AMPA receptor upregulation in the nucleus accumbens shell of cocaine-sensitized rats depends upon S-nitrosylation of stargazin

Neuropharmacology

Volumn 77, Issue , 2014, Pages 28-38

  Selvakumar, Balakrishnan ^a   Campbell, Peter W ^b   Milovanovic, Mike ^b   Park, Diana J ^b   West, Anthony R ^b   Snyder, Solomon H ^a   Wolf, Marina E ^b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

Author keywords

AMPA receptor; Cocaine; Nitric oxide synthase; Nitrosylation; Nucleus accumbens; Stargazin; TARP

Indexed keywords

AMPA RECEPTOR; COCAINE; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REGULATOR PROTEIN; STARGAZIN PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTROCHEMICAL DETECTION; ENZYME ACTIVATION; INTRACELLULAR SIGNALING; MALE; NEUROMODULATION; NITROSYLATION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; UPREGULATION; WITHDRAWAL SYNDROME;

AMPA RECEPTOR; AMPAR; BIS(SULFOSUCCINIMIDYL)SUBERATE; BS(3); CA(2+)/CALMODULIN-DEPENDENT PROTEIN KINASE II; CAMKII; COCAINE; L-NAME; L-NG-NITROARGININE METHYL ESTER; NAC; NEURONAL NOS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITROSYLATION; NNOS; NO; NOS; NUCLEUS ACCUMBENS; SNP; SODIUM NITROPRUSSIDE; STARGAZIN; TARP; TRANSMEMBRANE AMPA RECEPTOR REGULATORY PROTEIN; WD; WITHDRAWAL DAY;

ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; CALCIUM CHANNELS; COCAINE; COCAINE-RELATED DISORDERS; MALE; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; UP-REGULATION;

EID: 84885467092     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.08.036     Document Type: Article

References (48)

1. A.C. Boudreau, C.R. Ferrario, M.J. Glucksman, and M.E. Wolf Signaling pathway adaptations and novel protein kinase A substrates related to behavioral sensitization to cocaine J. Neurochem. 110 2009 363 377
2. A.C. Boudreau, M. Milovanovic, K.L. Conrad, C. Nelson, C.R. Ferrario, and M.E. Wolf A protein cross-linking assay for measuring cell surface expression of glutamate receptors subunits in the rodent brain after in vivo treatments Curr. Protocols. Neurosci. 2012 April; Chapter 5, Unit 5.30.1-19.
3. A.C. Boudreau, J.M. Reimers, M. Milovanovic, and M.E. Wolf Cell surface AMPA receptors in the nucleus accumbens increase during cocaine withdrawal but internalize after cocaine challenge in association with altered activation of mitogen-activated protein kinases J. Neurosci. 27 2007 10621 10635 (Pubitemid 47502017)
4. A.C. Boudreau, and M.E. Wolf Behavioral sensitization to cocaine is associated with increased AMPA receptor surface expression in the nucleus accumbens J. Neurosci. 25 2005 9144 9151 (Pubitemid 41500822)
5. J.J. Byrnes, M.M. Pantke, J.A. Onton, and R.P. Hammer Inhibition of nitric oxide synthase in the ventral tegmental area attenuates cocaine sensitization in rats Prog. Neuro-Psychopharmacol. Biol. Psychiatry 24 2000 261 273 (Pubitemid 30159535)
6. S.L. Collins, and K.M. Kantak Neuronal nitric oxide synthase inhibition decreases cocaine self-administration behavior in rats Psychopharmacology 159 4 2002 361 369 (Pubitemid 34143360)
7. M.A. Dwyer, D.S. Bredt, and S.H. Snyder Nitric oxide synthase: irreversible inhibition by L-NG-nitroarginine in brain in vitro and in vivo Biochem. Biophys. Res. Commun. 176 1991 1136 1141
8. C.R. Ferrario, X. Li, X. Wang, J.M. Reimers, J.L. Uejima, and M.E. Wolf The role of glutamate receptor redistribution in locomotor sensitization to cocaine Neuropsychopharmacology 35 2010 818 833
9. 2+-permeable AMPA receptors during the incubation of cocaine craving Neuropharmacology 61 2011 1141 1151
10. C.R. Ferrario, J.A. Loweth, M. Milovanovic, X. Wang, and M.E. Wolf Distribution of AMPA receptor subunits and TARPs in synaptic and extrasynaptic membranes of the adult rat nucleus accumbens Neurosci. Lett. 490 2011 180 184
11. S.J. French, G.P. Ritson, S. Hidaka, and S. Totterdell Nucleus accumbens nitric oxide immunoreactive interneurons receive nitric oxide and ventral subicular afferents in rats Neuroscience 135 2005 121 131 (Pubitemid 41219743)
12. J. Garthwaite Concepts of neural nitric oxide-mediated transmission Eur. J. Neurosci. 27 2008 2783 2802 (Pubitemid 351832227)
13. M.B. Ghasemzadeh, C. Mueller, and P. Vasudevan Behavioral sensitization to cocaine is associated with increased glutamate receptor trafficking to the postsynaptic density after extended withdrawal period Neuroscience 159 2009 414 426
14. J.L. Haracz, J.S. MacDonall, and R. Sircar Effects of nitric oxide synthase inhibitors on cocaine sensitization Brain Res. 746 1997 183 189 (Pubitemid 27060346)
15. D.T. Hess, A. Matsumoto, S.O. Kim, H.E. Marshall, and J.S. Stamler Protein S-nitrosylation: purview and parameters Nat. Rev. Mol. Cell. Biol. 6 2005 150 166 (Pubitemid 40215810)
16. S. Hidaka, and S. Totterdell Ultrastructural features of the nitric oxide synthase-containing interneurons in the nucleus accumbens and their relationship with tyrosine hydroxylase-containing terminals J. Comp. Neurol. 431 2001 139 154 (Pubitemid 32118650)
17. K.E. Hoque, and A.R. West Dopaminergic modulation of nitric oxide synthase activity in subregions of the rat nucleus accumbens Synapse 66 2012 220 231
18. Y.H. Huang, Y. Lin, P. Mu, B.R. Lee, T.E. Brown, G. Wayman, H. Marie, W. Liu, Z. Yan, B.A. Sorg, O.M. Schlüter, R.S. Zukin, and Y. Dong In vivo cocaine experience generates silent synapses Neuron 63 2009 40 47
19. Y. Huang, H.-Y. Man, Y. Sekine-Aizawa, Y. Han, K. Juluri, H. Luo, J. Cheah, C. Lowenstein, R.L. Huganir, and S.H. Snyder S-nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors Neuron 46 2005 533 540 (Pubitemid 40797379)
20. Y. Itzhak Modulation of cocaine- and methamphetamine-induced behavioral sensitization by inhibition of brain nitric oxide synthase J. Pharmacol. Exp. Ther. 282 1997 521 527 (Pubitemid 27340148)
21. Y. Itzhak, S.F. Ali, J.L. Martin, M.D. Black, and P.L. Huang Resistance of neuronal nitric oxide synthase-deficient mice to cocaine-induced locomotor sensitization Psychopharmacology 140 1998 378 386 (Pubitemid 28562458)
22. Y. Itzhak, J.L. Martin, M.D. Black, and P.L. Huang The role of nitric oxide synthase in cocaine-induced conditioned place preference NeuroReport 9 11 1998 2485 2488 (Pubitemid 28387135)
23. Y. Itzhak Role of the NMDA receptor and nitric oxide in memory reconsolidation of cocaine-induced conditioned place preference in mice Ann. N. Y. Acad. Sci. 1139 2008 350 357
24. A.C. Jackson, and R.A. Nicoll Neuroscience: AMPA receptors get 'pickled' Nature 458 2009 585 586
25. A.C. Jackson, and R.A. Nicoll The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits Neuron 70 2011 178 199
26. H.S. Kim, and W.K. Park Nitric oxide mediation of cocaine-induced dopaminergic behaviors: ambulation-accelerating activity, reverse tolerance and conditioned place preference in mice J. Pharmacol. Exp. Ther. 275 1995 551 557
27. S. Kourrich, P.E. Rothwell, J.R. Klug, and M.J. Thomas Cocaine experience controls bidirectional synaptic plasticity in the nucleus accumbens J. Neurosci. 27 2007 7921 7928 (Pubitemid 47173313)
28. D.K. Lee, W.C.A. Koh, Y.B. Shim, I. Shim, and E.S. Choe Repeated cocaine administration increases nitric oxide efflux in the rat dorsal striatum Psychopharmacology 208 2010 245 256
29. D.K. Lee, S.M. Ahn, Y.B. Shim, W.C.A. Koh, I. Shim, and E.S. Choe Interactions of dopamine D1 and NMDA receptors are required for acute cocaine-evoked nitric oxide efflux in the dorsal striatum Exp. Neurobiol. 20 2 2011 116 122
30. J.E. McCutcheon, X. Wang, K.Y. Tseng, M.E. Wolf, and M. Marinelli Calcium-permeable AMPA receptors are present in nucleus accumbens synapses after long withdrawal from cocaine self-administration but not experimenter- administered cocaine J. Neurosci. 31 2011 5737 5743
31. F.J. Nasif, X.-T. Hu, O.A. Ramirez, and M.F. Perez Inhibition of nitric oxide synthase prevents alterations in medial prefrontal cortex excitability induced by repeated cocaine administration Psychopharmacology 218 2011 323 330
32. C. Orsini, E. Izzo, G.F. Koob, and L. Pulvirenti Blockade of nitric oxide synthesis reduces responding for cocaine self-administration during extinction and reinstatement Brain Res. 925 2002 133 140 (Pubitemid 34131629)
33. D.J. Park, and A.R. West Regulation of striatal nitric oxide synthesis by local dopamine and glutamate interactions J. Neurochem. 111 2009 1457 1465
34. C.M. Pudiak, and M.A. Bozarth The effect of nitric oxide synthesis inhibition on intravenous cocaine self-administration Prog. Neuro- Psychopharmacol. Biol. Psychiatry 26 1 2002 189 196 (Pubitemid 34045167)
35. L. Pulvirenti, C. Balducci, and G.F. Koob Inhibition of nitric oxide synthesis reduces intravenous cocaine self-administration in the rat Neuropharmacology 35 1996 1811 1814 (Pubitemid 27090801)
36. J.M. Reimers, M. Milovanovic, and M.E. Wolf Quantitative analysis of AMPA receptor subunit composition in addiction-related brain regions Brain Res. 1367 2011 223 233
37. T.E. Robinson, and K.C. Berridge The incentive sensitization theory of addiction: some current issues Philos. Trans. R. Soc. Lond. B. Biol. Sci. 363 2008 3137 3146
38. S. Sammut, and A.R. West Acute cocaine administration increases NO efflux in the rat prefrontal cortex via a neuronal NOS-dependent mechanism Synapse 62 9 2008 710 713 (Pubitemid 352032546)
39. 2+ channels mediate cocaine-induced GluA1 trafficking in the nucleus accumbens, a long-term adaptation dependent on ventral tegmental area Ca(v)1.3 channels J. Neurosci. 31 2011 13562 13575
40. J. Schumann, and R. Yaka Prolonged withdrawal from repeated noncontingent cocaine exposure increases NMDA receptor expression and ERK activity in the nucleus accumbens J. Neurosci. 29 2009 6955 6963
41. B. Selvakumar, R.L. Huganir, and S.H. Snyder S-nitrosylation of stargazin regulates surface expression of AMPA-glutamate neurotransmitter receptors Proc. Natl. Acad. Sci. U. S. A. 106 2009 16440 16445
42. B. Selvakumar, M.A. Jenkins, N.K. Hussain, R.L. Huganir, S.F. Traynelis, and S.H. Snyder S-nitrosylation of AMPA receptor GluA1 regulates phosphorylation, single-channel conductance, and endocytosis Proc. Natl. Acad. Sci. U. S. A. 110 3 2012 1077 1082
43. Y. Serulle, S. Zhang, I. Ninan, D. Puzzo, M. McCarthy, L. Khatri, O. Arancio, and E.B. Ziff A GluR1-cGKII interaction regulates AMPA receptor trafficking Neuron 56 2007 670 688 (Pubitemid 350102028)
44. S.R. Sesack, and A.A. Grace Cortico-basal ganglia reward network: microcircuitry Neuropsychopharmacology 35 2010 27 47
45. C. Straub, and S. Tomita The regulation of glutamate receptor trafficking and function by TARPs and other transmembrane auxilliary subunits Curr. Opin. Neurobiol. 22 2012 488 495
46. K.T. Wakabayashi, and E.A. Kiyatkin Rapid changes in extracellular glutamate induced by natural arousing stimuli and intravenous cocaine in the nucleus accumbens shell and core J. Neurophysiol. 108 2012 285 299
47. M.E. Wolf The Bermuda triangle of cocaine-induced neuroadaptations Trends Neurosci. 33 2010 391 398
48. M.E. Wolf, and C.R. Ferrario AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine Neurosci. Biobehav. Rev. 35 2010 185 211