β-amyloid(Phe(SO3H)24)25-35 in rat nucleus basalis induces behavioral dysfunctions, impairs learning and memory and disrupts cortical cholinergic innervation

Behavioural Brain Research

Volumn 90, Issue 2, 1998, Pages 133-145

  Harkany, T ^a,b   O'Mahony, S ^c   Kelly, J P ^c   Soos K ^d   Toro I ^d   Penke, B ^d   Luiten, P G M ^e   Nyakas, C ^a   Gulya, K ^b   Leonard, B E ^c  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b UNIVERSITY OF SZEGED   (Hungary)

^c NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^d UNIVERSITY OF SZEGED   (Hungary)

^e UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

amyloid neurotoxicity; Acetylcholinesterase; Behavior; Cholinergic system; Learning and memory; Parietal cortex

Indexed keywords

ACETYLCHOLINESTERASE; AMYLOID BETA PROTEIN;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CHOLINERGIC NERVE; CONTROLLED STUDY; HISTOCHEMISTRY; LEARNING DISORDER; MAGNOCELLULAR NUCLEUS; MAZE TEST; MEMORY; METABOLISM; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; OLIVARY NUCLEUS; PARASYMPATHETIC INNERVATION; PARIETAL LOBE; PRIORITY JOURNAL; RAT; SOLUBILITY;

ACETYLCHOLINESTERASE; AMYLOID BETA-PROTEIN; ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; CEREBRAL CORTEX; ELECTROSHOCK; HISTOCYTOCHEMISTRY; LEARNING DISORDERS; MALE; MAZE LEARNING; MEMORY DISORDERS; MOTOR ACTIVITY; NEUROPEPTIDES; NEUROTOXINS; PARASYMPATHETIC NERVOUS SYSTEM; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 0031890373     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(97)00091-0     Document Type: Article

References (48)

1. Abe E., Casamenti F., Giovannelli L., Scali C., Pepeu G. Administration of amyloid β-peptides into the medial septum of rats decreases acetylcholine release from hippocampus in vivo. Brain Res. 636:1994;162-164.
2. Barrow C.J., Zagorski M.G. Solution structures of β-peptide and its constituent fragments: relation to amyloid deposition. Science. 253:1991;179-182.
3. Bartus R.T., Dean III R.L., Beer B., Lippa S. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217:1982;408-414.
4. G-Nitro-L-arginine protects against ischemia-induced increases in nitric oxide and hippocampal neuro-degeneration in the gerbil. Eur. J. Pharmacol. 260:1994;191-200.
5. Chiba A.A., Bucci D.J., Holland P.C., Gallagher M. Basal forebrain cholinergic lesions disrupt increments but not decrements in conditioned stimulus processing. J. Neurosci. 15:1995;7315-7322.
6. G.I. De Jong, E.A. Proper, J. Korf, T. Harkany, P.G.M. Luiten, Short-term in vivo neurotoxicity of β-amyloid fragments (25-35 and 1-40) in rat nucleus basalis and influence of pH, submitted.
7. Emre M., Genla C., Ransil B.J., Mesulam M.M. The acute neurotoxicity and effects upon cholinergic axons of intracerebrally injected β-amyloid in the rat brain. Neurobiol. Aging. 13:1992;553-559.
8. Estus S., Golde T.E., Kunishita T., Blades D., Lowery D., Eisen M., Usiak M., Qu X., Tabira T., Greenberg B.D., Younkin S.G. Potentially amyloidogenic carboxyl-terminal derivatives of the amyloid precursor protein. Science. 255:1992;726-728.
9. Flood J.F., Morley J.E., Roberts E. An amyloid β-protein fragment, Aβ[12-28] equipotently impairs post-training memory processing when injected into different limbic structures. Brain Res. 663:1994;271-2766.
10. Games D., Adams D., Alessandrini R., Barbour R., Berthelette P., Blackwell C., Carr T., Clemens J., Donaldson T., Gillespie F., Guido T., Hagopian S., Johnson-Wood K., Khan K., Lee M., Leibowitz P., Lieberburg I., Little S., Masliah E., McConlogue L., Montoya-Zavala M., Mucke L., Paganini L., Penniman E., Power M., Schenk D., Seubert P., Snyder B., Soriano F., Tan H., Vitale J., Wadsworth S., Wolozin B., Zhao J. Alzheimer-type neuropathology in transgenic mice overexpressing V717F β-amyloid precursor protein. Nature. 373:1995;523-527.
11. Gaykema R.P.A., Nyakas C., Horvath E., Hersh L.B., Majtenyi C., Luiten P.G.M. Cholinergic fiber aberrations in nucleus basalis lesioned rat and Alzheimer's disease. Neurobiol. Aging. 13:1992;441-448.
12. Giovannelli L., Casamenti F., Scali C., Bartolini L., Pepeu G. Differential effects of amyloid peptides β-(1-40) and β-(25-35) injections into the rat nucleus basalis. Neuroscience. 66:1995;781-792.
13. Glenner G.G., Wong C.W. Initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120:1984;885-890.
14. 2+ channels controlling presynaptic release of glutamate. Ann. New York Acad. Sci. 730:1995;210-229.
15. Gray J.A., Lalljee B. Sex differences in emotional behaviour in the rat: Correlation between the open field defecation and avoidance behaviour. Anim. Behav. 22:1974;856-881.
16. Haass C., Schlossmacher M.G., Hung A.Y., Vigo-Pelfrey C., Mellon A., Ostaszewski B.L., Lieberburg I., Koo E.H., Schenk D., Teplow D.B., Selkoe D.J. Amyloid β-peptide is produced by cultured cells during normal metabolism. Nature. 359:1992;322-325.
17. Haass C., Selkoe D.J. Cellular processing of β-amyloid precursor protein and the genesis of amyloid β-peptide. Cell. 75:1993;1039-1042.
18. (1-42) affects cholinergic but not parvalbumin-containing neurons in the septal complex of the rat. Brain Res. 698:1995;270-274.
19. (1-42) peptide on cortical projections of the rat nucleus basalis magnocellularis. Brain Res. 695:1995;71-75.
20. Hedreen J.C., Bacon S.J., Price D.L. A modified histochemical technique to visualize acetylcholinesterase-containing axons. J. Histochem. Cytochem. 33:1985;134-140.
21. Kang J., Lemaire H.-G., Unterbeck A., Salbaum J.M., Masters C.L., Grzeschik K-H., Maulthaup G., Beyreuther K., Müller-Hill B. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature. 325:1987;733-736.
22. Kimura H., Schubert D. Amyloid β-protein activates tachykinin receptors and inositol triphosphate accumulation by synergy with glutamate. Proc. Natl. Acad. Sci. USA. 90:1993;7508-7512.
23. K. Kovacs, G.K. Toth, M. Zarandi, B. Penke, T. Kadar, G. Telegdy, F. Hajual, J. Lonovics, Cholecystokinin analogs containing non-coded amino acids, in: C.M. Deber, V.J. Wuby, K.D. Kopple (Eds.), Peptides (Structure and Function), Proceedings of the 9th American Peptide Symposium. Pierce Chem., Rockford, Illinois, 1985, pp. 583-586.
24. Kowall W.N., Beal F.M., Busciglio J., Duffy K.L., Yankner B.A. An in vivo model for the neurodegenerative effects of β-amyloid and protection by substance P. Proc. Natl. Acad. Sci. USA. 88:1991;7247-7251.
25. Kowall W.N., McKee C.A., Yankner B.A., Beal F.M. In vivo neurotoxicity of beta-amyloid [β(1-40)] and the β(25-35) fragments. Neurobiol. Aging. 13:1992;537-542.
26. 2+ antagonist nimodipine, influence of aging and developmerdal drug treatment. Neurodegeneration. 4:1995;307-314.
27. Luiten P.G.M., Gaykema R.P.A., Traber J., Spencer D.G. Cortical projection patterns of magnocellular basal nucleus subdivisions as revealed by anterogradely transported Phaseolus vulgaris leucoagglutinin. Brain Res. 413:1987;229-250.
28. Luiten P.G.M., Spencer D.G. Jr., Traber J., Gaykema R.P.A. The pattern of cortical projections from the intermediate parts of the magnocellular nucleus basalis in the rat demonstrated by tracing with Phaseolus vulgaris-leucoagglutinin. Neurosci. Lett. 57:1985;137-142.
29. Mattson M.P. Secreted forms of β-amyloid precursor protein modulate dendrite outgrowth and calcium responses to glutamate in cultured embryonic hippocampal neurons. J. Neurobiol. 25:1994;439-450.
30. 2+ homeostasis in Alzheimer's disease. Trends Neurosci. 16:1993;409-414.
31. Mattson M.P., Cheng B., Davis D., Bryant K., Lieberburg I., Rydel R.E. β-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neurosci. 12:1992;376-389.
32. Mileson B.E., Schwartz R.D. The use of locomotor activity as a behavioural screen for neuronal damage following transient forebrain ischemia in gerbils. Neurosci. Lett. 128:1991;71-74.
33. Moran P.M., Higgins L.S., Cordell B., Moser P.C. Age-related learning deficits in transgenic mice expressing the 751-amino acid isoform of human β-amyloid precursor protein. Proc. Natl. Acad. Sci. USA. 92:1995;5341-5345.
34. Morris R.G.M., Garrard P., Rawlins J.N.P., O'Keefe J. Place navigation impaired in rats with hippocampal lesions. Nature. 297:1982;681-683.
35. Mouton P.R., Meyer E.M., Dunn A.J., Millard W., Arendash G.W. Induction of cortical cholinergic hypofunction and memory retention deficits through intracortical AF64A infusions. Brain Res. 444:1988;104-118.
36. Nitta A., Itoh A., Hasegawa T., Nabeshima T. β-Amyloid protein-induced Alzheimer's disease animal model. Neurosci. Lett. 170:1994;63-66.
37. G. Paxinos, C. Watson, The rat brain in stereotaxic coordinates, 2nd ed., Academic Press, Sydney, 1986.
38. B. Penke, L. Tóth, K. Soós, J. Varga, E.Z. Szabó, J. Márki-Zay, A. Baranyi, Amyloid peptides: the active center and the possible mechanism of action, starting and maintaining neuronal death, in: H.L.S. Maia (Ed.), Peptides 1994 (Proceedings of the 23th European Peptide Symposium), ESCOM, Leider, 1995, pp 101-102.
39. Pike C., Burdick D., Walencewicz A., Glabe C., Cotman C. Neurodegeneration induced by β-amyloid peptides in vitro: The role of peptide assembly state. J. Neurosci. 13:1993;1676-1687.
40. Pike C.J., Cotman C.W. Cultured GABA-immunoreactive neurons are resistant to toxicity induced by β-amyloid. Neuroscience. 56:1993;269-274.
41. Selkoe D.J. The molecular pathology of Alzheimer's disease. Neuron. 6:1991;487-498.
42. Szymusiak R. Magnocellular nuclei of the basal forebrain: substrate of sleep and arousal regulation. Sleep. 18:1995;478-500.
43. Takadera T., Sakura N., Mohri T., Hashimoto T. Toxic effect of a β-amyloid peptide (β22-35) on the hippocampal neuron and its prevention. Neurosci. Lett. 161:1993;41-44.
44. Tamborini P., Sigg H., Zbinden G. Ouantitative analysis of rat activity in the home cage by infrared monitoring. Application to the acute toxicity testing of acetanilideand phenylmercuric acetate. Arch. Toxicol. 63:1989;85-96.
45. Van der Zee E.A., Douma B.R.K., Bohus B., Luiten P.G.M. Passive avoidance training induces enhanced levels of immunoreactivity for muscarinic acetylcholine receptor and coexpressed PKCγ and MAP-2 in rat cortical neurons. Cereb. Cortex. 4:1994;376-390.
46. Waite J.J., Chen A.D., Wardlow M.L., Wiley R.G., Lappi D.A., Thal L.J. 192 Immunoglobulin G-saporin produces graded behavioral and biochemical changes accompanying the loss of cholinergic neurons of the basal forebrain and cerebellar Purkinje cells. Neuroscience. 65:1995;463-476.
47. Whiston J.S., Selkoe D.J., Cotman C.W. Amyloid β protein enhances the survival of hippocampal neurons in vitro. Science. 243:1989;1488-1490.
48. Yankner B.A., Duffy L.K., Kirschner D.A. Neurotrophic and neurotoxic effects of amyloid β protein: reversal by tachykinin neuropeptides. Science. 250:1990;279-282.