Beta amyloid differently modulate nicotinic and muscarinic receptor subtypes which stimulate in vitro and in vivo the release of glycine in the rat hippocampus

Frontiers in Pharmacology

Volumn 3 JUL, Issue , 2012, Pages

  Zappettini, Stefania ^a   Grilli, Massimo ^a   Olivero, Guendalina ^a   Mura, Elisa ^b   Preda, Stefania ^b   Govoni, Stefano ^b   Salamone, Alessia ^a   Marchi, Mario ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

Author keywords

Amyloid; Glycine release; Microdialysis; Muscarinic receptors; Nicotinic receptors

Indexed keywords

3 (2 AZETIDINYLMETHOXY)PYRIDINE; ACETYLCHOLINE; AMYLOID BETA PROTEIN[1-40]; BUNGAROTOXIN RECEPTOR; CHOLINE; GLYCINE; MUSCARINIC RECEPTOR; N (3 QUINUCLIDINYL)FURO[2,3 C]PYRIDINE 5 CARBOXAMIDE; NICOTINE; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA4BETA2; OXOTREMORINE; POTASSIUM CHLORIDE; VERATRIDINE;

ALZHEIMER DISEASE; AMINO ACID ANALYSIS; AMINO ACID SYNTHESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELLULAR SECRETION; CHOLINERGIC ACTIVITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; HIPPOCAMPUS; MALE; MICRODIALYSIS; NERVE STIMULATION; NEUROMODULATION; NONHUMAN; PROTEIN PROTEIN INTERACTION; RAT; SYNAPTOSOME;

EID: 84866157415     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2012.00146     Document Type: Article

References (51)

1. Baker, A. J., Zornow, M. H., Scheller, M. S., Yaksh, T. L, Skilling, S. R., Smullin, D. H., Larson, A. A., and Kuczenski, R. (1991). Changes in extracellular concentrations of glutamate, aspartate, glycine, dopamine, serotonin, and dopamine metabolites after transient global ischemia in the rabbit brain.. Neurochem. 57, 1370-1379.
2. Chen, L., Yamada, K., Nabeshima, T., and Sokabe, M. (2006). alpha7 Nicotinic acetylcholine receptor as a target to rescue deficit in hippocampal LTP induction in beta-amyloid infused rats. Neuropharmacology 50, 254-268.
3. Cramer, P. E., Cirrito, J. R., Wesson, D. W., Lee, C. Y., Karlo, J. C, Zinn, A. E., Casali, B. T., Restivo, J. L., Goebel, W. D., James, M. J., Brunden, K. R., Wilson, D. A., and Landreth, G. E. (2012). ApoE-directed therapeutics rapidly clear (3-amyloid and reverse deficits in AD mouse models. Science 335, 1503-1506.
4. Di Chiara, G. (1990). In-vivo brain dialysis of neurotransmitters. Trends Pharmacol Sci 11,116-121.
5. Dickinson, J. A., Hanrott, K. E., Mok, M. H., Kew, J. N., and Wonnacott, S. (2007). Differential coupling of alpha7 and nonalpha7 nicotinic acetylcholine receptors to calciuminduced calcium release and voltageoperated calcium channels in PC12 cells.. Neurochem. 100, 1089-1096.
6. Farrant, M., and Nusser, Z. (2005). Variations on an inhibitory theme: phasic and tonic activation of GABA(A) receptors. Nat. Rev. Neurosci. 6, 215-229.
7. Fedele, E., Varnier, G., Ansaldo, M. A., and Raiteri, M. (1998). Nicotine administration stimulates the in vivo N-methyl-D-aspartate receptornitric oxidecyclic GMP pathway in rat hippocampus through glutamate release. Br. J. Pharmacol. 125, 1042-1048.
8. Gill, J. K., Dhankher, P., Sheppard, T. D., Sher, E., and Millar, N. S. (2012). A series of a7 nicotinic acetylcholine receptor allosteric modulators with close chemical similarity but diverse pharmacological properties. Mol. Pharmacol. 81, 710-718.
9. Gill, J. K., Savolainen, M., Young, G. T., Zwart, R., Sher, E., and Millar, N. S. (2011). Agonist activation of alpha7 nicotinic acetylcholine receptors via an allosteric transmembrane site. Proc. Natl. Acad. Sci. U.S.A. 108, 5867-5872.
10. Grilli, M., Zappettini, S., Raiteri, L., and Marchi, M. (2009). Nicotinic and muscarinic cholinergic receptors coexist on GABAergic nerve endings in the mouse striatum and interact in modulating GABA release. Neuropharmacology 56, 610-614.
11. Hirai, H., Kirsch, J., Laube, B., Betz, H., and Kuhse, J. (1996). The glycine binding site of the N-methyl-D-aspartate receptor subunit NR1: identification of novel determinants of coagonist potentiation in the extracellular M3-M4 loop region. Proc. Natl. Acad. Sci. U.S.A. 93, 6031-6036.
12. Johnson, J. W., and Ascher, P. (1987). Glycine potentiates the NMDA response in cultured mouse brain neurons. Nature 325, 529-531.
13. Jiirgensen, S., and Ferreira, S. T. (2010). Nicotinic receptors, amyloid-beta, and synaptic failure in Alzheimer's disease.. Mol. Neurosci. 40, 221-229.
14. Kubota, H., Alle, H., Betz, H., and Geiger, J. R. (2010). Presynaptic glycine receptors on hippocampal mossy fibers. Biochem. Biophys. Res. Commun. 393,587-591.
15. Levin, E., and Simon, B. (1998). Nicotinic acetylcholine involvement in cognitive function in animals. Psychopharmacology (Berl.) 138, 217-230.
16. Lu, Y, Grady, S., Marks, M. J., Picciotto, M., Changeux, J. P., and Collins, A. C. (1998). Pharmacological characterization of nicotinic receptorstimulated GABA release from mouse brain synaptosomes.. Pharmacol. Exp. Ther. 287, 648.
17. Luccini, E., Romei, C, and Raiteri, L. (2008). Glycinergic nerve endings in hippocampus and spinal cord release glycine by different mechanisms in response to identical depolarizing stimuli.. Neurochem. 105, 2179-2189.
18. McQuiston, A. R., and Madison, D. V. (1999). Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus.. Neurosci. 19,2887-2896.
19. Mori, M., Gahwiler, B. H., and Gerber, U. (2002). Beta-alanine and taurine as endogenous agonists at glycine receptors in rat hippocampus in vitro.. Physiol (Land.) 539, 191-200.
20. Mukhin, A. G., Giindisch, D., Horti, A. G., Koren, A. O., Tamagnan, G., Kimes, A. S., Chambers, J., Vaupel, D. B., King, S. L., Picciotto, M. R., Innis, R. B., and London, E. D. (2000). 5-Iodo-A-85380, an alpha4beta2 subtypeselective ligand for nicotinic acetylcholine receptors. Mol. Pharmacol. 57, 642-649.
21. Mura, E., Lanni, C, Preda, S., Pistoia, F., Sara, M., Racchi, M., Schettini, G., Marchi, M., and Govoni, S. (2010a). Beta-amyloid: a disease target or a synaptic regulator affecting age-related neurotransmitter changes? Curr. Pharm. Des. 16, 672-683.
22. Mura, E., Preda, S., Govoni, S., Lanni, C, Trabace, L., Grilli, M., Lagomarsino, E, Pittaluga, A., and Marchi, M. (2010b). Specific neuromodulatory actions of amyloidbeta on dopamine release in rat nucleus accumbens and caudate putamen.. Alzheimers Dis. 19, 1041-1053.
23. Mura, E., Zappettini, S., Preda, S., Biundo, E, Lanni, C, Grilli, M., Cavallero, A., Olivero, G., Salamone, A., Govoni, S., and Marchi, M. (2012). Dual effect of beta-amyloid on α7 and α4(32 nicotinic receptors controlling the release of glutamate, aspartate and GABA in rat hippocampus. PLoS ONE 7, e29661. doi:10.1371joumal.pone.0029661
24. Nakamura, Y, Iga, K., Shibata, T., Shudo, M., and Kataoka, K. (1993). dial plasmalemmal vesicles: a subcellular fraction from rat hippocampal homogenate distinct from synaptosomes. Glia 9, 48-56.
25. Ondrejcak, T., Klyubin, I., Hu, N. W., Barry, A. E., Cullen, W. K., and Rowan, M. J. (2010). Alzheimer's disease amyloid beta-protein and synaptic function. Neuromokcular Med. 12, 13-26.
26. Parri, H. R., Hernandez, C. M., and Dineley, K. T. (2011). Research update: alpha7 nicotinic acetylcholine receptor mechanisms in Alzheimer's disease. Biochem. Pharmacol. 82,931-942.
27. Paxinos, G., and Watson, C. (1986). The Rat Brain in Stereotaxic Coordinates, 2nd Edn. New York: Academic Press.
28. Petrini, E. M., Marchionni, I., Zacchi, P., Sieghart, W., and Cherubini, E. (2004). Clustering of extrasynaptic GABA(A) receptors modulates tonic inhibition in cultured hippocampal neurons.. Biol. Chem. 279, 45833-45843.
29. Picciotto, M., Zoli, M., Lena, C, Bessis, A., Lallemand, Y., Le Novere, N., Vincent, P., Pich, E., Brulet, P., and Changeux, J. (1995). Abnormal avoidance learning in mice lacking functional highaffinity nicotine receptor in the brain. Nature 374, 65-67.
30. Preda, S., Govoni, S., Lanni, C, Racchi, M., Mura, E., Grilli, M., and Marchi, M. (2008). Acute betaamyloid administration disrupts the cholinergic control of dopamine release in the nucleus accumbens. Neuropsychopharmacology 33, 1062-1070.
31. Puzzo, D., Privitera, L., Leznik, E., Fa, M., Staniszewski, A., Palmeri, A., and Arancio, O. (2008). Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus.. Neurosci. 28, 14537-14545.
32. Raiteri, L., and Raiteri, M. (2000). Synaptosomes still viable after 25 years of superfusion. Neurochem. Res. 25, 1265-1274.
33. Raiteri, M., Leardi, R., and Marchi, M. (1984). Heterogeneity of presynaptic muscarinic receptors regulating neurotransmitter release in the rat brain.. Pharmacol. Exp. Ther. 228, 209.
34. Reaume, A. G., Howland, D. S., Trusko, S. P., Savage, M. J., Lang, D. M., Greenberg, B. D., Siman, R., and Scott, R. W. (1996). Enhanced amyloidogenic processing of the beta-amyloid precursor protein in gene-targeted mice bearing the Swedish familial Alzheimer's disease mutations and a "humanized" Abeta sequence.. Biol. Chem. 271, 23380-23388.
35. + exchangers and GlyT2 transporter reversal.. Neurochem. 119,50-63.
36. Romei, C, Luccini, E., Raiteri, M., and Raiteri, L. (2009). GABA(B) presynaptic receptors modulate glycine exocytosis from mouse spinal cord and hippocampus glycinergic nerve endings. Pharmacol. Res. 59, 154-159.
37. Russo, C, Marchi, M., Andrioli, G. C, Cavazzani, P., and Raiteri, M. (1993). Enhancement of glycine release from human brain cortex synaptosomes by acetylcholine acting at M4 muscarinic receptors.. Pharmacol. Exp. Ther. 266, 142.
38. Saransaari, P., and Oja, S. S. (2008). Effects of inhibitory amino acids on adenosine release in the mouse hippocampus. Proc. West. Pharmacol. Soc. 51,15-17.
39. Saransaari, P., Oja, S. S., Borkowska, H. D., Koistinaho, J., Hilgier, W., and Albrecht, J. (1997). Effects of thioacetamideinduced hepatic failure on the N-methyl-D-aspartate receptor complex in the rat cerebral cortex, striatum, and hippocampus. Binding of different ligands and expression of receptor subunit mRNAs. Mol. Chem. Neuropathol. 32, 179-193.
40. Sudweeks, S. N., and Yakel, J. L. (2000). Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons.. Physiol. (Lond.) 527(Pt 3), 515-528.
41. Toth,E. (1996). Effect of nicotine on the level of extracellular amino acids in the hippocampus of rat. Neurochem. Res. 21,903-907.
42. Uteshev, V., Meyer, E., and Papke, R. (2003). Regulation of neuronal function by choline and 4OH-GTS-21 through alpha 7 nicotinic receptors.. Neurophysiol. 89,1797-1806.
43. Wang, H. Y, Bakshi, K., Shen, C, Frankfurt, M., Trocme-Thibierge, C, and Morain, P. (2010). S 24795 limits beta-amyloid-alpha7 nicotinic receptor interaction and reduces Alzheimer's diseaselike pathologies. Biol. Psychiatry 67, 522-530.
44. Wang, H. Y, Stucky, A., Liu, J., Shen, C, Trocme-Thibierge, C, and Morain, P. (2009a). Dissociating beta-amyloid from alpha 7 nicotinic acetylcholine receptor by a novel therapeutic agent, S 24795, normalizes alpha 7 nicotinic acetylcholine and NMDA receptor function in Alzheimer's disease brain.. Neurosci. 29,10961-10973.
45. Wang, Y, Zhang, G., Zhou, H., Barakat, A., and Querfurth, H. (2009b). Opposite effects of low and high doses of Abeta42 on electrical network and neuronal excitability in the rat prefrontal cortex. PLoS ONE 4, e8366. doi:10.1371journal.pone.0008366
46. Wu, M. N., He, Y X., Guo, E, and Qi, J. S. (2008). Alpha4beta2 nicotinic acetylcholine receptors are required for the amyloid beta proteininduced suppression of long-term potentiation in rat hippocampal CA1 region in vivo. Brain Res. Bull. 77, 84-90.
47. Yakel, J., and Shao, Z. (2004). Functional and molecular characterization of neuronal nicotinic ACh receptors in rat hippocampal interneurons. Prog. Brain Res. 145, 95-107.
48. Young, G. T., Zwart, R., Walker, A. S., Sher, E., and Millar, N. S. (2008). Potentiation of alpha7 nicotinic acetylcholine receptors via an allosteric transmembrane site. Proc. Natl. Acad. Sci. U.S.A. 105, 14686-14691.
49. Zappettini, S., Grilli, M., Salamone, A., Fedele, E., and Marchi, M. (2010). Presynaptic nicotinic receptors evoke endogenous glutamate and aspartate release from hippocampal synaptosomes by way of distinct coupling mechanisms. Br. J. Pharmacol. 161, 1161-1171.
50. Zappettini, S., Mura, E., Grilli, M., Preda, S., Salamone, A., Olivero, G., Govoni, S., and Marchi, M. (2011). Different presynaptic nicotinic receptor subtypes modulate in vivo and in vitro the release of glycine in the rat hippocampus. Neurochem. Int. 59, 729-738.
51. Zhao, P., Qian, H., and Xia, Y (2005). GABA and glycine are protective to mature but toxic to immature rat cortical neurons under hypoxia. Eur. J. Neurosci. 22, 289-300.