Dual effect of beta-amyloid on α7 and α4β2 nicotinic receptors controlling the release of glutamate, aspartate and GABA in rat hippocampus

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Mura, Elisa ^a   Zappettini, Stefania ^b   Preda, Stefania ^a   Biundo, Fabrizio ^a   Lanni, Cristina ^a   Grilli, Massimo ^b   Cavallero, Anna ^b   Olivero, Guendalina ^b   Salamone, Alessia ^b   Govoni, Stefano ^a   Marchi, Mario ^b  

^a UNIVERSITY OF PAVIA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; AMYLOID BETA PROTEIN[1-40]; ASPARTIC ACID; BUNGAROTOXIN RECEPTOR; CHOLINE; GLUTAMIC ACID; NICOTINE; NICOTINIC RECEPTOR ALPHA4BETA2; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; AMYLOID BETA PROTEIN; NICOTINIC AGENT; NICOTINIC RECEPTOR; POTASSIUM; VERATRIDINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONCENTRATION RESPONSE; CONTROLLED STUDY; EVOKED RESPONSE; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; LEARNING; MALE; MEMORY; MICRODIALYSIS; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; PROTEIN FUNCTION; RAT; STIMULUS RESPONSE; ANIMAL; CYTOLOGY; DRUG EFFECT; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; SECRETION; TIME; WISTAR RAT;

RATTUS;

AMYLOID BETA-PEPTIDES; ANIMALS; ASPARTIC ACID; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; HIPPOCAMPUS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEUROTRANSMITTER AGENTS; NICOTINE; NICOTINIC AGONISTS; POTASSIUM; RATS; RATS, WISTAR; RECEPTORS, NICOTINIC; TIME FACTORS; VERATRIDINE;

EID: 84855675656     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029661     Document Type: Article

References (57)

1. Glenner GG, Wong CW, (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem Biophys Res Commun 120: 885-90.
2. Hardy JA, Higgins GA, (1992) Alzheimer's disease: the amyloid cascade hypothesis. Science 256: 184-5.
3. Hardy J, (2006) Alzheimer's disease: the amyloid cascade hypothesis: an update and reappraisal. J Alzheimers Dis 9: 151-3.
4. Mura E, Lanni C, Preda S, Pistoia F, Sarà M, et al. (2010a) Beta-amyloid: a disease target or a synaptic regulator affecting age-related neurotransmitter changes? Curr Pharm Des 16: 672-83.
5. Preda S, Govoni S, Lanni C, Racchi M, Mura E, et al. (2008) Acute beta-amyloid administration disrupts the cholinergic control of dopamine release in the nucleus accumbens. Neuropsychopharmacology 33: 1062-70.
6. Mura E, Preda S, Govoni S, Lanni C, Trabace L, et al. (2010b) Specific neuromodulatory actions of amyloid-beta on dopamine release in rat nucleus accumbens and caudate putamen. J Alzheimers Dis 19: 1041-53.
7. Grilli M, Lagomarsino F, Zappettini S, Preda S, Mura E, et al. (2010) Specific inhibitory effect of amyloid-beta on presynaptic muscarinic receptor subtypes modulating neurotransmitter release in the rat nucleus accumbens. Neuroscience 167: 482-9.
8. Wang HY, Lee DH, Davis CB, Shank RP, (2000) Amyloid peptide Abeta(1-42) binds selectively and with picomolar affinity to alpha7 nicotinic acetylcholine receptors. J Neurochem 75: 1155-61.
9. Buckingham SD, Jones AK, Brown LA, Sattelle DB, (2009) Nicotinic acetylcholine receptor signalling: roles in Alzheimer's disease and amyloid neuroprotection. Pharmacol Rev 61: 39-61.
10. Jürgensen S, Ferreira ST, (2010) Nicotinic receptors, amyloid-beta, and synaptic failure in Alzheimer's Disease. J Mol Neurosci 40: 221-229.
11. Parri RH, Dineley TK, (2010) Nicotinic acetylcholine receptor interaction with beta-amyloid: molecular, cellular, and physiological consequences. Curr Alzheimer Res 7: 27-39.
12. Thal DR, Griffin WS, Braak H, (2008) Parenchymal and vascular Abeta-deposition and its effects on the degeneration of neurons and cognition in Alzheimer's disease. J Cell Mol Med 12: 1848-62.
13. Alonso JR, Amaral DG, (1995) Cholinergic innervation of the primate hippocampal formation. Distribution of choline acetyltransferase immunoreactivity in the Macaca fascicularis and Macaca mulatta monkeys. J Comp Neurol 355: 135-70.
14. Yoshida K, Oka H, (1995) Topographical projections from the medial septum-diagonal band complex to the hippocampus: a retrograde tracing study with multiple fluorescent dyes in rats. Neurosci Res 21: 199-209.
15. Hefft S, Hulo S, Bertrand D, Muller D, (1999) Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol 515: 769-76.
16. Descarries L, Gisiger V, Steriade M, (1997) Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53: 603-25.
17. Zappettini S, Grilli M, Salamone A, Fedele E, 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: 1161-71.
18. Zappettini S, Grilli M, Lagomarsino F, Cavallero A, Fedele E, et al. (2011) Presynaptic nicotinic α7 and non-α7 receptors stimulate endogenous GABA release from rat hippocampal synaptosomes through two mechanisms of action. PLoS One 6: e16911.
19. Ji D, Lape R, Dani JA, (2001) Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31: 131-41.
20. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, et al. (2003) APP processing and synaptic function. Neuron 37: 925-37.
21. Terai K, Iwai A, Kawabata S, Tasaki Y, Watanabe T, et al. (2001) beta-amyloid deposits in transgenic mice expressing human beta-amyloid precursor protein have the same characteristics as those in Alzheimer's disease. Neuroscience 104: 299-310.
22. Walsh DM, Selkoe DJ, (2007) A beta oligomers- a decade of discovery. J Neurochem 101: 1172-84.
23. Bitan G, Kirkitadze MD, Lomakin A, Vollers SS, Benedek GB, et al. (2003) Amyloid beta-protein (Abeta) assembly: Abeta 40 and Abeta 42 oligomerize through distinct pathways. Proc Natl Acad Sci U S A 100: 330-5.
24. Verdile G, Fuller S, Atwood CS, Laws SM, Gandy SE, et al. (2004) The role of beta amyloid in Alzheimer's disease: still a cause of everything or the only one who got caught? Pharmacol Res 50: 397-409.
25. Fedele E, Varnier G, Ansaldo MA, Raiteri M, (1998) Nicotine administration stimulates the in vivo N-methyl-D-aspartate receptor/nitric oxide/cyclic GMP pathway in rat hippocampus through glutamate release. Br J Pharmacol 125: 1042-8.
26. Toth E, (1996) Effect of nicotine on the level of extracellular amino acids in the hippocampus of rat. Neurochem Res 21: 903-7.
27. Benowitz NL, Porchet H, Jacob PI, (1990) Pharmacokinetics, metabolism, and pharmacodynamics of nicotine. In: Wonnacott S, Russell MAH, Stolerman IP, editors. Nicotine Psychopharmacology: Molecular, Cellular, and Behavioural Aspects Oxford, England Oxford University Press pp. 112-157.
28. Battaglia G, Monn JA, Schoepp DD, (1997) In vivo inhibition of veratridine-evoked release of striatal excitatory amino acids by the group II metabotropic glutamate receptor agonist LY354740 in rats. Neurosci Lett 229: 161-4.
29. Ahmad S, Fowler LJ, Whitton PS, (2004) Effects of acute and chronic lamotrigine treatment on basal and stimulated extracellular amino acids in the hippocampus of freely moving rats. Brain Res 1029: 41-7.
30. Raiteri L, Raiteri M, (2000) Synaptosomes still viable after 25 years of superfusion. Neurochem Res 25: 1265-1274.
31. Suzuki N, Cheung TT, Cai XD, Odaka A, Otvos L Jr, et al. (1994) An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta APP717) mutants. Science 264: 1336-40.
32. Kirkitadze MD, Kowalska A, (2005) Molecular mechanisms initiating amyloid β-fibril formation in Alzheimer's disease. Acta Biochim Pol 52: 417-423.
33. Sabella S, Quaglia M, Lanni C, Racchi M, Govoni S, et al. (2004) Capillary electrophoresis studies on the aggregation process of beta-amyloid 1-42 and 1-40 peptides. Electrophoresis 25: 3186-94.
34. Wu M, Hajszan T, Leranth C, Alreja M, (2003) Nicotine recruits a local glutamatergic circuit to excite septohippocampal GABAergic neurons. European Journal of Neuroscience 18: 1155-1168.
35. Lee DH, Wang HY, (2003) Differential physiologic responses of alpha7 nicotinic acetylcholine receptors to beta-amyloid1-40 and beta-amyloid1-42. J Neurobiol 55: 25-30.
36. Kar S, Seto D, Gaudreau P, Quirion R, (1996) Beta-amyloid-related peptides inhibit potassium-evoked acetylcholine release from rat hippocampal slices. J Neurosci 16: 1034-40.
37. Wang SY, Wang GK, (2003) Voltage-gated sodium channels as primary targets of diverse lipid-soluble neurotoxins. Cell Signal 15: 151-9.
38. Fekete A, Franklin L, Ikemoto T, Rózsa B, Lendvai B, et al. (2009) Mechanism of the persistent sodium current activator veratridine-evoked Ca elevation: implication for epilepsy. J Neurochem 111: 745-56.
39. Luccini E, Romei C, Di Prisco S, Raiteri M, Raiteri L, (2010) Ionic dysregulations typical of ischemia provoke release of glycine and GABA by multiple mechanisms. J Neurochem 114: 1074-84.
40. Dickinson JA, Kew JN, 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: 348-59.
41. Ida N, Hartmann T, Pantel J, Schröder J, Zerfass R, et al. (1996) Analysis of heterogeneous A4 peptides in human cerebrospinal fluid and blood by a newly developed sensitive Western blot assay. J Biol Chem 271: 22908-14.
42. Brody DL, Magnoni S, Schwetye KE, Spinner ML, Esparza TJ, et al. (2008) Amyloid-beta dynamics correlate with neurological status in the injured human brain. Science 321: 1221-4.
43. Dineley KT, Bell KA, Bui D, Sweatt JD, (2002) Beta-Amyloid peptide activates alpha 7 nicotinic acetylcholine receptors expressed in Xenopus oocytes. J Biol Chem 277: 25056-61.
44. Puzzo D, Privitera L, Leznik E, Fà M, Staniszewski A, et al. (2008) Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus. J Neurosci 28: 14537-45.
45. Puzzo D, Privitera L, Fa' M, Staniszewski A, Hashimoto G, et al. (2011) Endogenous amyloid-β is necessary for hippocampal synaptic plasticity and memory. Ann Neurol 69: 819-30.
46. Magdesian MH, Nery AA, Martins AH, Juliano MA, Juliano L, et al. (2005) Peptide blockers of the inhibition of neuronal nicotinic acetylcholine receptors by amyloid beta. J Biol Chem 280: 31085-90.
47. Small DH, Maksel D, Kerr ML, Ng J, Hou X, et al. (2007) The β-amyloid protein of Alzheimer's disease binds to membrane lipids but does not bind to the α7 nicotinic acetylcholine receptor. Journal of Neurochemistry 101: 1527-1538.
48. Saavedra L, Mohamed A, Ma V, Kar S, de Chaves EP, (2007) Internalization of beta-amyloid peptide by primary neurons in the absence of apolipoprotein E. J Biol Chem 282: 35722-32.
49. Mehta TK, Dougherty JJ, Wu J, Choi CH, Khan GM, et al. (2009) Defining pre-synaptic nicotinic receptors regulated by beta amyloid in mouse cortex and hippocampus with receptor null mutants. J Neurochem 109: 1452-8.
50. Dougherty JJ, Wu J, Nichols RA, (2003) Beta-amyloid regulation of presynaptic nicotinic receptors in rat hippocampus and neocortex. J Neurosci 23: 6740-7.
51. Boyd-Kimball D, Castegna A, Sultana R, Poon HF, Petroze R, et al. (2005) Proteomic identification of proteins oxidized by Abeta(1-42) in synaptosomes: implications for Alzheimer's disease. Brain Res 1044: 206-15.
52. Verderio C, Grumelli C, Raiteri L, Coco S, Paluzzi S, et al. (2007) Traffic of botulinum toxins A and E in excitatory and inhibitory neurons. Traffic 8: 142-53.
53. Stitzel JA, Blanchette JM, Collins AC, (1998) Sensitivity to the seizure-inducing effects of nicotine is associated with strain-specific variants of the alpha 5 and alpha 7 nicotinic receptor subunit genes. J Pharmacol Exp Ther 284: 1104-11.
54. Paxinos G, Watson C, (1986) The Rat Brain in Stereotaxic coordinates Second Edition, New York Academic Press.
55. Di Chiara G, (1990) In-vivo brain dialysis of neurotransmitters. Trends Pharmacol Sci 11: 116-121.
56. Dunkley PR, Jarvie PE, Heath JW, Kidd GJ, Rostas JA, (1986) A rapid method for isolation of synaptosomes on Percoll gradients. Brain Res 372: 115-29.
57. Lu Y, Grady S, Marks MJ, Picciotto M, Changeux J-P, et al. (1998) Pharmacological characterization of nicotinic receptor-stimulated GABA release from mouse brain synaptosomes. J Pharmacol Exp Ther 287: 648-657.