Prolonged nicotine exposure down-regulates presynaptic NMDA receptors in dopaminergic terminals of the rat nucleus accumbens

Neuropharmacology

Volumn 79, Issue , 2014, Pages 488-497

  Salamone, Alessia ^a   Zappettini, Stefania ^a   Grilli, Massimo ^a   Olivero, Guendalina ^a   Agostinho, Paula ^c,d   Tomé, Angelo R ^b,c   Chen, Jiayang ^a   Pittaluga, Anna ^a   Cunha, Rodrigo A ^c,d   Marchi, Mario ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Calcium levels; Isolated nerve endings; Neurotransmitter release; Nicotinic receptors; NMDA receptors; Nucleus accumbens

Indexed keywords

4 AMINOPYRIDINE; 4 BENZYL ALPHA (4 HYDROXYPHENYL) BETA METHYL 1 PIPERIDINEPROPANOL; 5 IODO 3 (2 AZETIDINYLMETHOXY)PYRIDINE; BIOTIN; CPP 19755; DIHYDRO BETA ERYTHROIDINE; DIZOCILPINE; DOPAMINE; IFENPRODIL; MECAMYLAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; NICOTINE; NICOTINIC RECEPTOR; UNCLASSIFIED DRUG; ZINC CHLORIDE; AMINO ACID RECEPTOR BLOCKING AGENT; CALCIUM; N METHYLASPARTIC ACID; N-METHYL D-ASPARTATE RECEPTOR SUBTYPE 2A; NICOTINIC ACETYLCHOLINE RECEPTOR ALPHA4 SUBUNIT; NICOTINIC AGENT; NICOTINIC RECEPTOR ALPHA4BETA2; NICOTINIC RECEPTOR BLOCKING AGENT; NMDA RECEPTOR A1; NR2B NMDA RECEPTOR; POTASSIUM CHANNEL BLOCKING AGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; HUMAN; IMMUNOCYTOCHEMISTRY; INTERNALIZATION; LONG TERM EXPOSURE; MALE; NEUROCHEMISTRY; NEUROMODULATION; NONHUMAN; NUCLEUS ACCUMBENS; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR BLOCKING; RECEPTOR DOWN REGULATION; SYNAPTOSOME; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; METABOLISM; SPRAGUE DAWLEY RAT;

ANIMALS; CALCIUM; DOPAMINE; DOPAMINERGIC NEURONS; EXCITATORY AMINO ACID ANTAGONISTS; MALE; N-METHYLASPARTATE; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; NUCLEUS ACCUMBENS; POTASSIUM CHANNEL BLOCKERS; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, NICOTINIC; SYNAPTOSOMES;

EID: 84892589518     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.12.014     Document Type: Article

References (73)

1. L. Bard, and L. Groc Glutamate receptor dynamics and protein interaction: lessons from the NMDA receptor Mol. Cell. Neurosci. 48 2011 298 307
2. R.M. Brown, S. Mustafa, M.A. Ayoub, P.R. Dodd, K.D. Pfleger, and A.J. Lawrence mGlu5 Receptor functional interactions and addiction Front. Pharmacol. 3 2012 84
3. 2+ release from internal stores in adrenal chromaffin cells. Differential sensitivity to UTP and suramin J. Biol. Chem. 270 1995 5098 5106
4. B.S. Chen, and K.W. Roche Regulation of NMDA receptors by phosphorylation Neuropharmacology 53 2007 362 368
5. A receptors in cultured neurons of the rat inferior colliculus Sci. China Life Sci. 54 2011 560 566
6. S.V. Costes, D. Daelemans, E.H. Cho, Z. Dobbin, G. Pavlakis, and S. Lockett Automatic and quantitative measurement of protein-protein colocalization in live cells Biophys. J. 86 2004 3993 4003
7. N. Delibas, D.K. Doguc, R. Sutcu, E. Eroglu, and O. Gãkalp Effect of nicotine on hippocampal nicotinic acetylcholine alpha7 receptor and NMDA receptor subunits 2A and 2B expression in young and old rats Int. J. Neurosci. 115 2005 1151 1163
8. H.K. Delille, M. Mezler, and G.J. Marek The two faces of the pharmacological interaction of mGlu2 and 5-HT2A - relevance of receptor heterocomplexes and interaction through functional brain pathways Neuropharmacology 70 2013 296 305
9. J.M. Desce, G. Godeheu, T. Galli, F. Artaud, A. Chéramy, and J. Glowinski Lglutamate-evoked release of dopamine from synaptosomes of the rat striatum: involvement of AMPA and N-methyl-D-aspartate receptors Neuroscience 47 1992 333 339
10. G. Di Chiara Nucleus accumbens shell and core dopamine: differential role in behavior and addiction Behav. Brain Res. 137 2002 75 114
11. M.S. D'Souza, and A. Markou Neuronal mechanisms underlying development of nicotine dependence: implications for novel smoking-cessation treatments Addict. Sci. Clin. Pract. 6 2011 4 16
12. P.R. Dunkley, P.E. Jarvie, J.W. Heath, G.J.E. Kiddn, and J.A.P. Rostas A rapid method for isolation of synaptosomes on Percoll gradient Brain Res. 372 1986 115 129
13. L.P. Dwoskin, T.E. Wooters, S.P. Sumithran, K.B. Siripurapu, B.M. Joyce, P.R. Lockman, V.K. Manda, J.T. Ayers, Z. Zhang, A.G. Deaciuc, J.M. McIntosh, P.A. Crooks, and M.T. Bardo N,N'-Alkane-diyl-bis-3-picoliniums as nicotinic receptor antagonists: inhibition of nicotine-evoked dopamine release and hyperactivity J. Pharmacol. Exp. Ther. 326 2008 563 576
14. R. Exley, and S.J. Cragg Presynaptic nicotinic receptors: a dynamic and diverse cholinergic filter of striatal dopamine neurotransmission Br. J. Pharmacol 1 153 Suppl 2008 S283 S297
15. R. Exley, M.A. Clements, H. Hartung, J.M. McIntosh, and S.J. Cragg Alpha6-containing nicotinic acetylcholine receptors dominate the nicotine control of dopamine neurotransmission in nucleus accumbens Neuropsychopharmacology 33 2008 2158 2166
16. R. Fant, L. Owen, and J. Henningfield Nicotine replacement therapy Prim. Care 26 1999 633 652
17. M. Gao, Y. Jin, K. Yang, D. Zhang, R.J. Lukas, and J. Wu Mechanisms involved in systemic nicotine-induced glutamatergic synaptic plasticity on dopamine neurons in the ventral tegmental area J. Neurosci. 30 2010 13814 13825
18. R.C. Gonzalez, and P. Wintz Digital Image Processing second ed. 1987 Addison-Wesley Reading, MA, USA
19. C. Gotti, M. Moretti, A. Gaimarri, A. Zanardi, F. Clementi, and M. Zoli Heterogeneity and complexity of native brain nicotinic receptors Biochem. Pharmacol. 74 2007 1102 1111
20. M. Grilli, L. Patti, F. Robino, S. Zappettini, M. Raiteri, and M. Marchi Release-enhancing pre-synaptic muscarinic and nicotinic receptors co-exist and interact on dopaminergic nerve endings of rat nucleus accumbens J. Neurochem. 105 2008 2205 2213
21. M. Grilli, S. Zappettini, L. Raiteri, and M. Marchi Nicotinic and muscarinic cholinergic receptors coexist on GABAergic nerve endings in the mouse striatum and interact in modulating GABA release Neuropharmacology 56 2009 610 614
22. M. Grilli, A. Pittaluga, E. Merlo-Pich, and M. Marchi NMDA-mediated modulation of dopamine release is modified in rat prefrontal cortex and nucleus accumbens after chronic nicotine treatment J. Neurochem. 108 2009 408 416
23. M. Grilli, M. Summa, A. Salamone, G. Olivero, S. Zappettino, S. Di Prisco, M. Religioni, C. Usai, A. Pittaluga, and M. Marchi In vitro exposure to nicotine induces endocytosis of presynaptic AMPA receptors modulating dopamine release in rat nucleus accumbens nerve terminals Neuropharmacology 63 2012 916 926
24. J.E. Henningfield, E.T. Moolchan, and M. Zeller Regulatory strategies to reduce tobacco addiction in youth Tob. Control 1 12 Suppl. 2003 i14 i24
25. J. Hukkanen, P. Jacob, and N.L. Benowitz Metabolism and disposition kinetics of nicotine Pharmacol Rev. 57 2005 79 115
26. S. Ikemoto, and J. Panksepp The role of nucleus accumbens dopamine in motivated behavior: a unifying interpretation with special reference to reward-seeking Brain Res. Brain Res. Rev. 31 1999 6 41
27. L.D. Jayanthi, D.J. Samuvel, and S. Ramamoorthy Regulated internalization and phosphorylation of the native norepinephrine transporter in response to phorbol esters. Evidence for localization in lipid rafts and lipid raft-mediated internalization J. Biol. Chem. 30 2004 19315 19326
28. L.A. Johnson, C.A. Furman, M. Zhang, B. Guptaroy, and M.E. Gnegy Rapid delivery of the dopamine transporter to the plasmalemmal membrane upon amphetamine stimulation Neuropharmacology 49 2005 750 758
29. P.W. Kalivas The glutamate homeostasis hypothesis of addiction Nat. Rev. Neurosci. 10 2009 561 572
30. P.J. Kenny, E. Chartoff, M. Roberto, W.A. Carlezon Jr., and A. Markou NMDA receptors regulate nicotine-enhanced brain reward function and intravenous nicotine self-administration: role of the ventral tegmental area and central nucleus of the amygdala Neuropsychopharmacology 34 2009 266 281
31. G. Köhr NMDA receptor function: subunit composition versus spatial distribution Cell Tissue Res. 326 2006 439 446
32. C.G. Lau, and R.S. Zukin NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders Nat. Rev. Neurosci. 8 2007 413 426
33. B. Lendvai, and E.S. Vizi Nonsynaptic chemical transmission through nicotinic acetylcholine receptors Physiol. Rev. 88 2008 333 349
34. V. Lev-Ram, H. Miyakawa, N. Lasser-Ross, and W.N. Ross Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation J. Neurophysiol. 68 1992 1167 1177
35. E.D. Levin, Y. Tizabi, A.H. Rezvani, D.P. Caldwell, A. Petro, and B. Getachew Chronic nicotine and dizocilpine effects on regionally specific nicotinic and NMDA glutamate receptor binding Brain Res. 1041 2005 132 142
36. M.E. Liechti, and A. Markou Role of the glutamatergic system in nicotine dependence: implications for the discovery and development of new pharmacological smoking cessation therapies CNS Drugs 22 2008 705 724
37. H. Lin, S. Vicini, F.C. Hsu, S. Doshi, H. Takano, D.A. Coulter, and D.R. Lynch Axonal a7 nicotinic ACh receptors modulate presynaptic NMDA receptor expression and structural plasticity of glutamatergic presynaptic boutons Proc. Natl. Acad. Sci. U. S. A. 107 2010 16661 16666
38. Y. Liu, T.P. Wong, M. Aarts, A. Rooyakkers, L. Liu, T.W. Lai, D.C. Wu, J. Lu, M. Tymianski, A.M. Craig, and Y.T. Wang NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo J. Neurosci. 27 2007 2846 2857
39. E.M. Manders, J. Stap, G.J. Brakenhoff, R. van Driel, and J.A. Aten Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy J. Cell Sci. 103 1992 857 862
40. M. Marchi, and M. Grilli Presynaptic nicotinic receptors modulating neurotransmitter release in the central nervous system: functional interactions with other coexisting receptors Prog. Neurobiol. 92 2010 105 111
41. G.P. Mark, S. Shabani, L.K. Dobbs, and S.T. Hansen Cholinergic modulation of mesolimbic dopamine function and reward Physiol. Behav. 104 2011 76 81
42. 2+ signals mediated by P2X-type purinoceptors in cultured cerebellar Purkinje cells J. Neurosci. 18 1998 1704 1712
43. N.S. Millar, and C. Gott Diversity of vertebrate nicotinic acetylcholine receptors Neuropharmacology 56 2009 237 246
44. A. Nakajima, Y. Kinugasa, J. Torii, T. Hishinuma, Y. Tomioka, K. Yamada, and T. Yamakuni Repeated treatment with nicotine induces phosphorylation of NMDA receptor NR2B subunit in the brain regions involved in behavioral sensitization Neurosci. Lett. 524 2012 133 138
45. R.L. Papke, L.P. Dwoskin, P.A. Crooks, G. Zheng, Z. Zhang, J.M. McIntosh, and C. Stokes Extending the analysis of nicotinic receptor antagonists with the study of alpha6 nicotinic receptor subunit chimeras Neuropharmacology 54 2008 1189 1200
46. M. Parodi, L. Patti, M. Grilli, M. Raiteri, and M. Marchi Nicotine has a permissive role on the activation of metabotropic glutamate 5 receptors coexisting with nicotinic receptors on rat hippocampal noradrenergic nerve terminals Neurochem. Int. 48 2006 138 143
47. G. Pakinos, and C. Watson The Rat Brain in Stereotaxic Coordinates second ed. 1986 Academic Press San Diego, CA, USA
48. A. Pittaluga, R. Pattarini, M. Feligioni, and M. Raiteri NMDA receptors mediating hippocampal noradrenaline and striatal dopamine release display differential sensitivity to quinolinic acid, the HIV-1 envelope protein gp120, external pH and PKC inhibition J. Neurochem. 76 2001 139 148
49. A. Pittaluga, M. Feligioni, F. Longordo, M. Arvigo, and M. Raiteri Somatostatin-induced activation and up-regulation of N-methyl-D-aspartate receptor function: mediation through calmodulin-dependent protein kinase II, phospholipase C, protein kinase C, and tyrosine kinase in hippocampal noradrenergic nerve endings J. Pharmacol. Exp. Ther. 313 2005 242 249
50. M. Raiteri, B. Garrone, and A. Pittaluga N-methyl-D-aspartic acid (NMDA) and non-NMDA receptors regulating hippocampal norepinephrine release. II. Evidence for functional cooperation and for coexistence on the same axon terminal J. Pharmacol. Exp. Ther. 260 1992 238 242
51. K.J. Reissner, and P.W. Kalivas Using glutamate homeostasis as a target for treating addictive disorders Behav. Pharmacol. 21 2010 514 522
52. A.H. Rezvani, Y. Tizabi, B. Getachew, S.R. Hauser, D.P. Caldwell, C. Hunter, and E.D. Levin Chronic nicotine and dizocilpine effects on nicotinic and NMDA glutamatergic receptor regulation: interactions with clozapine actions and attentional performance in rats Prog. Neuropsychopharmacol. Biol. Psychiatry 32 2008 1030 1040
53. F. Risso, M. Parodi, M. Grilli, F. Molïno, M. Raiteri, and M. Marchi Chronic nicotine causes functional upregulation of ionotropic glutamate receptors mediating hippocampal noradrenaline and striatal dopamine release Neurochem. Int. 44 2004 293 301
54. F. Risso, M. Grilli, M. Parodi, M. Bado, M. Raiteri, and M. Marchi Nicotine exerts a permissive role on NMDA receptor function in hippocampal noradrenergic terminals Neuropharmacology 47 2004 65 71
55. B. Ritz, A. Ascherio, H. Checkoway, K.S. Marder, L.M. Nelson, W.A. Rocca, G.W. Ross, D. Strickland, S.K. Van Den Eeden, and J. Gorell Pooled analysis of tobacco use and risk of Parkinson disease Arch. Neurol. 64 2007 990 997
56. 2A and metabotropic group 5 receptors in glutamatergic nerve terminals of the rat striatum J. Neurochem. 92 2005 433 441
57. R.J. Rodrigues, T. Almeida, P.J. Richardson, C.R. Oliveira, and R.A. Cunha Dual presynaptic control by ATP of glutamate release via facilitatory P2X1, P2X2/3, and P2X3 and inhibitory P2Y1, P2Y2, and/or P2Y4 receptors in the rat hippocampus J. Neurosci. 25 2005 6286 6295
58. O. Salminen, K.L. Murphy, J.M. McIntosh, J. Drago, M.J. Marks, A.C. Collins, and S.R. Grady Subunit composition and pharmacology of two classes of striatal presynaptic nicotinic acetylcholine receptors mediating dopamine release in mice Mol. Pharmacol. 65 2004 1526 1535
59. H. Shen, T. Kihara, H. Hongo, X. Wu, W.R. Kem, S. Shimohama, A. Akaike, T. Niidome, and H. Sugimoto Neuroprotection by donepezil against glutamate excitotoxicity involves stimulation of alpha7 nicotinic receptors and internalization of NMDA receptors Br. J. Pharmacol. 161 2010 127 139
60. E. Sher, Y. Chen, T.J. Sharples, L.M. Broad, G. Benedetti, R. Zwart, G.I. McPhie, K.H. Pearson, T. Baldwinson, and G. De Filippi Physiological roles of neuronal nicotinic receptor subtypes: new insights on the nicotinic modulation of neurotransmitter release, synaptic transmission and plasticity Curr. Top. Med. Chem. 4 2004 283 297
61. Y. Takada, A. Yonezawa, T. Kume, H. Katsuki, S. Kaneko, H. Sugimoto, and A. Akaike Nicotinic acetylcholine receptor-mediated neuroprotection by donepezil against glutamate neurotoxicity in rat cortical neurons J. Pharmacol. Exp. Ther. 306 2003 772 777
62. M.T. Tebano, A. Martire, N. Rebola, R. Pepponi, M.R. Domenici, M.C. Grò, M.A. Schwarzschild, J.F. Chen, R.A. Cunha, and P. Popoli Adenosine A2A receptors and metabotropic glutamate 5 receptors are co-localized and functionally interact in the hippocampus: a possible key mechanism in the modulation of N-methyl-D-aspartate effects J. Neurochem. 95 2005 1188 1200
63. O.A. Timofeeva, and E.D. Levin Glutamate and nicotinic receptor interactions in working memory: importance for the cognitive impairment of schizophrenia Neuroscience 195 2011 21 36
64. S.F. Traynelis, L.P. Wollmuth, C.J. McBain, F.S. Menniti, K.M. Vance, K.K. Ogden, K.B. Hansen, H. Yuan, S.J. Myers, and R. Dingledine Glutamate receptor ion channels: structure, regulation, and function Pharmacol. Rev. 62 2010 405 496
65. P. Vieyra-Reyes, M.R. Picciotto, and Y.S. Mineur Voluntary oral nicotine intake in mice down-regulates GluR2 but does not modulate depression-like behaviors Neurosci. Lett. 434 2008 18 22
66. E. Vizi, and B. Lendvai Modulatory role of presynaptic nicotinic receptors in synaptic and non-synaptic chemical communication in the central nervous system Brain Res. Brain Res. Rev. 30 1999 219 235
67. E.S. Vizi, M. Kisfali, and T. Lorincz Role of nonsynaptic GluN2B-containing NMDA receptors in excitotoxicity: evidence that fluoxetine selectively inhibits these receptors and may have neuroprotective effects Brain Res Bull. 93 2013 32 38
68. F. Wang, H. Chen, J.D. Steketee, and B.M. Sharp Upregulation of ionotropic glutamate receptor subunits within specific mesocorticolimbic regions during chronic nicotine self-administration Neuropsychopharmacology 32 2007 103 109
69. H.Y. Wang, K. Bakshi, C. Shen, M. Frankfurt, C. Trocmé-Thibierge, and P. Morain S 24795 limits beta-amyloid-alpha7 nicotinic receptor interaction and reduces Alzheimer's disease-like pathologies Biol. Psychiatry 67 2010 522 530
70. M. Wang, Y. Yang, Z. Dong, J. Cao, and L. Xu NR2B-containing N-methyl-D-aspartate subtype glutamate receptors regulate the acute stress effect on hippocampal long-term potentiation/long-term depression in vivo Neuroreport 17 2006 1343 1346
71. Y.T. Wang, and M.W. Salter Regulation of NMDA receptors by tyrosine kinases and phosphatases Nature 369 1994 233 235
72. Y. Yamazaki, Y. Jia, R. Niu, and K. Sumikawa Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus Eur. J. Neurosci. 23 2006 1819 1828
73. J. Yang, S.E. Chamberlain, G.L. Woodhall, and R.S. Jones Mobility of NMDA autoreceptors but not postsynaptic receptors at glutamate synapses in the rat entorhinal cortex J. Physiol. 586 2008 4905 4924