Fraser SE, Lester HA (2003) Assembly of α4β2 nicotinic acetylcholine receptors assessed with functional fluorescently labeled subunits: effects of localization, trafficking, and nicotine-induced upregulation in clonal mammalian cells and in cultured midbrain neurons. J Neurosci 23:11554-11567.
39. Nelson ME, Kuryatov A, Choi CH, Zhou Y, Lindstrom J (2003) Alternate stoichiometries of alpha4beta2 nicotinic acetylcholine receptors. Mol Pharmacol 63:332-341.
40. Parker SL, Fu Y, McAllen K, Luo J, McIntosh JM, Lindstrom JM, Sharp BM (2004) Up-regulation of brain nicotinic acetylcholine receptors in the rat during long-term self-administration of nicotine: disproportionate increase of the alpha6 subunit. Mol Pharmacol 65:611-622.
41. Pauly JR, Stitzel JA, Marks MJ, CollinsAC (1989) An autoradiographic analysis of cholinergic receptors in mouse brain. Brain Res Bull 22:453-459.
42. Peng X, Gerzanich V, Anand R, Whiting PJ, Lindstrom J (1994) Nicotineinduced increase in neuronal nicotinic receptors results from a decrease in the rate of receptor turnover. Mol Pharmacol 46:523-530.
43. Perry DC, Dávila-García MI, Stockmeier CA, Kellar KJ (1999) Increased nicotinic receptors in brains from smokers: membrane binding and autoradiography studies. J Pharmacol Exp Ther 289:1545-1552.
44. Rezvani K, Teng Y, Shim D, De Biasi M (2007) Nicotine regulates multiple synaptic proteins by inhibiting proteasomal activity. J Neurosci 27:10508-10519.
45. Rezvani K, Teng Y, Pan Y, Dani JA, Lindstrom J, García Gras EA, McIntosh JM, De BiasiM (2009) UBXD4, a UBX-containing protein, regulates the cell surface number and stability ofβ3-containing nicotinic acetylcholine receptors. J Neurosci 29:6883-6896.
46. Rogers SW, Gregori NZ, Carlson N, Gahring LC, NobleM (2001) Neuronal nicotinic acetylcholine receptor expression by O2A/oligodendrocyte progenitor cells. Glia 33:306-313.
47. Sallette J, Pons S, Devillers-Thiery A, Soudant M, Prado de Carvalho L, Changeux JP, Corringer PJ (2005) Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 46:595-607.
48. Salminen O, Drapeau JA, McIntosh JM, Collins AC, Marks MJ, Grady SR (2007) Pharmacology of alpha-conotoxin MII-sensitive subtypes of nicotinic acetylcholine receptors isolated by breeding of null mutant mice. Mol Pharmacol 71:1563-1571.
49. Sargent PB (1993) The diversity of neuronal nicotinic acetylcholine receptors. Annu Rev Neurosci 16:403-443.
50. Schwartz RD, Kellar KJ (1983) Nicotinic cholinergic receptor binding sites in the brain: regulation in vivo. Science 220:214-216.
51. Sheffield EB, Quick MW, Lester RA (2000) Nicotinic acetylcholine receptor subunitmRNAexpression and channel function in medial habenula neurons. Neuropharmacology 39:2591-2603.
52. Tumkosit P, Kuryatov A, Luo J, Lindstrom J (2006) Beta3 subunits promote expression and nicotine-induced up-regulation of human nicotinic alpha6* nicotinic acetylcholine receptors expressed in transfected cell lines. Mol Pharmacol 70:1358-1368.
53. Turner JR, Castellano LM, Blendy JA (2011) Parallel anxiolytic-like effects and upregulation of neuronal nicotinic acetylcholine receptors following chronic nicotine and varenicline. Nicotine Tob Res 13:41-46.
54. Vallejo YF, Buisson B, Bertrand D, Green WN (2005) Chronic nicotine exposure upregulates nicotinic receptors by a novel mechanism. J Neurosci 25:5563-5572.
55. Vezina P, McGehee DS, Green WN (2007) Exposure to nicotine and sensitization of nicotine-induced behaviors. Prog Neuropsychopharmacol Biol Psychiatry 31:1625-1638.
56. Walsh H, Govind AP, Mastro R, Hoda JC, Bertrand D, Vallejo Y, Green WN (2008) Up-regulation of nicotinic receptors by nicotine varies with receptor subtype. J Biol Chem 283:6022-6032.
57. Wang F, Nelson ME, Kuryatov A, Olale F, Cooper J, Keyser K, Lindstrom J (1998) Chronic nicotine treatment up-regulates human alpha3 beta2 but not alpha3 beta4 acetylcholine receptors stably transfected in human embryonic kidney cells. J Biol Chem 273:28721-28732.
58. Wecker L, Pollock VV, Pacheco MA, Pastoor T (2010) Nicotine-induced up regulation of alpha4beta2 neuronal nicotinic receptors is mediated by the protein kinase C-dependent phosphorylation of alpha4 subunits. Neuroscience 171:12-22.
59. Whiting PJ, Lindstrom JM (1988) Characterization of bovine and human neuronal nicotinic acetylcholine receptors using monoclonal antibodies. J Neurosci 8:3395-3404.
60. Xu W, Orr-Urtreger A, Nigro F, Gelber S, Sutcliffe CB, Armstrong D, Patrick JW, Role LW, Beaudet AL, De Biasi M (1999) Multiorgan autonomic dysfunction in mice lacking the α2 and the α4 subunits of neuronal nicotinic acetylcholine receptors. J Neurosci 19:9298-9305.