Hormetic effect of amyloid-beta peptide in synaptic plasticity and memory

Neurobiology of Aging

Volumn 33, Issue 7, 2012, Pages 1484.e15-1484.e24

  Puzzo, Daniela ^a   Privitera, Lucia ^a   Palmeri, Agostino ^a  

^a UNIVERSITY OF CATANIA   (Italy)

Author keywords

Alzheimer's disease; Amyloid beta; Hippocampus; Hormesis; Low doses; Memory; Synaptic plasticity

Indexed keywords

AMYLOID BETA PROTEIN[1-42];

ANIMAL EXPERIMENT; ARTICLE; COGNITION; CONCENTRATION RESPONSE; CONTROLLED STUDY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; HORMESIS; LONG TERM POTENTIATION; MAZE TEST; MEMORY; MORRIS WATER MAZE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REFERENCE MEMORY; SPATIAL MEMORY;

EID: 84861198956     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2011.12.020     Document Type: Article

References (73)

1. Albuquerque E.X., Pereira E.F., Alkondon M., Rogers S.W. Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol. Rev 2009, 89:73-120.
2. Beach T.G., Walker D.G., Potter P.E., Sue L.I., Fisher A. Reduction of cerebrospinal fluid amyloid beta after systemic administration of M1 muscarinic agonists. Brain Res 2001, 905:220-223.
3. Blennow K. Cerebrospinal fluid protein biomarkers for Alzheimer's disease. Neurorx 2004, 1:213-225.
4. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
5. Brody D.L., Magnoni S., Schwetye K.E., Spinner M.L., Esparza T.J., Stocchetti N., Zipfel G.J., Holtzman D.M. Amyloid-beta dynamics correlate with neurological status in the injured human brain. Science 2008, 321:1221-1224.
6. Caccamo A., Oddo S., Billings L.M., Green K.N., Martinez-Coria H., Fisher A., LaFerla F.M. M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron 2006, 49:671-682.
7. Calabrese E.J. Amyloid β-Peptide: Biphasic Dose Responses. Crit. Rev. Toxicol 2001, 31:605-606.
8. Calabrese E.J. Nitric Oxide: Biphasic Dose Responses. Crit. Rev. Toxicol 2001, 31:489-501.
9. Calabrese E.J. Hormesis and medicine. Br. J. Clin. Pharmacol 2008, 66:594-617.
10. Calabrese E.J. Neuroscience and hormesis: overview and general findings. Crit. Rev. Toxicol 2008, 38:249-252.
11. Calabrese E.J. Getting the dose-response wrong: why hormesis became marginalized and the threshold model accepted. Arch. Toxicol 2009, 83:227-247.
12. Calabrese E.J. Hormesis is central to toxicology, pharmacology and risk assessment. Hum. Exp. Toxicol 2010, 29:249-261.
13. Calabrese E.J., Baldwin L.A. A general classification of U-shaped dose-response relationships in toxicology and their mechanistic foundations. Hum. Exp. Toxic 1998, 17:353-364.
14. Calabrese E.J., Baldwin L.A. U-shaped dose-responses in biology, toxicology, and public health. Annu. Rev. Public Health 2001, 22:15-33.
15. Calabrese E.J., Baldwin L.A. Defining hormesis. Hum. Exp. Toxicol 2002, 21:91-97.
16. Calabrese E.J., Baldwin L.A. Hormesis: the dose-response devolution. Annu. Rev. Pharmacol. Toxicol 2003, 43:175-197.
17. Calabrese E.J., Baldwin L.A. Peptides and Hormesis. Crit. Rev. Toxicol 2003, 33:355-405.
18. Calabrese E.J., Baldwin L.A., Holland C.D. Hormesis: a highly generalizable and reproducible phenomenon with important implications for risk assessment. Risk Anal 1999, 19:261-281.
19. Choi D.W. Glutamate neurotoxicity and diseases of the nervous system. Neuron 1988, 1:623-634.
20. Chow V.W., Mattson M.P., Wong P.C., Gleichmann M. An Overview of APP Processing Enzymes and Products. Neuromol. Med 2010, 12:1-12.
21. Cirrito J.R., Kang J.E., Lee J., Stewart F.R., Verges D.K., Silverio L.M., Bu G., Mennerick S., Holtzman D.M. Endocytosis is required for synaptic activity-dependent release of amyloid-beta in vivo. Neuron 2008, 58:42-51.
22. Clader J.W., Wang Y. Muscarinic receptor agonists and antagonists in the treatment of Alzheimer's disease. Curr. Pharm. Des 2005, 11:3353-3361.
23. Cummings J. What can be inferred from the interruption of the semagacestat trial for treatment of Alzheimer's disease?. Biol. Psych 2010, 68:876-878.
24. Dawson G.R., Seabrook G.R., Zheng H., Smith D.W., Graham S., O'Dowd G., Bowery B.J., Boyce S., Trumbauer M.E., Chen H.Y., Van der Ploeg L.H., Sirinathsinghji D.J. Age-related cognitive deficits, impaired long-term potentiation and reduction in synaptic marker density in mice lacking the beta-amyloid precursor protein. Neuroscience 1999, 90:1-13.
25. Dineley K.T., Bell K.A., Bui D., Sweatt J.D. Beta-amyloid peptide activates alpha 7 nicotinic acetylcholine receptors expressed in Xenopus oocytes. J. Biol. Chem 2002, 277:25056-25061.
26. Dineley K.T., Westerman M., Bui D., Bell K., Ashe K.H., Sweatt J.D. Beta-amyloid activates the mitogen-activated protein kinase cascade via hippocampal alpha7 nicotinic acetylcholine receptors: In vitro and in vivo mechanisms related to Alzheimer's disease. J. Neurosci 2001, 21:4125-4133.
27. Dominguez D.I., De Strooper B. Novel therapeutic strategies provide the real test for the amyloid hypothesis of Alzheimer's disease. Trends Pharmacol. Sci 2002, 23:324-330.
28. Duncan A.J., Heales S.J. Nitric oxide and neurological disorders. Mol. Aspects Med 2005, 26:67-96.
29. Fehér A., Juhász A., Rimanóczy A., Csibri E., Kálmán J., Janka Z. Association between a genetic variant of the alpha-7 nicotinic acetylcholine receptor subunit and four types of dementia. Dement. Geriatr. Cogn. Disord 2009, 28:56-62.
30. Fodero L.R., Mok S.S., Losic D., Martin L.L., Aguilar M.I., Barrow C.J., Livett B.G., Small D.H. Alpha7-nicotinic acetylcholine receptors mediate an Abeta(1-42)-induced increase in the level of acetylcholinesterase in primary cortical neurones. J. Neurochem 2004, 88:1186-1193.
31. Giuffrida M.L., Caraci F., De Bona P., Pappalardo G., Nicoletti F., Rizzarelli E., Copani A. The monomer state of beta-amyloid: where the Alzheimer's disease protein meets physiology. Rev. Neurosci 2010, 21:83-93.
32. Grassi F., Palma E., Tonini R., Amici M., Ballivet M., Eusebi F. Amyloid beta(1-42) peptide alters the gating of human and mouse alpha-bungarotoxin-sensitive nicotinic receptors. J. Physiol 2003, 547:147-157.
33. Gray R., Rajan A.S., Radcliffe K.A., Yakehiro M., Dani J.A. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 1996, 383:713-716.
34. Hardy J., Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 2002, 297:353-356.
35. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., Malinow R. APP processing and synaptic function. Neuron 2003, 37:925-937.
36. Kastin A.J., Pan W. Peptides and Hormesis. Crit. Rev. Toxicol 2008, 38:629-631.
37. Kendig E.L., Le H.H., Belcher S.M. Defining hormesis: evaluation of a complex concentration response phenomenon. Int. J. Toxicol 2010, 29:235-246.
38. Laird F.M., Cai H., Savonenko A.V., Farah M.H., He K., Melnikova T., Wen H., Chiang H.C., Xu G., Koliatsos V.E., Borchelt D.R., Price D.L., Lee H.K., Wong P.C. BACE1, a major determinant of selective vulnerability of the brain to amyloid-beta amyloidogenesis, is essential for cognitive, emotional, and synaptic functions. J. Neurosci 2005, 25:11693-11709.
39. Levey A.I. Muscarinic acetylcholine receptor expression in memory circuits: implications for treatment of Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A 1996, 93:13541-13546.
40. Levin E.D. Nicotinic receptor subtypes and cognitive function. J. Neurobiol 2002, 53:633-640.
41. Lewczuk P., Beck G., Esselmann H., Bruckmoser R., Zimmermann R., Fiszer M., Bibl M., Maler J.M., Kornhuber J., Wiltfang J. Effect of sample col- lection tubes on cerebrospinal fluid concentrations of tau proteins and amyloid beta peptides. Clin. Chem 2006, 52:332-334.
42. López-Toledano M.A., Shelanski M.L. Neurogenic effect of β-amyloid peptide in the development of neural stem cells. J. Neurosci 2004, 24:5439-5444.
43. Lowenstein C.J., Dinerman J.L., Snyder S.H. Nitric oxide: a physiologic messenger. Ann. Intern. Med 1994, 120:227-237.
44. Lupien S.J., Buss C., Schramek T.E., Maheu F., Pruessner J. Hormetic Influence of Glucocorticoids on Human Memory. Nonlinearity Biol. Toxicol. Med 2005, 3:23-56.
45. Ma H., Lesné S., Kotilinek L., Steidl-Nichols J.V., Sherman M., Younkin L., Younkin S., Forster C., Sergeant N., Delacourte A., Vassar R., Citron M., Kofuji P., Boland L.M., Ashe K.H. Involvement of beta-site APP cleaving enzyme 1 (BACE1) in amyloid precursor protein-mediated enhancement of memory and activity-dependent synaptic plasticity. Proc. Natl. Acad. Sci. U. S. A 2007, 104:8167-8172.
46. Mattson M.P. Cellular actions of beta-amyloid precursor protein and its soluble and fibrillogenic derivatives. Physiol. Rev 1997, 77:1081-1132.
47. Mattson M.P. Pathways towards and away from Alzheimer's disease. Nature 2004, 430:631-639.
48. Mattson M.P. Glutamate and neurotrophic factors in neuronal plasticity and disease. Ann. N. Y. Acad. Sci 2008, 1144:97-112.
49. Mattson M.P. Hormesis and disease resistance: activation of cellular stress response pathways. Hum. Exp. Toxicol 2008, 27:155-162.
50. Medeiros R., Kitazawa M., Caccamo A., Baglietto-Vargas D., Estrada-Hernandez T., Cribbs D.H., Fisher A., LaFerla F.M. Loss of muscarinic M1 receptor exacerbates Alzheimer's disease-like pathology and cognitive decline. Am. J. Pathol 2011, 179:980-991.
51. Oddo S., LaFerla F.M. The role of nicotinic acetylcholine receptors in Alzheimer's disease. J. Physiol. Paris 2006, 99:172-179.
52. Ondrejcak T., Klyubin I., Hu N.W., Barry A.E., Cullen W.K., Rowan M.J. Alzheimer's disease amyloid β-protein and synaptic function. Neuromol. Med 2010, 12:13-26.
53. Paxinos G. Mouse Brain in Stereotaxic Coordinates 1998, Academic, New York. second ed.
54. Phinney A.L., Calhoun M.E., Wolfer D.P., Lipp H.P., Zheng H., Jucker M. No hippocampal neuron or synaptic bouton loss in learning-impaired aged beta-amyloid precursor protein-null mice. Neuroscience 1999, 90:1207-1216.
55. Plant L.D., Boyle J.P., Smith I.F., Peers C., Pearson H.A. The production of amyloid beta peptide is a critical requirement for the viability of central neurons. J. Neurosci 2003, 23:5531-5535.
56. Puzzo D., Palmeri A., Arancio O. Involvement of the nitric oxide pathway in synaptic dysfunction following amyloid elevation in Alzheimer's disease. Rev. Neurosci 2006, 17:497-523.
57. Puzzo D., Privitera L., Fa' M., Staniszewski A., Hashimoto G., Aziz F., Sakurai M., Ribe E.M., Troy C.M., Mercken M., Jung S.S., Palmeri A., Arancio O. Endogenous amyloid-β is necessary for hippocampal synaptic plasticity and memory. Ann. Neurol 2011, 69:819-830.
58. Puzzo D., Privitera L., Leznik E., Fà M., Staniszewski A., Palmeri A., Arancio O. Picomolar amyloid-beta positively modulates synaptic plasticity and memory in hippocampus. J. Neurosci 2008, 28:14537-14545.
59. Radcliffe K.A., Dani J.A. Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J. Neurosci 1998, 18:7075-7083.
60. Randall A.D., Witton J., Booth C., Hynes-Allen A., Brown J.T. The functional neurophysiology of the amyloid precursor protein (APP) processing pathway. Neuropharmacology 2010, 59:243-267.
61. Rezvani A.H. Involvement of the NMDA system in learning and memory. Animal Models of Cognitive Impairment 2006, 37-48. CRC Press, Boca Raton, Section I, Chapter 4. E.D. Levin, J.J. Buccafusco (Eds.).
62. Saura C.A., Choi S.Y., Beglopoulos V., Malkani S., Zhang D., Shankaranarayana Rao B.S., Chattarji S., Kelleher R.J., Kandel E.R., Duff K., Kirkwood A., Shen J. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 2004, 42:23-36.
63. Schenk F., Morris R.G. Dissociation between components of spatial memory in rats after recovery from the effects of retrohippocampal lesions. Exp. Brain Res 1985, 58:11-28.
64. Seabrook G.R., Smith D.W., Bowery B.J., Easter A., Reynolds T., Fitzjohn S.M., Morton R.A., Zheng H., Dawson G.R., Sirinathsinghji D.J., Davies C.H., Collingridge G.L., Hill R.G. Mechanisms contributing to the deficits in hippocampal synaptic plasticity in mice lacking amyloid precursor protein. Neuropharmacology 1999, 38:349-359.
65. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
66. Seo H., Ferree A.W., Isacson O. Cortico-hippocampal APP and NGF levels are dynamically altered by cholinergic muscarinic antagonist or M1 agonist treatment in normal mice. Eur. J. Neurosci 2002, 15:498-506.
67. Small D.H., Maksel D., Kerr M.L., Ng J., Hou X., Chu C., Mehrani H., Unabia S., Azari M.F., Loiacono R., Aguilar M.I., Chebib M. The beta-amyloid protein of Alzheimer's disease binds to membrane lipids but does not bind to the alpha7 nicotinic acetylcholine receptor. J. Neurochem 2007, 101:1527-1538.
68. Trinchese F., Liu S., Battaglia F., Walter S., Mathews P.M., Arancio O. Progressive age-related development of Alzheimer-like pathology in APP/PS1 mice. Ann. Neurol 2004, 55:801-814.
69. Wang H., Song L., Laird F., Wong P.C., Lee H.K. BACE1 knock-outs display deficits in activity-dependent potentiation of synaptic transmission at mossy fiber to CA3 synapses in the hippocampus. J. Neurosci 2008, 28:8677-8681.
70. Wang H.Y., Lee D.H., D'Andrea M.R., Peterson P.A., Shank R.P., Reitz A.B. Beta-amyloid(1-42) binds to alpha7 nicotinic acetylcholine receptor with high affinity. Implications for Alzheimer's disease pathology. J. Biol. Chem 2000, 275:5626-5632.
71. Wieloch T. Hypoglycemia-induced neuronal damage prevented by an N-methyl-d-aspartate antagonist. Science 1985, 230:681-683.
72. Williams J.H., Wilcock G.K., Seeburger J., Dallob A., Laterza O., Potter W., Smith A.D. Non-linear relationships of cerebrospinal fluid biomarker levels with cognitive function: an observational study. Alz. Res. Ther 2011, 3:5.
73. Yankner B.A., Duffy L.K., Kirschner D.A. Neurotrophic and neurotoxic effects of amyloid beta protein: reversal by tachykinin neuropeptides. Science 1990, 250:279-282.