Pharmacological chaperoning of nicotinic acetylcholine receptors reduces the endoplasmic reticulum stress response

Molecular Pharmacology

Volumn 81, Issue 6, 2012, Pages 759-769

  Srinivasan, Rahul ^a   Richards, Christopher I ^a   Xiao, Cheng ^a   Rhee, Doreen ^a   Pantoja, Rigo ^a   Dougherty, Dennis A ^b   Miwa, Julie M ^a   Lester, Henry A ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; CHAPERONE; CYTISINE; DIHYDRO BETA ERYTHROIDINE; ENHANCED GREEN FLUORESCENT PROTEIN; INITIATION FACTOR 2ALPHA; NICOTINE; NICOTINIC RECEPTOR ALPHA4BETA2;

ANIMAL CELL; ARTICLE; BRAIN CELL; CELL MANIPULATION; CELL MEMBRANE; CELL NUCLEUS; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE PREDISPOSITION; ENDOPLASMIC RETICULUM STRESS; MOUSE; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; RECEPTOR UPREGULATION; SMOKING; STOICHIOMETRY; TRANS GOLGI NETWORK; UNFOLDED PROTEIN RESPONSE;

ACTIVATING TRANSCRIPTION FACTOR 6; ANIMALS; CELL LINE; CELL NUCLEUS; ENDOPLASMIC RETICULUM; EUKARYOTIC INITIATION FACTOR-2; FLUORESCENCE RESONANCE ENERGY TRANSFER; GOLGI APPARATUS; MICE; MOLECULAR CHAPERONES; NICOTINE; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN TRANSPORT; RECEPTORS, NICOTINIC; SPECTROMETRY, FLUORESCENCE; UNFOLDED PROTEIN RESPONSE;

EID: 84861420190     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.112.077792     Document Type: Article

References (61)

1. Ahmadi FA, Grammatopoulos TN, Poczobutt AM, Jones SM, Snell LD, Das M, and Zawada WM (2008) Dopamine selectively sensitizes dopaminergic neurons to rotenone-induced apoptosis. Neurochem Res 33:886-901.
2. Azam L, Winzer-Serhan UH, Chen Y, and Leslie FM (2002) Expression of neuronal nicotinic acetylcholine receptor subunit mRNAs within midbrain dopamine neurons. J Comp Neurol 444:260-274. (Pubitemid 34117090)
3. Bommiasamy H, Back SH, Fagone P, Lee K, Meshinchi S, Vink E, Sriburi R, Frank M, Jackowski S, Kaufman RJ, et al. (2009) ATF6α induces XBP1-independent expansion of the endoplasmic reticulum. J Cell Sci 122:1626-1636.
4. Buisson B and Bertrand D (2001) Chronic exposure to nicotine upregulates the human α4β2 nicotinic acetylcholine receptor function. J Neurosci 21:1819-1829. (Pubitemid 32221365)
5. Buisson B and Bertrand D (2002) Nicotine addiction: the possible role of functional upregulation. Trends Pharmacol Sci 23:130-136. (Pubitemid 34185414)
6. Champtiaux N, Gotti C, Cordero-Erausquin M, David DJ, Przybylski C, Léna C, Clementi F, Moretti M, Rossi FM, Le Novère N, et al. (2003) Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knockout mice. J Neurosci 23:7820-7829. (Pubitemid 37055453)
7. Commons KG (2008) α4 containing nicotinic receptors are positioned to mediate postsynaptic effects on 5-HT neurons in the rat dorsal raphe nucleus. Neuroscience 153:851-859.
8. Corringer PJ, Sallette J, and Changeux JP (2006) Nicotine enhances intracellular nicotinic receptor maturation: a novel mechanism of neural plasticity? J Physiol Paris 99:162-171.
9. DuRose JB, Scheuner D, Kaufman RJ, Rothblum LI, and Niwa M (2009) Phosphorylation of eukaryotic translation initiation factor 2α coordinates rRNA transcription and translation inhibition during endoplasmic reticulum stress. Mol Cell Biol 29:4295-4307.
10. Egawa N, Yamamoto K, Inoue H, Hikawa R, Nishi K, Mori K, and Takahashi R (2011) The endoplasmic reticulum stress sensor, ATF6α, protects against neurotoxin-induced dopaminergic neuronal death. J Biol Chem 286:7947-7957.
11. Fonck C, Nashmi R, Salas R, Zhou C, Huang Q, De Biasi M, Lester RA, and Lester HA (2009) Demonstration of functional α4-containing nicotinic receptors in the medial habenula. Neuropharmacology 56:247-253.
12. Galehdar Z, Swan P, Fuerth B, Callaghan SM, Park DS, and Cregan SP (2010) Neuronal apoptosis induced by endoplasmic reticulum stress is regulated by ATF4-CHOP-mediated induction of the Bcl-2 homology 3-only member PUMA. J Neurosci 30:16938-16948.
13. Goldstein EN, Owen CR, White BC, and Rafols JA (1999) Ultrastructural localization of phosphorylated eIF2α [eIF2α(P)] in rat dorsal hippocampus during reperfusion. Acta Neuropathol 98:493-505. (Pubitemid 29476169)
14. Gopalakrishnan M, Molinari EJ, and Sullivan JP (1997) Regulation of human α4β2 neuronal nicotinic acetylcholine receptors by cholinergic channel ligands and second messenger pathways. Mol Pharmacol 52:524-534. (Pubitemid 27412979)
15. 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. (Pubitemid 47432651)
16. Harding HP, Novoa I, Zhang Y, Zeng H, Wek R, Schapira M, and Ron D (2000) Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099-1108.
17. Hernán MA, Takkouche B, Caamaño-Isorna F, and Gestal-Otero JJ (2002) A meta-analysis of coffee drinking, cigarette smoking, and the risk of Parkinson's disease. Ann Neurol 52:276-284. (Pubitemid 35001493)
18. Hetz C and Glimcher LH (2009) Fine-tuning of the unfolded protein response: assembling the IRE1α interactome. Mol Cell 35:551-561.
19. Hill JA Jr, Zoli M, Bourgeois JP, and Changeux JP (1993) Immunocytochemical localization of a neuronal nicotinic receptor: the β2-subunit. J Neurosci 13:1551-1568. (Pubitemid 23095398)
20. Holtz WA and O'Malley KL (2003) Parkinsonian mimetics induce aspects of unfolded protein response in death of dopaminergic neurons. J Biol Chem 278:19367-19377. (Pubitemid 36799332)
21. Hoozemans JJ, van Haastert ES, Eikelenboom P, de Vos RA, Rozemuller JM, and Scheper W (2007) Activation of the unfolded protein response in Parkinson's disease. Biochem Biophys Res Commun 354:707-711. (Pubitemid 46186242)
22. Kabbani N, Woll MP, Levenson R, Lindstrom JM, and Changeux JP (2007) Intracellular complexes of the β2 subunit of the nicotinic acetylcholine receptor in brain identified by proteomics. Proc Natl Acad Sci USA 104:20570-20575.
23. Kim R, Emi M, Tanabe K, and Murakami S (2006) Role of the unfolded protein response in cell death. Apoptosis 11:5-13. (Pubitemid 43151639)
24. Kishi M and Steinbach JH (2006) Role of the agonist binding site in up-regulation of neuronal nicotinic α4β2 receptors. Mol Pharmacol 70:2037-2044. (Pubitemid 44771919)
25. Kuryatov A, Luo J, Cooper J, and Lindstrom J (2005) Nicotine acts as a pharmacological chaperone to up-regulate human α4β2 acetylcholine receptors. Mol Pharmacol 68:1839-1851. (Pubitemid 41654365)
26. Lester HA, Xiao C, Srinivasan R, Son CD, Miwa J, Pantoja R, Banghart MR, Dougherty DA, Goate AM, and Wang JC (2009) Nicotine is a selective pharmacological chaperone of acetylcholine receptor number and stoichiometry. Implications for drug discovery. AAPS J 11:167-177.
27. Li J, Lee B, and Lee AS (2006) Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J Biol Chem 281:7260-7270. (Pubitemid 43847494)
28. Maiuolo J, Bulotta S, Verderio C, Benfante R, and Borgese N (2011) Selective activation of the transcription factor ATF6 mediates endoplasmic reticulum proliferation triggered by a membrane protein. Proc Natl Acad Sci USA 108:7832-7837.
29. Matsushita N, Okada H, Yasoshima Y, Takahashi K, Kiuchi K, and Kobayashi K (2002) Dynamics of tyrosine hydroxylase promoter activity during midbrain dopaminergic neuron development. J Neurochem 82:295-304. (Pubitemid 34774620)
30. 2α4 nicotinic receptor influences agonist sensitivity. J Biol Chem 286:31043-31054.
31. Miwa JM, Freedman R, and Lester HA (2011) Neural systems governed by nicotinic acetylcholine receptors: emerging hypotheses. Neuron 70:20-33.
32. Miyazaki I and Asanuma M (2009) Approaches to prevent dopamine quinoneinduced neurotoxicity. Neurochem Res 34:698-706.
33. Moss FJ, Imoukhuede PI, Scott K, Hu J, Jankowsky JL, Quick MW, and Lester HA (2009) GABA transporter function, oligomerization state, and anchoring: correlates with subcellularly resolved FRET. J Gen Physiol 134:489-521.
34. Nashmi R, Dickinson ME, McKinney S, Jareb M, Labarca C, Fraser SE, and 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. (Pubitemid 38021283)
35. Nashmi R, Xiao C, Deshpande P, McKinney S, Grady SR, Whiteaker P, Huang Q, McClure-Begley T, Lindstrom JM, Labarca C, et al. (2007) Chronic nicotine cell specifically upregulates functional α4*nicotinic receptors: basis for both tolerance in midbrain and enhanced long-term potentiation in perforant path. J Neurosci 27:8202-8218. (Pubitemid 47219619)
36. Peng X, Gerzanich V, Anand R, Whiting PJ, and Lindstrom J (1994) Nicotineinduced increase in neuronal nicotinic receptors results from a decrease in the rate of receptor turnover. Mol Pharmacol 46:523-530. (Pubitemid 24296687)
37. Quik M, Bordia T, Huang L, and Perez X (2011) Targeting nicotinic receptors for Parkinson's disease therapy. CNS Neurol Disord Drug Targets 10:651-658.
38. Rezvani K, Teng Y, and De Biasi M (2010) The ubiquitin-proteasome system regulates the stability of neuronal nicotinic acetylcholine receptors. J Mol Neurosci 40:177-184.
39. Rezvani K, Teng Y, Shim D, and De Biasi M. (2007) Nicotine regulates multiple synaptic proteins by inhibiting proteasomal activity. J Neurosci 27:10508-10519. (Pubitemid 47501994)
40. Richards CI, Srinivasan R, Xiao C, Mackey ED, Miwa JM, and Lester HA (2011) Trafficking of α4*nicotinic receptors revealed by superecliptic phluorin: effects of a β4 ALS-associated mutation and chronic exposure to nicotine. J Biol Chem 286:31241-31249.
41. Ritz B, Ascherio A, Checkoway H, Marder KS, Nelson LM, Rocca WA, Ross GW, Strickland D, Van Den Eeden SK, and Gorell J (2007) Pooled analysis of tobacco use and risk of Parkinson disease. Arch Neurol 64:990-997. (Pubitemid 47047999)
42. Ron D and Walter P (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8:519-529. (Pubitemid 46985379)
43. Ryu EJ, Harding HP, Angelastro JM, Vitolo OV, Ron D, and Greene LA (2002) Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. J Neurosci 22:10690-10698. (Pubitemid 36005143)
44. Sallette J, Pons S, Devillers-Thiery A, Soudant M, Prado de Carvalho L, Changeux JP, and Corringer PJ (2005) Nicotine upregulates its own receptors through enhanced intracellular maturation. Neuron 46:595-607.
45. Sasaya H, Utsumi T, Shimoke K, Nakayama H, Matsumura Y, Fukunaga K, and Ikeuchi T (2008) Nicotine suppresses tunicamycin-induced, but not thapsigargin-induced, expression of GRP78 during ER stress-mediated apoptosis in PC12 cells. J Biochem 144:251-257.
46. Schaub BE, Berger B, Berger EG, and Rohrer J (2006) Transition of galactosyltransferase 1 from trans-Golgi cisterna to the trans-Golgi network is signal mediated. Mol Biol Cell 17:5153-5162. (Pubitemid 44907358)
47. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S, and Kaufman RJ (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7:1165-1176. (Pubitemid 32607351)
48. Schwartz RD and Kellar KJ (1983) Nicotinic cholinergic receptor binding sites in the brain: regulation in vivo. Science 220:214-216. (Pubitemid 13115272)
49. Shen J and Prywes R (2005) ER stress signaling by regulated proteolysis of ATF6. Methods 35:382-389. (Pubitemid 40445372)
50. Shen J, Snapp EL, Lippincott-Schwartz J, and Prywes R (2005) Stable binding of ATF6 to BiP in the endoplasmic reticulum stress response. Mol Cell Biol 25:921-932. (Pubitemid 40165801)
51. Silva RM, Ries V, Oo TF, Yarygina O, Jackson-Lewis V, Ryu EJ, Lu PD, Marciniak SJ, Ron D, Przedborski S, et al. (2005) CHOP/GADD153 is a mediator of apoptotic death in substantia nigra dopamine neurons in an in vivo neurotoxin model of parkinsonism. J Neurochem 95:974-986. (Pubitemid 41713483)
52. Son CD, Moss FJ, Cohen BN, and Lester HA (2009) Nicotine normalizes intracellular subunit stoichiometry of nicotinic receptors carrying mutations linked to autosomal dominant nocturnal frontal lobe epilepsy. Mol Pharmacol 75:1137-1148.
53. Srinivasan R, Pantoja R, Moss FJ, Mackey ED, Son CD, Miwa J, and Lester HA (2011) Nicotine up-regulates α4β2 nicotinic receptors and ER exit sites via stoichiometry-dependent chaperoning. J Gen Physiol 137:59-79.
54. Surmeier DJ, Guzman JN, Sanchez-Padilla J, and Goldberg JA (2011) The origins of oxidant stress in Parkinson's disease and therapeutic strategies. Antioxid Redox Signal 14:1289-1301.
55. Tejada S, Lobo MV, García-Villanueva M, Sacristán S, Pérez-Morgado MI, Salinas M, and Martín ME (2009) Eukaryotic initiation factors (eIF) 2α and 4E expression, localization, and phosphorylation in brain tumors. J Histochem Cytochem 57:503-512.
56. Thayanidhi N, Helm JR, Nycz DC, Bentley M, Liang Y, and Hay JC (2010) α-Synuclein delays endoplasmic reticulum (ER)-to-Golgi transport in mammalian cells by antagonizing ER/Golgi SNAREs. Mol Biol Cell 21:1850-1863.
57. Warpman U, Friberg L, Gillespie A, Hellström-Lindahl E, Zhang X, and Nordberg A (1998) Regulation of nicotinic receptor subtypes following chronic nicotinic agonist exposure in M10 and SH-SY5Y neuroblastoma cells. J Neurochem 70:2028-2037. (Pubitemid 28207827)
58. Whiteaker P, Sharples CG, and Wonnacott S (1998) Agonist-induced up-regulation of α4β2 nicotinic acetylcholine receptors in M10 cells: pharmacological and spatial definition. Mol Pharmacol 53:950-962. (Pubitemid 28244084)
59. Xiao C, Nashmi R, McKinney S, Cai H, McIntosh JM, and Lester HA (2009) Chronic nicotine selectively enhances α4β2*nicotinic acetylcholine receptors in the nigrostriatal dopamine pathway. J Neurosci 29:12428-12439.
60. Xu J, Zhu Y, and Heinemann SF (2006) Identification of sequence motifs that target neuronal nicotinic receptors to dendrites and axons. J Neurosci 26:9780-9793. (Pubitemid 44427717)
61. Yang X and Buccafusco JJ (1994) Effect of chronic central treatment with the acetylcholine analog methylcarbamylcholine on cortical nicotinic receptors: correlation between receptor changes and behavioral function. J Pharmacol Exp Ther 271:651-659. (Pubitemid 24377747)