Nicotinic α7 receptor activation selectively potentiates the function of NMDA receptors in glutamatergic terminals of the nucleus accumbens

Frontiers in Cellular Neuroscience

Volumn 8, Issue OCT, 2014, Pages

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

^a INSERM   (France)

^b UNIVERSITY OF GENOA   (Italy)

^c UNIVERSITY OF COIMBRA   (Portugal)

^d UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Neurotransmitters release; Nicotine Treatment; Nicotinic receptors; NMDA receptors; Nucleus accumbens; Synaptosomes

Indexed keywords

2 AMINO 5 PHOSPHONOVALERIC ACID; ALPHA BUNGAROTOXIN; BUNGAROTOXIN RECEPTOR; CHOLINE; DIZOCILPINE; GLUTAMATE RECEPTOR; IFENPRODIL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NICOTINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; CONTROLLED STUDY; EVOKED RESPONSE; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MALE; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEUS ACCUMBENS; POLYACRYLAMIDE GEL ELECTROPHORESIS; RADIOACTIVITY; RAT; RECEPTOR BINDING; SYNAPTOSOME; WESTERN BLOTTING;

EID: 84908006452     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00332     Document Type: Article

References (42)

1. Ávila-Ruiz, T., Carranza, V., Gustavo, L. L., Limón, D. I., Martínez, I., Flores, G., et al. (2014). Chronic administration of nicotine enhances NMDA-activated currents in the prefrontal cortex and core part of the nucleus accumbens of rats. Synapse 68, 248–256. doi: 10.1002/syn.21726
2. Bardoni, R., Torsney, C., Tong, C. K., Prandini, M., and MacDermott, A. B. (2004). Presynaptic NMDA receptors modulate glutamate release from primary sensory neurons in rat spinal cord dorsal horn. J. Neurosci. 24, 2774–2781. doi: 10. 1523/jneurosci.4637-03.2004
3. Bidoret, C., Ayon, A., Barbour, B., and Casado, M. (2009). Presynaptic NR2A-containing NMDA receptors implement a high-pass filter synaptic plasticity rule. Proc. Natl. Acad. Sci. U S A 106, 14126–14131. doi: 10.1073/pnas. 0904284106
4. Callahan, P. M., Terry, A. V., and Tehim, A. (2014). Effects of the nicotinic α7 receptor partial agonist GTS-21 on NMDA-glutamatergic receptor related deficits in sensorimotor gating and recognition memory in rats. Psychopharma-cology (Berl) 231, 3695–3706. doi: 10.1007/s00213-014-3509-2
5. Carlezon, W. A., and Thomas, M. J. (2009). Biological substrates of reward and aversion: a nucleus accumbens activity hypothesis. Neuropharmacology 56(Suppl 1), 122–132. doi: 10.1016/j.neuropharm.2008.06.075
6. 2+ release from internal stores in adrenal chromaffin cells. Differential sensitivity to UTP and suramin. J. Biol. Chem. 270, 5098–5106. doi: 10.1074/jbc. 270.10.5098
7. Chen, B. S., and Roche, K. W. (2007). Regulation of NMDA receptors by phos-phorylation. Neuropharmacology 53, 362–368. doi: 10.1016/j.neuropharm.2007. 05.018
8. 2A receptor heteromers. J. Neurosci. 26, 2080–2087. doi: 10. 1523/jneurosci.3574-05.2006
9. Corlew, R., Brasier, D. J., Feldman, D. E., and Philpot, B. D. (2008). Presynaptic NMDA receptors: newly appreciated roles in cortical synaptic function and plasticity. Neuroscientist 14, 609–625. doi: 10.1177/1073858408322675
10. Delibas, N., Doguc, D. K., Sutcu, R., Eroglu, E., and Gökalp, O. (2005). 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, 1151–1163. doi: 10.1080/00207450590914437
11. Dickinson, J. A., Hanrott, K. E., Mok, M. H., Kew, J. N., and Wonnacott, S. (2007). Differential coupling of alpha7 and non-alpha7 nicotinic acetylcholine receptors to calcium-induced calcium release and voltage-operated calcium channels in PC12 cells. J. Neurochem. 100, 1089–1096. doi: 10.1111/j.1471-4159.2006. 04273.x
12. Dickinson, J. A., Kew, J. N., and Wonnacott, S. (2008). Presynaptic alpha 7-and beta 2-containing nicotinic acetylcholine receptors modulate excitatory amino acid release from rat prefrontal cortex nerve terminals via distinct cellular mechanisms. Mol. Pharmacol. 74, 348–359. doi: 10.1124/mol.108.04 6623
13. Dorostkar, M. M., and Boehm, S. (2008). Presynaptic ionotropic receptors. Handb. Exp. Pharmacol. 184, 479–527. doi: 10.1007/978-3-540-74805-2_15
14. Giocomo, L. M., and Hasselmo, M. E. (2007). Neuromodulation by glutamate and acetylcholine can change circuit dynamics by regulating the relative influence of afferent input and excitatory feedback. Mol. Neurobiol. 36, 184–200. doi: 10. 1007/s12035-007-0032-z
15. Gomez-Varela, D., and Berg, D. K. (2013). Lateral mobility of presynaptic α7-containing nicotinic receptors and its relevance for glutamate release. J. Neurosci. 33, 17062–17071. doi: 10.1523/jneurosci.1482-13.2013
16. Grilli, M., Patti, L., Robino, F., Zappettini, S., Raiteri, M., and Marchi, M. (2008). Release-enhancing pre-synaptic muscarinic and nicotinic receptors co-exist and interact on dopaminergic nerve endings of rat nucleus accumbens. J. Neurochem. 105, 2205–2213. doi: 10.1111/j.1471-4159.2008.05307.x
17. Grilli, M., Summa, M., Salamone, A., Olivero, G., Zappettini, S., Di Prisco, S., et al. (2012). In vitro exposure to nicotine induces endocytosis of presynaptic AMPA receptors modulating dopamine release in rat nucleus accumbens nerve terminals. Neuropharmacology 63, 916–926. doi: 10.1016/j.neuropharm.2012. 06.049
18. Grilli, M., Zappettini, S., Raiteri, L., and Marchi, M. (2009). Nicotinic and mus-carinic cholinergic receptors coexist on GABAergic nerve endings in the mouse striatum and interact in modulating GABA release. Neuropharmacology 56, 610–614. doi: 10.1016/j.neuropharm.2008.10.014
19. Grueter, B. A., Rothwell, P. E., and Malenka, R. C. (2012). Integrating synaptic plasticity and striatal circuit function in addiction. Curr. Opin. Neurobiol. 22, 545–551. doi: 10.1016/j.conb.2011.09.009
20. Kalivas, P. W., and Volkow, N. D. (2011). New medications for drug addiction hiding in glutamatergic neuroplasticity. Mol. Psychiatry 16, 974–986. doi: 10. 1038/mp.2011.46
21. Lan, J. Y., Skeberdis, V. A., Jover, T., Grooms, S. Y., Lin, Y., Araneda, R. C., et al. (2001). Protein kinase C modulates NMDA receptor trafficking and gating. Nat. Neurosci. 4, 382–390. doi: 10.1038/86028
22. Lau, C. G., and Zukin, R. S. (2007). NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat. Rev. Neurosci. 8, 413–426. doi: 10. 1038/nrn2171
23. Levin, E. D., Tizabi, Y., Rezvani, A. H., Caldwell, D. P., Petro, A., and Getachew, B. (2005). Chronic nicotine and dizocilpine effects on regionally specific nicotinic and NMDA glutamate receptor binding. Brain Res. 1041, 132–142. doi: 10. 1016/j.brainres.2005.01.104
24. Lev-Ram, V., Miyakawa, H., Lasser-Ross, N., and Ross, W. N. (1992). Calcium transients in cerebellar Purkinje neurons evoked by intracellular stimulation. J. Neurophysiol. 68, 1167–1177.
25. Li, S., Nai, Q., Lipina, T. V., Roder, J. C., and Liu, F. (2013). α7nAchR/NMDAR coupling affects NMDAR function and object recognition. Mol. Brain 6:58. doi: 10.1186/1756-6606-6-58
26. Liechti, M. E., and Markou, A. (2008). Role of the glutamatergic system in nicotine dependence: implications for the discovery and development of new pharmacological smoking cessation therapies. CNS Drugs 22, 705–724. doi: 10. 2165/00023210-200822090-00001
27. Lin, H., Vicini, S., Hsu, F. C., Doshi, S., Takano, H., Coulter, D. A., et al. (2010). Axonal α7 nicotinic ACh receptors modulate presynaptic NMDA receptor expression and structural plasticity of glutamatergic presynaptic boutons. Proc. Natl. Acad. Sci. U S A 107, 16661–16666. doi: 10.1073/pnas.1007397107
28. Luccini, E., Musante, V., Neri, E., Raiteri, M., and Pittaluga, A. (2007). N-methyl-D-aspartate autoreceptors respond to low and high agonist concentrations by facilitating, respectively, exocytosis and carrier-mediated release of glutamate in rat hippocampus. J. Neurosci. Res. 85, 3657–3665. doi: 10.1002/jnr.21446
29. Ma, Y. Y., Cepeda, C., and Cui, C. L. (2009). The role of striatal NMDA receptors in drug addiction. Int. Rev. Neurobiol. 89, 131–146. doi: 10.1016/s0074-7742(09)89006-5
30. MacDermott, A. B., Role, L. W., and Siegelbaum, S. A. (1999). Presynaptic ionotropic receptors and the control of transmitter release. Annu. Rev. Neurosci. 22, 443–485. doi: 10.1146/annurev.neuro.22.1.443
31. Marchi, M., Risso, F., Viola, C., Cavazzani, P., and Raiteri, M. (2002). Direct evidence that release-stimulating alpha7* nicotinic cholinergic receptors are localized on human and rat brain glutamatergic axon terminals. J. Neurochem. 80, 1071–1078. doi: 10.1046/j.0022-3042.2002.00805.x
32. McGehee, D. S., Heath, M. J., Gelber, S., Devay, P., and Role, L. W. (1995). Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269, 1692–1696. doi: 10.1126/science.7569895
33. 2+ ions. J. Neurochem. 117, 516–527. doi: 10.1111/j.1471-4159.2011.07223.x
34. Paxinos, G., and Watson, C. (1986). The Rat Brain in Stereotaxic Coordinates. 2nd Edn. San Diego, CA, USA: Academic Press.
35. Reissner, K. J., and Kalivas, P. W. (2010). Using glutamate homeostasis as a target for treating addictive disorders. Behav. Pharmacol. 21, 514–522. doi: 10.1097/fbp. 0b013e32833d41b2
36. Rodrigues, R. J., Almeida, T., Richardson, P. J., Oliveira, C. R., and Cunha, R. A. (2005). 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, 6286–6295. doi: 10.1523/jneurosci.0628-05.2005
37. Salamone, A., Zappettini, S., Grilli, M., Olivero, G., Agostinho, P., Tomé, A. R., et al. (2014). Prolonged nicotine exposure down-regulates presynaptic NMDA receptors in dopaminergic terminals of the rat nucleus accumbens. Neurophar-macology 79, 488–497. doi: 10.1016/j.neuropharm.2013.12.014
38. Sjöström, P. J., Turrigiano, G. G., and Nelson, S. B. (2003). Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39, 641–654. doi: 10.1016/s0896-6273(03)00476-8
39. Timofeeva, O. A., and Levin, E. D. (2011). Glutamate and nicotinic receptor interactions in working memory: importance for the cognitive impairment of schizophrenia. Neuroscience 195, 21–36. doi: 10.1016/j.neuroscience.2011. 08.038
40. Wang, F., Chen, H., Steketee, J. D., and Sharp, B. M. (2007). Upregulation of ionotropic glutamate receptor subunits within specific mesocorticolimbic regions during chronic nicotine self-administration. Neuropsychopharmacology 32, 103–109. doi: 10.1038/sj.npp.1301033
41. Yamazaki, Y., Jia, Y., Niu, R., and Sumikawa, K. (2006). Nicotine exposure in vivo induces long-lasting enhancement of NMDA receptor-mediated currents in the hippocampus. Eur. J. Neurosci. 23, 1819–1828. doi: 10.1111/j.1460-9568.2006. 04714.x
42. Zappettini, S., Grilli, M., Salamone, A., Fedele, E., and Marchi, M. (2010). Pre-synaptic nicotinic receptors evoke endogenous glutamate and aspartate release from hippocampal synaptosomes by way of distinct coupling mechanisms. Br. J. Pharmacol 161, 1161–1171. doi: 10.1111/j.1476-5381.2010.00958.x