Effects of soluble β-amyloid on the release of neurotransmitters from rat brain synaptosomes

Frontiers in Aging Neuroscience

Volumn 6, Issue JUL, 2014, Pages

  Olivero, Guendalina ^a   Grilli, Massimo ^a   Chen, Jiayang ^a   Preda, Stefania ^b   Mura, Elisa ^b   Govoni, Stefano ^b   Marchi, Mario ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

Author keywords

Alzheimer's disease; Beta amyloid; Dopamine release; Muscarinic receptors; Nicotinic receptors

Indexed keywords

ALPHA CONOTOXIN MII; AMYLOID BETA PROTEIN[1-40]; DESFORMYLFLUSTRABROMINE; DOPAMINE; GALANTAMINE; MUSCARINIC RECEPTOR; NEUROTRANSMITTER; NICOTINIC RECEPTOR; NORADRENALIN; OXOTREMORINE; UNCLASSIFIED DRUG;

ADULT; ALLOSTERISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN PERFUSION; BRAIN SYNAPTOSOME; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG ANTAGONISM; DRUG BINDING SITE; IN VITRO STUDY; MALE; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEUS ACCUMBENS; RAT;

EID: 84904655289     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00166     Document Type: Article

References (53)

1. Azam, L., and McIntosh, J. M. (2006). Characterization of nicotinic acetylcholine receptors that modulate nicotine-evoked [3H]norepinephrine release from mouse hippocampal synaptosomes. Mol. Pharmacol. 70, 967-976. doi: 10.1124/mol.106.024513
2. Buckingham, S. D., Jones, A. K., Brown, L. A., and Sattelle, D. B. (2009). Nicotinic acetylcholine receptor signalling: roles in Alzheimer's disease and amyloid neuroprotection. Pharmacol. Rev. 61, 39-61. doi: 10.1124/pr.108.000562
3. Bukanova, J. V., Sharonova, I. N., and Skrebitsky, V. G. (2014). Amyloid β peptide, (25-35) in picomolar concentrations modulates the function of glycine receptors in rat hippocampal pyramidal neurons through interaction with extracellular site(s). Brain Res. 1558, 1-10. doi: 10.1016/j.brainres.2014.02.031
4. Burghaus, L., Schütz, U., Krempel, U., de Vos, R. A., Jansen Steur, E. N., Wevers, A., et al. (2000). Quantitative assessment of nicotinic acetylcholine receptor proteins in the cerebral cortex of Alzheimer patients. Brain Res. Mol. Brain Res. 76, 385-388. doi: 10.1016/s0169-328x(00)00031-0
5. 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. doi: 10.1016/j.neuropharm.2005.09.018
6. Cleary, J. P., Walsh, D. M., Hofmeister, J. J., Shankar, G. M., Kuskowski, M. A., Selkoe, D. J., et al. (2005). Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat. Neurosci. 8, 79-84. doi: 10.1038/nn1372
7. De Felice, F. G., Velasco, P. T., Lambert, M. P., Viola, K., Fernandez, S. J., Ferreira, S. T., et al. (2007). Abeta oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J. Biol. Chem. 282, 11590-11601. doi: 10.1074/jbc.m607483200
8. Dineley, K. T. (2007). Beta-amyloid peptide-nicotinic acetylcholine receptor interaction: the two faces of health and disease. Front. Biosci. 12, 5030-5038. doi: 10.2741/2445
9. Dougherty, J. J., Wu, J., and Nichols, R. A. (2003). Beta-amyloid regulation of presynaptic nicotinic receptors in rat hippocampus and neocortex. J. Neurosci. 23, 6740-6747.
10. Gotti, C., Clementi, F., Fornari, A., Gaimarri, A., Guiducci, S., Manfredi, I., et al. (2009). Structural and functional diversity of native brain neuronal nicotinic receptors. Biochem. Pharmacol. 78, 703-711. doi: 10.1016/j.bcp.2009.05.024
11. Govoni, S., Mura, E., Preda, S., Racchi, M., Lanni, C., Grilli, M., et al. (2014). Dangerous liaisons between beta-amyloid and cholinergic neurotransmission. Curr. Pharm. Des. 20, 2525-2538. doi: 10.2174/13816128113199990503
12. Grilli, M., Lagomarsino, F., Zappettini, S., Mura, E., Preda, S., Govoni, S., et al. (2010). Specific inhibitory effects of β-amyloid on presynaptic muscarinic receptor subtypes modulating neurotransmitter release in the rat nucleus accumbens. Neuroscience 167, 482-489. doi: 10.1016/j.neuroscience.2010.01.058
13. Grilli, M., Patti, L., Robino, F., Zappettini, S., Raiteri, M., and Marchi, M. (2008). Release-enhancing presynaptic muscarinic and nicotinic receptors coexist and interact on dopaminergic nerve endings of rat nucleus accumbens. J. Neurochem. 105, 2205-2213. doi: 10.1111/j.1471-4159.2008.05307.x
14. 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
15. Janíčková, H., Rudajev, V., Zimčík, P., Jakubík, J., Tanila, H., El-Fakahany, E. E., et al. (2013). Uncoupling of M1 muscarinic receptor/G-protein interaction by amyloid β, (1-42). Neuropharmacology 67, 272-283. doi: 10.1016/j.neuropharm.2012.11.014
16. Jürgensen, S., and Ferreira, S. T. (2010). Nicotinic receptors, amyloid-beta and synaptic failure in Alzheimer's disease. J. Mol. Neurosci. 40, 221-229. doi: 10.1007/s12031-009-9237-0
17. Kelly, J. F., Furukawa, K., Barger, S. W., Rengen, M. R., Mark, R. J., Blanc, E. M., et al. (1996). Amyloid beta-peptide disrupts carbachol-induced muscarinic cholinergic signal transduction in cortical neurons. Proc. Natl. Acad. Sci. U S A 93, 6753-6758. doi: 10.1073/pnas.93.13.6753
18. Kennett, A., Heal, D. J., and Wonnacott, S. (2012). Pharmacological differences between rat frontal cortex and hippocampus in the nicotinic modulation of noradrenaline release implicate distinct receptor subtypes. Nicotine Tob. Res. 14, 1339-1345. doi: 10.1093/ntr/nts128
19. Khan, G. M., Tong, M., Jhun, M., Arora, K., and Nichols, R. A. (2010). Beta-Amyloid activates presynaptic alpha7 nicotinic acetylcholine receptors reconstituted into a model nerve cell system: involvement of lipid rafts. Eur. J. Neurosci. 31, 788-796. doi: 10.1111/j.1460-9568.2010.07116.x
20. Kim, J. S., Padnya, A., Weltzin, M., Edmonds, B. W., Schulte, M. K., and Glennon, R. A. (2007). Synthesis of desformylflustrabromine and its evaluation as an alpha4beta2 and alpha7 nACh receptor modulator. Bioorg. Med. Chem. Lett. 17, 4855-4860. doi: 10.1016/j.bmcl.2007.06.047
21. Lesné, S., Koh, M. T., Kotilinek, L., Kayed, R., Glabe, C. G., Yang, A., et al. (2006). A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440, 352-357. doi: 10.1038/nature04533
22. Liu, Q., Kawai, H., and Berg, D. K. (2001). Beta-amyloid peptide blocks the response of alpha 7-containing nicotinic receptors on hippocampal neurons. Proc. Natl. Acad. Sci. U S A 98, 4734-4739. doi: 10.1073/pnas.081553598
23. Lundgren, J. L., Ahmed, S., Winblad, B., Gouras, G. K., Tjernberg, L. O., and Frykman, S. (2014). Activity-independent release of the amyloid β-peptide from rat brain nerve terminals. Neurosci. Lett. 566, 125-130. doi: 10.1016/j.neulet.2014.02.050
24. Mohamed, A., and Posse de Chaves, E. (2011). Aβ internalization by neurons and glia. Int. J. Alzheimers Dis. 2011:127984. doi: 10.4061/2011/127984
25. Mucke, L., and Selkoe, D. J. (2012). Neurotoxicity of amyloid β-protein: synaptic and network dysfunction. Cold Spring Harb. Perspect. Med. 2:a006338. doi: 10.1101/cshperspect.a006338
26. Mura, E., Lanni, C., Preda, S., Pistoia, F., Sarà, M., Racchi, M., et al. (2010a). Beta-amyloid: a disease target or a synaptic regulator affecting age-related neurotransmitter changes? Curr. Pharm. Des. 16, 672-683. doi: 10.2174/138161210790883723
27. Mura, E., Preda, S., Govoni, S., Lanni, C., Trabace, L., Grilli, M., et al. (2010b). Specific neuromodulatory actions of amyloid-beta on dopamine release in rat nucleus accumbens and caudate putamen. J. Alzheimers Dis. 19, 1041-1053. doi: 10.3233/JAD-2010-1299
28. Mura, E., Zappettini, S., Preda, S., Biundo, F., Lanni, C., Grilli, M., et al. (2012). Dual effect of beta-amyloid on α7 and α4β2 nicotinic receptors controlling the release of glutamate, aspartate and GABA in rat hippocampus. PLoS One 7:e29661. doi: 10.1371/journal.pone.0029661
29. Nery, A. A., Magdesian, M. H., Trujillo, C. A., Sathler, L. B., Juliano, M. A., Juliano, L., et al. (2013). Rescue of amyloid-Beta-induced inhibition of nicotinic acetylcholine receptors by a peptide homologous to the nicotine binding domain of the alpha 7 subtype. PLoS One 8:e67194. doi: 10.1371/journal.pone.0067194
30. Oddo, S., Caccamo, A., Smith, I. F., Green, K. N., and LaFerla, F. M. (2006). A dynamic relationship between intracellular and extracellular pools of Abeta. Am. J. Pathol. 168, 184-194. doi: 10.2353/ajpath.2006.050593
31. Olariu, A., Yamada, K., Mamiya, T., Hefco, V., and Nabeshima, T. (2002). Memory impairment induced by chronic intracerebroventricular infusion of beta-amyloid (1-40) involves downregulation of protein kinase C. Brain Res. 957, 278-286. doi: 10.1016/s0006-8993(02)03608-9
32. Pandya, A., and Yakel, J. L. (2011). Allosteric modulator Desformylflustrabromine relieves the inhibition of α2β2 and α4β2 nicotinic acetylcholine receptors by β-amyloid(1-42) peptide. J. Mol. Neurosci. 45, 42-47. doi: 10.1007/s12031-011-9509-3
33. Parihar, M. S., and Brewer, G. J. (2010). Amyloid-β as a modulator of synaptic plasticity. J. Alzheimers Dis. 22, 741-763. doi: 10.3233/JAD-2010-101020
34. Patti, L., Raiteri, L., Grilli, M., Parodi, M., Raiteri, M., and Marchi, M. (2006). P2X7 receptors exert a permissive role on the activation of release-enhancing presynaptic α7 nicotinic receptors coexisting on rat neocortex glutamatergic terminals. Neuropharmacology 50, 705-713. doi: 10.1016/j.neuropharm.2005.11.016
35. Paxinos, G., and Watson, C. (1986). The Rat Brain in Stereotaxic Coordinates. 2nd Edn. New York: Academic Press.
36. Pettit, D. L., Shao, Z., and Yakel, J. L. (2001). Beta-Amyloid (1-42) peptide directly modulates nicotinic receptors in the rat hippocampal slice. J. Neurosci. 21:RC120.
37. Preda, S., Govoni, S., Lanni, C., Racchi, M., Mura, E., Grilli, M., et al. (2008). Acute β-amyloid administration disrupts the cholinergic control of dopamine release in the nucleus accumbens. Neuropsychopharmacology 33, 1062-1070. doi: 10.1038/sj.npp.1301485
38. Puzzo, D., Privitera, L., Leznik, E., Fà, M., Staniszewski, A., Palmeri, A., et al. (2008). Picomolar amyloid-β positively modulates synaptic plasticity and memory in hippocampus. J. Neurosci. 28, 14537-14545. doi: 10.1523/JNEUROSCI.2692-08.2008
39. Pym, L., Kemp, M., Raymond-Delpech, V., Buckingham, S., Boyd, C. A., and Sattelle, D. (2005). Subtype-specific actions of beta-amyloid peptides on recombinant human neuronal nicotinic acetylcholine receptors (alpha7, alpha4beta2, alpha3beta4) expressed in Xenopus laevis oocytes. Br. J. Pharmacol. 146, 964-971. doi: 10.1038/sj.bjp.0706403
40. Raiteri, M., Sala, R., Fassio, A., Rossetto, O., and Bonanno, G. (2000). Entrapping of impermeant probes of different size into nonpermeabilized synaptosomes as a method to study presynaptic mechanisms. J. Neurochem. 74, 423-431. doi: 10.1046/j.1471-4159.2000.0740423.x
41. Risso, F., Grilli, M., Parodi, M., Bado, M., Raiteri, M., and Marchi, M. (2004). Nicotine exerts a permissive role on NMDA receptor function in hippocampal noradrenergic terminals. Neuropharmacology 47, 65-71. doi: 10.1016/s0028-3908(04)00055-3
42. Samochocki, M., Höffle, A., Fehrenbacher, A., Jostock, R., Ludwig, J., Christner, C., et al. (2003). Galantamine is an allosterically potentiating ligand of neuronal nicotinic but not of muscarinic acetylcholine receptors. J. Pharmacol. Exp. Ther. 305, 1024-1036. doi: 10.1124/jpet.102.045773
43. Small, D. H., Maksel, D., Kerr, M. L., Ng, J., Hou, X., Chu, C., et al. (2007). The beta-amyloid protein of Alzheimer's disease binds to membrane lipids but does not bind to the alpha7 nicotinic acetylcholine receptor. J. Neurochem. 101, 1527-1538. doi: 10.1111/j.1471-4159.2006.04444.x
44. Spires-Jones, T. L., and Hyman, B. T. (2014). The intersection of amyloid beta and tau at synapses in Alzheimer's disease. Neuron 82, 756-771. doi: 10.1016/j.neuron.2014.05.004
45. Tong, M., Arora, K., White, M. M., and Nichols, R. A. (2011). Role of key aromatic residues in the ligand-binding domain of alpha7 nicotinic receptors in the agonist action of beta-amyloid. J. Biol. Chem. 286, 34373-34381. doi: 10.1074/jbc.M111.241299
46. Walsh, D. M., Tseng, B. P., Rydel, R. E., Podlisny, M. B., and Selkoe, D. J. (2000). The oligomerization of amyloid beta-protein begins intracellularly in cells derived from human brain. Biochemistry 39, 10831-10839. doi: 10.1021/bi001048s
47. Wang, H. Y., Lee, D. H., D'Andrea, M. R., Peterson, P. A., Shank, R. P., and Reitz, A. B. (2000). Beta-Amyloid (1-42) binds to alpha7 nicotinic acetylcholine receptor with high affinity. Implications for Alzheimer's disease pathology. J. Biol. Chem. 275, 5626-5632. doi: 10.1074/jbc.275.8.5626
48. Weltzin, M. M., and Schulte, M. K. (2010). Pharmacological characterization of the allosteric modulator desformylflustrabromine and its interaction with alpha4beta2 neuronal nicotinic acetylcholine receptor orthosteric ligands. J. Pharmacol. Exp. Ther. 334, 917-926. doi: 10.1124/jpet.110.167684
49. Williams, D. K., Wang, J., and Papke, R. L. (2011). Positive allosteric modulators as an approach to nicotinic acetylcholine receptor-targeted therapeutics: advantages and limitations. Biochem. Pharmacol. 82, 915-930. doi: 10.1016/j.bcp.2011.05.001
50. Wonnacott, S. (1997). Presynaptic nicotinic ACh receptors. Trends Neurosci. 20, 92-98. doi: 10.1016/s0166-2236(96)10073-4
51. Zappettini, S., Grilli, M., Olivero, G., Mura, E., Preda, S., Govoni, S., et al. (2012). Beta amyloid differently modulate nicotinic and muscarinic receptor subtypes which stimulate in vitro and in vivo the release of glycine in the rat hippocampus. Front. Pharmacol. 3:146. doi: 10.3389/fphar.2012.00146
52. Zaveri, N., Jiang, F., Olsen, C., Polgar, W., and Toll, L. (2010). Novel α3β4 nicotinic acetylcholine receptor-selective ligands. Discovery, structure-activity studies and pharmacological evaluation. J. Med. Chem. 53, 8187-8191. doi: 10.1021/jm1006148
53. Zhong, P., Gu, Z., Wang, X., Jiang, H., Feng, J., and Yan, Z. (2003). Impaired modulation of GABAergic transmission by muscarinic receptors in a mouse transgenic model of Alzheimer's disease. J. Biol. Chem. 278, 26888-26896. doi: 10.1074/jbc.m302789200