Amyloid β peptide induces tau phosphorylation and loss of cholinergic neurons in rat primary septal cultures

Neuroscience

Volumn 115, Issue 1, 2002, Pages 201-211

  Zheng, W H ^a   Bastianetto, S ^a   Mennicken, F ^a   Ma, W ^a   Kar, S ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Alzheimer's disease; Cholinergic neurons; Neurotoxicity; Signal transduction; Tau phosphorylation; Western blotting

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; AMYLOID BETA PROTEIN; CHOLINE ACETYLTRANSFERASE; GLYCOGEN SYNTHASE KINASE 3BETA; LITHIUM CHLORIDE; MITOGEN ACTIVATED PROTEIN KINASE; TAU PROTEIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CHOLINERGIC NERVE CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOSKELETON; DRUG EFFECT; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RAT;

AMYLOID BETA-PROTEIN; ANIMALS; CELL SURVIVAL; CELLS, CULTURED; CHOLINE O-ACETYLTRANSFERASE; CHOLINERGIC FIBERS; EMBRYO; FEMALE; NEURONS; PEPTIDE FRAGMENTS; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SEPTUM OF BRAIN; TAU PROTEINS;

EID: 0037110601     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(02)00404-9     Document Type: Article

References (66)

1. Alvarez A., Toro R., Caceres A., Maccioni R.B. Inhibition of tau phosphorylating protein kinase cdk5 prevents β-amyloid-induced neuronal death. FEBS Lett. 459:2001;421-426.
2. Alvarez G., Munoz-Montano J.R., Satrustegui J., Avila J., Bogonez E., Diaz-Nido J. Lithium protects cultured neurons against β-amyloid-induced neurodegeneration. FEBS Lett. 453:1999;260-264.
3. Auld D.S., Kar S., Quirion R. β-Amyloid peptides as direct cholinergic neuromodulators: a missing link. Trends Neurosci. 21:1998;408-417.
4. Bartus R.T., Dean R.L. III, Beer B., Lipa A.S. The cholinergic hypothesis of geriatric memory dysfunction. Science. 217:1982;408-417.
5. Bastianetto S., Ramassamy C., Dore S., Christen Y., Poirier J., Quirion R. The ginko biloba extract (Egb 761) protects hippocampal neurons against cell death induced by β-amyloid. Eur. J. Neurosci. 12:2000;1882-1890.
6. Billingsley M.L., Kincaid R.L. Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneraion. Biochem. J. 323:1997;577-591.
7. Brion J.P., Anderton B.H., Authelet M., Dayanandan R., Leroy K., Lovestone S., Octave J.N., Pradier L., Touchet N., Tremp G. Neurofibrillary tangles and tau phosphorylation. Biochem. Soc. Symp. 67:2001;81-88.
8. Busciglio J., Lorenzo A., Yeh J., Yankner B.A. β-Amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron. 14:1995;879-888.
9. Calhoun M., Wiederhold K., Abramowski D., Phinney A.L., Sturchler-Pierrat C., Staufenbiel M., Sommer B., Jucker M. Neuron loss in APP transgenic mice. Nature. 395:1998;755-756.
10. Cordell B. β-Amyloid formation as a potential therapeutic target for Alzheimer's disease. Annu. Rev. Pharmacol. Toxicol. 34:1994;69-89.
11. Cotman, C.W., Pike, C.J., 1994. β-Amyloid and its contribution to neurodegeneration in Alzheimer's disease. In: Terry, R.D., Katzman, R., Bick, K.L. (Eds.), Alzheimer Disease. Raven Press, New York, pp. 305-315.
12. Davis D.R., Brion J.-P., Couck A.-M., Gallo J.-M., Hanger D.P., Ladhani K., Lewis C., Miller C.C.J., Rupniak T., Smith C., Anderton B.H. The phosphorylation state of the microtubule-associated protein tau as affected by glutamate, colchicines and β-amyloid in primary rat cortical neuronal cultures. Biochem. J. 309:1995;941-949.
13. DeKosky S.T., Scheff S.W. Synapse loss of frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann. Neurol. 27:1990;457-464.
14. Ekinci E.J., Malik K.U., Shea T.B. Activation of the voltage-sensitive calcium channel by mitogen-activated protein (MAP) kinase following exposure of neuronal cells to β-amyloid. J. Biol. Chem. 274:1999;30322-30327.
15. Ferreira A., Lu Q., Orecchio L., Kosik K.S. Selective phosphorylation of adult tau isoforms in mature hippocampal neurons exposed to fibrillar Aβ Mol. Cell. Neurosci. 9:1997;220-234.
16. Francis P.T., Palmer A.M., Snape M., Wilcock G.K. The cholinergic hypothesis of Alzheimer's disease: a review of progress. J. Neurol. Neurosurg. Psychiatry. 66:1999;137-147.
17. Geula, C., Mesulam, M.M., 1994. Cholinergic system and related neuropathological predilection patterns in Alzheimer's disease. In: Terry, R.D., Katzman, R., Bick, K.L. (Eds.), Alzheimer Disease. Raven Press, New York, pp. 263-291.
18. Geula C., Wu C.K., Saroff D., Lorenzo A., Yuan M., Yanker B.A. Aging renders the brain vulnerable to amyloid β-protein neurotoxicity. Nat. Med. 4:1998;827-831.
19. Giaccone G., Tagliavini F., Linoli G., Bouras C., Frigerio L., Frangione B., Bugiani O. Down patients: extracellular preamyloid deposits precede neuritic degeneration and senile plaques. Neurosci. Lett. 97:1989;232-238.
20. Giovannelli L., Casamenti F., Scali C., Bartolini L., Pepeu G. Differential effects of amyloid peptides β-(1-40) and β-(25-35) injections into rat nucleus basalis. Neuroscience. 66:1995;781-792.
21. Goedert M. Tau protein and the neurofibrillary pathology of Alzheimer's disease. Trends Neurosci. 16:1993;460-465.
22. Gotz J., Chen F., van Dorpe J., Nitsch R.M. Formation of neurofibrillary tangles in P301L tau transgenic mice induced by Aβ42 fibrils. Science. 293:2001;1491-1495.
23. Greenberg S.M., Koo E.H., Selkoe D.J., Qiu W.Q., Kosik K.S. Secreted β-amyloid precursor protein stimulates mitogen-activated protein kinase and enhances ô phosphorylation. Proc. Natl. Acad. Sci. USA. 91:1994;7104-7108.
24. Greenberg S.M., Kosik K.S. Secreted β-APP stimulates MAP kinase and phosphorylation of tau in neurons. Neurobiol. Aging. 16:1995;403-408.
25. Gschwind M., Huber S. Apoptotic cell death induced by β-amyloid1-42 is cell type dependent. J. Neurochem. 65:1995;292-300.
26. 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.
27. Hardy J. Amyloid, the presenilins and Alzheimer's disease. Trends Neurosci. 20:1997;154-159.
28. Harkany T., De Jong G.I., Soos K., Penke B., Luiten P.G.M., Gulya K. β-Amyloid1-42 affects cholinergic but not parvalbumin-containing neurones in the septal complex of the rat. Brain Res. 698:1995;27-274.
29. Hellstrom-Lindahl E. Modulation of β-amyloid precursor protein processing and tau phosphorylation by acetylcholine receptors. Eur. J. Pharmacol. 393:2000;255-263.
30. Hohmann, C., Antuono, P., Coyle, J.T., 1988. Basal forebrain cholinergic neurons and Alzheimer's disease. In: Iversen, L.L., Snyder, S.H. (Eds.), Handbook of Psychopharmacology: Psychopharmacology of the Aging Nervous System. Plenum Press, New York, pp. 69-106.
31. Hong M., Chen D.C.R., Klein P.S., Lee V.M.-Y. Lithium reduces tau phosphorylation by inhibition of glycogen synthase kinase-3. J. Biol. Chem. 40:1997;25326-25332.
32. 1-42 supresses acetylcholine synthesis. J. Biol. Chem. 272:1997;2038-2041.
33. Hyman B.T., Elvhage T.E., Reiter J. Extracellular signal regulated kinases. Localization of protein and mRNA in the human hippocampal formation in Alzheimer's disease. Am. J. Pathol. 144:1994;565-572.
34. Iqbal K., Alonso A.C., Gong C.X., Khatoon S., Pei J.J., Wang J.Z., Grundke-Iqbal I. Mechanisms of neurofibrillary degeneration and the formation of neurofibrillary tangles. J. Neural Transm. (Suppl.). 53:1998;169-180.
35. Itoh A., Nitta A., Nadai M., Nishimura K., Hirose M., Hasegawa T., Nabeshima T. Dysfunction of cholinergic and dopaminergic neuronal systems in β-amyloid protein-infused rats. J. Neurochem. 66:1996;1113-1117.
36. Johnson G.V.W., Jenkins S.M. Tau protein in normal and Alzheimer's disease brain. Alzheimer's Dis. Rev. 1:1996;38-54.
37. Kar S., Issa A.M., Seto D., Auld D.S., Collier B., Quirion R. Amyloid β-peptide inhibits high-affinity choline uptake and acetylcholine release in rat hippocampal slices. J. Neurochem. 70:1998;2179-2187.
38. Kar S., Seto D., Gaudreau P., Quirion R. β-Amyloid-related peptides inhibit potassium-evoked acetylcholine release from rat hippocampal formation. J. Neurosci. 16:1996;1034-1040.
39. Kelly J.F., Furukawa K., Barger S.W., Rengen M.R., Mark R.J., Blanc E.M., Roth G.S., Mattson M.P. Amyloid β-peptide disrupts carbachol-induced muscarinic cholinergic signal transduction in cortical neurons. Proc. Natl. Acad. Sci. USA. 93:1996;6753-6758.
40. Le W., Xie W.J., Kong R., Appel S.H. β-Amyloid-induced neurotoxicity of a hybrid septal cell line associated with increased tau phosphorylation and expression β-amyloid precursor protein. J. Neurochem. 69:1997;978-985.
41. Lee V.M.-Y. Tauists and Baptists united - well almost. Science. 293:2001;1446-1447.
42. Lewis J., Dickson D.W., Lin W.-L., Chisholm L., Corral A., Jones G., Yen S., Sahara N., Skipper L., Yager D., Eckman C., Hardy J., Hutton M., McGowan E. Enhanced neurofibrillary degeneration in transgenic mice expressing mutant tau and APP. Science. 293:2001;1487-1491.
43. Lovestone S., Reynolds C.H., Latimer D., Davis D.R., Anderton B.H., Gallo J.M., Hanger D., Mulot S., Marquardt B., Stabel S., Woodgett J.R., Miller C.J. Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells. Curr. Biol. 4:1994;1077-1086.
44. Ma W., Zheng W.-H., Belanger S., Kar S., Quirion R. Effects of amyloid peptides on cell viability and expression of neuropeptides in cultured rat dorsal root ganglion neurons: a role for free radicals and protein kinase C. Eur. J. Neurosci. 13:2001;1125-1135.
45. Mark R.J., Lovell M.A., Markesbery W.R., Uchida K., Mattson M.P. A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid β-peptide. J. Neurochem. 68:1997;255-264.
46. Masliah E., Sisk A., Mallory M., Games D. Neurofibrillary pathology in transgenic mice overexpressing V717F beta-amyloid precursor protein. J. Neuropathol. Exp. Neurol. 60:2001;357-368.
47. 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.
48. Maurice T., Lockhart B.P., Privat A. Amnesia induced in mice by centrally administered β-amyloid peptides involves cholinergic dysfunction. Brain Res. 706:1996;181-193.
49. Mennicken F., Quirion R. Interleukin-2 increases choline acetyltransferase activity in septal-cell cultures. Synapse. 26:1997;175-183.
50. Olesen O.F., Dago L., Mikkelsen J.D. Amyloid β neurotoxicity in the cholinergic but not in the serotonergic phenotype of RN46A cells. Mol. Brain Res. 57:1998;266-274.
51. Pedersen W.A., Kloczewiak M.A., Blusztajn J.K. Amyloid β-protein reduces acetylcholine synthesis in a cell line derived from cholinergic neurons of the basal forebrain. Proc. Natl. Acad. Sci. USA. 93:1996;8068-8071.
52. Pike C.J., Burdick D., Walencewicz A.J., Glabe C.G., Cotman C.W. Neurodegeneration induced by β-amyloid peptides in vitro: the role of peptide assembly state. J. Neurosci. 13:1993;1676-1687.
53. Pike C.J., Cotman C.W. Cultured GABA-immunoreactive neurons are resistant to toxicity induced by β-amyloid. Neuroscience. 56:1993;269-274.
54. Price D.L., Sisodia S.S. Mutant genes in familial Alzheimer's disease and transgenic models. Annu. Rev. Neurosci. 21:1998;479-505.
55. Quirion R. Cholinergic markers in Alzheimer's disease and the autoregulation of acetylcholine release. J. Psychiatry Neurosci. 18:1993;226-234.
56. Rapoport M., Ferreira A. PD98059 prevents neurite degeneration induced by fibrillar β-amyloid in mature hippocampal neurons. J. Neurochem. 74:2000;125-133.
57. Selkoe D.J. Translating cell biology into therapeutic advances in Alzheimer's disease. Nature. 399:1999;A23-A31.
58. Seubert P., Vigo-Pelfrey C., Esch F., Lee M., Dovey H., Davis D., Sinha S., Schlossmacher M., Whaley J., Swindlehurst C., McCormack R., Wolfert R., Selkoe D., Lieberburg I., Schenk D. Isolation and quantification of soluble Alzheimer β-peptide from biological fluids. Nature. 359:1992;325-327.
59. Shea T.B., Prabhakar S., Ekinci F.J. β-Amyloid and ionophore A23187 evoke tau hyperphosphorylation bt distinct intracellular pathways: differential involvement of the calpain/protein kinase C system. J. Neurosci. Res. 49:1997;759-768.
60. Shiurba R.A., Ishiguro K., Takahashi M., Sato K., Spooner E.T., Mercken M., Yoshida R., Wheelock T.R., Yanagawa H., Imahori K., Nixon R.A. Immunocytochemistry of tau phosphoserine 413 and tau protein kinase I in Alzheimer pathology. Brain Res. 737:1996;119-132.
61. Sindou P., Lesort M., Couratier P., Yardin C., Esclaire F., Hugon J. Glutamate increases tau phosphorylation in primary neuronal cultures from fetal rat cerebral cortex. Brain Res. 646:1994;124-128.
62. Takashima A., Honda T., Yasutake K., Michel G., Murayama O., Murayama M., Ishiguro K., Yamaguchi H. Activation of tau protein kinase I/glycogen synthase kinase-3 beta by amyloid beta peptide (25-35) enhances phosphorylation of tau in hippocampal neurons. Neurosci. Res. 4:1998;317-323.
63. Wurtman R. Choline metabolism as a basis for the selective vulnerability of cholinergic neurones. Trends Neurosci. 15:1992;117-122.
64. Yankner B.A. Mechanisms of neuronal degeneration in Alzheimer's disease. Neuron. 16:1996;921-932.
65. Zheng W.-H., Kar S., Quirion R. Insulin-like growth factor-1-induced phosphorylation of the Forkhead family transcriptiuon factor FKHRL1 is mediated by Akt kinase in PC12 cells. J. Biol. Chem. 275:2000;39152-39158.
66. Zheng W.-H., Kar S., Quirion R. Stimulation of protein kinase C modulates insulin-like growth factor-I (IGF-I) induced Akt activation in PC12 cells. J. Biol. Chem. 275:2000;13377-13385.