Beta-amyloid protein (25-35) disrupts hippocampal network activity: Role of Fyn-kinase

Hippocampus

Volumn 20, Issue 1, 2010, Pages 78-96

  Peña, Fernando ^a   Ordaz, Benito ^a   Balleza Tapia, Hugo ^a   Bernal Pedraza, Ramón ^a   Márquez Ramos, Abraham ^a,b   Carmona Aparicio, Liliana ^a   Giordano, Magda ^b  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Alzheimer's disease; Intracellular pathways; Intrinsic properties; Network activity; Synaptic transmission

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; AMYLOID BETA PROTEIN[25-35]; PROTEIN KINASE FYN;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DYSFUNCTION; BRAIN SLICE; CELL DISRUPTION; CELL POPULATION; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME ACTIVITY; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SYNAPTIC TRANSMISSION;

EID: 75149170925     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20592     Document Type: Article

References (142)

1. Abramowski D, Wiederhold KH, Furrer U, Jaton AL, Neuenschwander A, Runser MJ, Danner S, Reichwald J, Ammaturo D, Staab D, Stoeckli M, Rueeger H, Neumann U, Staufenbiel M. 2008. Dynamics of Abeta turnover and deposition in different betaamyloid precursor protein transgenic mouse models following gamma-secretase inhibition. J Pharmacol Exp Ther 327:411-424.
2. Angulo E, Noe V, Casado V, Mallol J, Gomez-Isla T, Lluis C, Ferrer I, Ciudad CJ, Franco R. 2004. Up-regulation of the Kv34 potassium channel subunit in early stages of Alzheimer's disease. J Neurochem 91:547-557.
3. Bi X, Gall CM, Zhou J, Lynch G. 2002. Uptake and pathogenic effects of amyloid beta peptide 1-42 are enhanced by integrin antagonists and blocked by NMDA receptor antagonists. Neuroscience 112:827-840.
4. Bates KA, Verdile G, Li QX, Ames D, Hudson P, Masters CL, Martins RN. 2008. Clearance mechanisms of Alzheimer's amyloid-beta peptide: Implications for therapeutic design and diagnostic tests. Mol Psychiatry (in press).
5. Bayer TA, Schäfer S, Simons A, Kemmling A, Kamer T, Tepest R, Eckert A, Schüssel K, Eikenberg O, Sturchler-Pierrat C, Abramowski D, Staufenbiel M, Multhaup G. 2003. Dietary Cu stabilizes brain superoxide dismutase 1 activity and reduces amyloid Abeta production in APP23 transgenic mice. Proc Natl Acad Sci USA 100:14187-14192.
6. Braak H, Braak E. 1997. Staging of Alzheimer-related cortical destruction. Int Psychogeriatr 1:257-261.
7. Busche MA, Eichhoff G, Adelsberger H, Abramowski D, Wiederhold KH, Haass C, Staufenbiel M, Konnerth A, Garaschuk O. 2008. Clusters of hyperactive neurons near amyloid plaques in a mouse model of Alzheimer's disease. Science 321:1686-1689.
8. Buzsaki G. 1989. Two-stage model of memory trace formation: A role for "noisy" brain states. Neuroscience 31:551-570.
9. Buzsaki G. 2002. Theta oscillations in the hippocampus. Neuron 33:325-340.
10. Buzsaki G, Draguhn A. 2004. Neuronal oscillations in cortical networks. Science 304:1926-1929.
11. Cacucci F, Yi M, Wills TJ, Chapman P, O'Keefe J. 2008. Place cell firing correlates with memory deficits and amyloid plaque burden in Tg2576 Alzheimer mouse model. Proc Natl Acad Sci USA 105:7863-7868.
12. Carmona-Aparicio L, Peña F, Borsodi A, Rocha L. 2007. Effects of nociceptin on the spread and seizure activity in the rat amygdala kindling model: Their correlations with 3H-leucyl-nociceptin binding. Epilepsy Res 77:75-84.
13. Carrillo-Reid L, Tecuapetla F, Tapia D, Hernández-Cruz A, Galarraga E, Drucker-Colin R, Bargas J. 2008. Encoding network states by striatal cell assemblies. J Neurophysiol 99:1435-1450.
14. Cecci C, Baglioni S, Fiorillo C, Pensalfini A, Liguri G, Nosi D, Rigacci S, Bucciantini M, Stefani M. 2005. Insights into the molecular basis of the differing susceptibility of varying cell types to the toxicity of amyloid aggregates. J Cell Sci 118:3459-3470.
15. Chin J, Palop JJ, Yu G-Q, Kojima N, Masliah E, Mucke L. 2004. Fyn kinase modulates synaptotoxicity but not aberrant sprouting in human amyloid precursor protein transgenic mice. J Neurosci 24:4692-4697.
16. Chin J, Palop JJ, Puoliväli J, Massaro C, Bien-Ly N, Gerstein H, Scearce-Levie K, Masliah E, Mucke L. 2005. Fyn kinase induces synaptic and cognitive impairments in a transgenic mouse model of Alzheimer's disease. J Neurosci 25:9694-9703.
17. Cullen WK, Wu J, Anwyl R, Rowan MJ. 1996. Beta-amyloid produces a delayed NMDA receptor-dependent reduction in synaptic transmission in rat hippocampus. NeuroReport 8:87-92.
18. Del Vecchio RA, Gold LH, Novick SJ, Wong G, Hyde LA. 2004. Increased seizure threshold and severity in young transgenic CRND8 mice. Neurosci Lett 367:164-167.
19. Delobette S, Privat A, Maurice T. 1997. In vitro aggregation facilities beta-amyloid peptide-(25-35)-induced amnesia in the rat. Eur J Pharmacol 319:1-4.
20. Dewachter I, Van Dorpe J, Smeijers L, Gilis M, Kuipéri C, Laenen I, Caluwaerts N, Moechars D, Checler F, Vanderstichele H, Van Leuven F. 2000. Aging increased amyloid peptide and caused amyloid plaques in brain of old APP/V717I transgenic mice by a different mechanism than mutant presenilin1. J Neurosci 20: 6452-6458.
21. Dineley KT, Westerman M, Bui D, Bell K, Ashe KH, Sweatt JD. 2001. b-Amyloid activates the mitogen-activated protein kinase cascade via hippocampal a7 nicotinic acetylcholine receptors: In vitro and in vivo mechanisms related to Alzheimer's disease. J Neurosci 21:4125-4133.
22. Driver JE, Racca C, Cunningham MO, Towers SK, Davies CH, Whittington MA, LeBeau FE. 2007. Impairment of hippocampal gamma-frequency oscillations in vitro in mice overexpressing human amyloid precursor protein (APP). Eur J Neurosci 26:1280-1288.
23. Engel AK, Fries P, Singer W. 2001. Dynamic predictions: Oscillations and synchrony in top-down processing. Nat RevNeurosci 2:704-716.
24. Fitzjohn SM, Morton RA, Kuenzi F, Rosahl TW, Shearman M, Lewis H, Smith D, Reynolds DS, Davies CH, Collingridge GL, Seabrook GR. 2001. Age-related impairment of synaptic transmission but normal long-term potentiation in transgenic mice that overexpress the human APP695SWE mutant form of amyloid precursor protein. J Neurosci 21:4691-4698.
25. Fonte J, Miklossy J, Atwood C, Martins R. 2001. The severity of cortical Alzheimer's type changes is positively correlated with increased amyloid-beta levels: Resolubilization of amyloid-beta with transition metal ion chelators. J Alzheimers Dis 3:209-219.
26. Freir DB, Herron CE. 2003. Nicotine enhances the depressive actions of A beta 1-40 on long-term potentiation in the rat hippocampal CA1 region in vivo. J Neurophysiol 89:2917-2922.
27. Freir DB, Costello DA, Herron CE. 2003. A beta 25-35-induced depression of long-term potentiation in area CA1 in vivo and in vitro is attenuated by verapamil. J Neurophysiol 89:3061-3069.
28. Gengler S, Gault VA, Harriott P, Hölscher C. 2007. Impairments of hippocampal synaptic plasticity induced by aggregated beta-amyloid (25-35) are dependent on stimulation-protocol and genetic background. Exp Brain Res 179:621-630.
29. Giacchino J, Criado JR, Games D, Henriksen S. 2000. In vivo synaptic transmission in young and aged amyloid precursor protein transgenic mice. Brain Res 876:185-190.
30. 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 120:885-890.
31. Grace EA, Rabiner CA, Busciglio J. 2002. Characterization of neuronal dystrophy induced by fibrillar amyloid β: Implications for Alzheimer's disease. Neuroscience 114:265-273.
32. Gregory GC, Halliday GM. 2005. What is the dominant Abeta species in human brain tissue? A review. Neurotox Res 7:29-41.
33. Gruden MA, Davudova TB, Malisauskas M, Zamotin VV, Sewell RD, Voskresenskaya NI, Kostanyan IA, Sherstnev VV, Morozova-Roche LA. 2004. Autoimmune responses to amyloid structures of Abeta(25-35) peptide and human lysozyme in the serum of patients with progressive Alzheimer's disease. Dement Geriatr Cogn Disord 18:165-171.
34. Gruden MA, Davidova TB, Malisauskas M, Sewell RD, Voskresenskaya NI, Wilhelm K, Elistratova EI, Sherstnev VV, Morozova-Roche LA. 2007. Differential neuroimmune markers to the onset of Alzheimer's disease neurodegeneration and dementia: Autoantibodies to Abeta((25-35)) oligomers, S100b and neurotransmitters. J Neuroimmunol 186:181-192.
35. Harris KD, Csicsvari J, Hirase H, Dragoi G, Buzsáki G. 2003. Organization of cell assemblies in the hippocampus. Nature 424:552-556.
36. Ho GJ, Hashimoto M, Adame A, Izu M, Alford MF, Thal LJ, Hansen LA, Masliah E. 2005. Altered p59Fyn kinase expression accompanies disease progression in Alzheimer's disease: Implications for its functional role. Neurobiol Aging 26:625-635.
37. Holscher C, Gengler S, Gault VA, Harriott P, Mallot HA. 2007. Soluble beta-amyloid[25-35] reversibly impairs hippocampal synaptic plasticity and spatial learning. Eur J Pharmacol 561:85-90.
38. Hommet C, Hureaux R, Barré J, Constans T, Berrut G. 2007. Epileptic seizures in clinically diagnosed Alzheimer's disease: Report from a geriatric medicine population. Aging Clin Exp Res 19:430-431.
39. Hooper C, Killick R, Lovestone S. 2008. The GSK3 hypothesis of Alzheimer's disease. J Neurochem 104:1433-1439.
40. Hsia AY, Masliah E, McConlogue L, Yu GQ, Tatsuno G, Hu K, Kholodenko D, Malenka RC, Nicoll RA, Mucke L. 1999. Plaqueindependent disruption of neural circuits in Alzheimer's disease mouse models. Proc Natl Acad Sci USA 96:3228-3233.
41. Hsiao K, Chapman P, Nilsen S, Eckman C, Harigaya Y, Younkin S, Yang F, Cole G. 1996. Correlative memory deficits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274:99-102.
42. Hsiao CF, Gougar K, Asai J, Chandler SH. 2007. Intrinsic membrane properties and morphological characteristics of interneurons in the rat supratrigeminal region. J Neurosci Res 85:3673-3686.
43. Hu H, Vervaeke K, Storm JF. 2002. Two forms of electrical resonance at theta frequencies generated by M-current h-current and persistent Na1 current in rat hippocampal pyramidal cells. J Physiol 545:783-805.
44. Hughes JR, Shanmugham S, Wetzel LC, Bellur S, Hughes CA. 1989. The relationship between EEG changes and cognitive functions in dementia: A study in a VA population. Clin Electroencephalogr 20:77-85.
45. Ihl R, Dierks T, Martin EM, Froolich L, Maurer K. 1996. Topography of the maximum of the amplitude of EEG frequency bands in dementia of the Alzheimer type. Biol Psychiatry 39:319-325.
46. Ikegaya Y, Aaron G, Cossart R, Aronov D, Lampl I, Ferster D, Yuste R. 2004. Synfire chains and cortical songs: Temporal modules of cortical activity. Science 304:559-564.
47. Ikegaya Y, Le Bon-Jego M, Yuste R. 2005. Large-scale imaging of cortical network activity with calcium indicators. Neurosci Res 52:132-138.
48. Ikonomovic MD, Klunk WE, Abrahamson EE, Mathis CA, Price JC, Tsopelas ND, Lopresti BJ, Ziolko S, Bi W, Paljug WR, Debnath ML, Hope CE, Isanski BA, Hamilton RL, DeKosky ST. 2008. Post-mortem correlates of in vivo PiB-PET amyloid imaging in a typical case of Alzheimer's disease. Brain 131:1630-1645.
49. Jankowsky JL, Younkin LH, Gonzales V, Fadale DJ, Slunt HH, Lester HA, Younkin SG, Borchelt DR. 2007. Rodent A beta modulates the solubility and distribution of amyloid deposits in transgenic mice. J Biol Chem 282:22707-22720.
50. Jhamandas JH, Cho C, Jassar B, Harris K, MacTavish D, Easaw J. 2001. Cellular mechanisms for amyloid b-protein activation of rat cholinergic basal forebrain neurons. J Neurophysiol 86:1312-1320.
51. Jolas T, Zhang XS, Zhang Q, Wong G, Del Vecchio R, Gold L, Priestley T. 2002. Long-term potentiation is increased in the CA1 area of the hippocampus of APP(swe/ind) CRND8 mice. Neurobiol Dis 11:394-409.
52. Kahana MJ, Sekuler R, Caplan JB, Kirschen M, Madsen JR. 1999. Human theta oscillations exhibit task dependence during virtual maze navigation. Nature 399:781-784.
53. Kahana MJ, Seelig D, Madsen JR. 2001. Theta returns. Curr Opin Neurobiol 11:739-744.
54. Kaneko I, Morimoto K, Kubo T. 2001. Drastic neuronal loss in vivo by beta-amyloid racemized at Ser(26) residue: Conversion of nontoxic [D-Ser(26)]beta-amyloid 1-40 to toxic and proteinase-resistant fragments. Neuroscience 104:1003-1011.
55. Kerr JN, Greenberg D, Helmchen F. 2005. Imaging input and output of neocortical networks in vivo. Proc Natl Acad Sci USA 102:14063-14068.
56. Kihara T, Shimohama S, Sawada H, Honda K, Nakamizo T, Shibasaki H, Kume T, Akaike A. 2001. Alpha 7 nicotinic receptor transduces signals to phosphatidylinositol 3-kinase to block A beta-amyloidinduced neurotoxicity. J Biol Chem 276:13541-13546.
57. Kinney GG, Patino P, Mermet-Bouvier Y, Starrett JE Jr, Gribkoff VK. 1999. Cognition-enhancing drugs increase stimulated hippocampal theta rhythm amplitude in the urethane-anesthetized rat. J Pharmacol Exp Ther 291:99-106.
58. Klementiev B, Novikova T, Novitskaya V, Walmod PS, Dmytriyeva O, Pakkenberg B, Berezin V, Bock E. 2007. A neural cell adhesion molecule-derived peptide reduces neuropathological signs and cognitive impairment induced by Abeta25-35. Neuroscience 145:209-224.
59. Klink R, Alonso A. 1993. Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons. J Neurophysiol 70:144-157.
60. Klunk WE, Lopresti BJ, Ikonomovic MD, Lefterov IM, Koldamova RP, Abrahamson EE, Debnath ML, Holt DP, Huang GF, Shao L, DeKosky ST, Price JC, Mathis CA. 2005. Binding of the positron emission tomography tracer Pittsburgh compound-B reflects the amount of amyloid-beta in Alzheimer's disease brain but not in transgenic mouse brain. J Neurosci 25:10598-10606.
61. Koudinov AR, Berezov TT. 2004. Alzheimer's amyloid-beta (A beta) is an essential synaptic protein not neurotoxic junk. Acta Neurobiol Exp (Warsz) 64:71-79.
62. Kowalski JW, Gawel M, Pfeffer A, Barcikowska M. 2001. The diagnostic value of EEG in Alzheimer disease: Correlation with the severity of mental impairment. J Clin Neurophysiol 18:570-575.
63. Kubo T, Nishimura S, Kumagae Y, Kaneko I. 2002. In vivo conversion of racemized beta-amyloid ([D-Ser 26]A beta 1-40) to truncated and toxic fragments ([D-Ser 26]A beta 25-35/40) and fragment presence in the brains of Alzheimer's patients. J Neurosci Res 70:474-483.
64. Kuo YM, Emmerling MR, Vigo-Pelfrey C, Kasunic TC, Kirkpatrick JB, Murdoch GH, Ball MJ, Roher AE. 1996. Water-soluble Abeta (N-40, N-42) oligomers in normal and Alzheimer disease brains. J Biol Chem 271:4077-4081.
65. Kuo YM, Emmerling MR, Bisgaier CL, Essenburg AD, Lampert HC, Drumm D, Roher AE. 1998. Elevated low-density lipoprotein in Alzheimer's disease correlates with brain abeta 1-42 levels. Biochem Biophys Res Commun 252:711-715.
66. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M, Morgan TE, Rozovsky I, Trommer B, Viola KL, Wals P, Zhang C, Finch CE, Krafft GA, Klein WL. 1998. Diffusible nonfibrillar ligands derived from Ab1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448-6453.
67. Lee JY, Friedman JE, Angel I, Kozak A, Koh JY. 2004. The lipophilic metal chelator DP-109 reduces amyloid pathology in brains of human beta-amyloid precursor protein transgenic mice. Neurobiol Aging 25:1315-1321.
68. Lemere CA, Maron R, Selkoe DJ, Weiner HL. 2001. Nasal vaccination with beta-amyloid peptide for the treatment of Alzheimer's disease. DNA Cell Biol 20:705-711.
69. Lemus-Aguilar I, Bargas J, Tecuapetla F, Galarraga E, Carrillo-Reid L. 2006. Diseño modular de instrumentación virtual para la manipulación y el análisis de señales electrofisioló gicas. Rev Mex Ing Biomed 27:82-92.
70. Leung LS, Yu HW. 1998. Theta-frequency resonance in hippocampal CA1 neurons in vitro demonstrated by sinusoidal current injection. J Neurophysiol 79:1592-1596.
71. Leung LW, Desborough KA. 1988. APV an N-methyl-D- aspartate receptor antagonist blocks the hippocampal theta rhythm in behaving rats. Brain Res 463:148-152.
72. Levites Y, Smithson LA, Price RW, Dakin RS, Yuan B, Sierks MR, Kim J, McGowan E, Reed DK, Rosenberry TL, Das P, Golde TE. 2006. Insights into the mechanisms of action of anti-Abeta antibodies in Alzheimer's disease mouse models. FASEB J 20:2576-2578.
73. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, Beach T, Kurth JH, Rydel RE, Rogers J. 1999. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 155:853-862.
74. Matsui T, Ingelsson M, Fukumoto H, Ramasamy K, Kowa H, Frosch MP, Irizarry MC, Hyman BT. 2007. Expression of APP pathway mRNAs and proteins in Alzheimer's disease. Brain Res 1161:116-123.
75. Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I, Rydel RE. 1992. Beta-amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J Neurosci 12:376-389.
76. Maurice T, Lockhart BP, Privat A. 1996. Amnesia induced in mice by centrally administered beta-amyloid peptides involves cholinergic dysfunction. Brain Res 706:181-193.
77. Menéndez M. 2005. Down syndrome, Alzheimer's disease and seizures. Brain Dev 27:246-252.
78. Moechars D, Dewachter I, Lorent K, Reverse D, Baekelandt V, Naidu A, Tesseur I, Spittaels K, Haute CV, Checler F, Godaux E, Cordell B, Van Leuven F. 1999. Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain. J Biol Chem 274:6483-6492.
79. Moore KJ, El Khoury J, Medeiros LA, Terada K, Geula C, Luster AD, Freeman MW. 2002. A CD36-initiated signaling cascade mediates inflammatory effects of beta-amyloid. J Biol Chem 277:47373-47379.
80. Mucke L, Masliah E, Yu GQ, Mallory M, Rockenstein EM, Tatsuno G, Hu K, Kholodenko D, Johnson-Wood K, McConlogue L. 2000. High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation. J Neurosci 20:4050-4058.
81. Naslund J, Haroutunian V, Mohs R, Davis KL, Davies P, Greengard P, Buxbaum JD. 2000. Correlation between elevated levels of amyloid beta-peptide in the brain and cognoscitive decline. JAMA 283:1571-1577.
82. Nimmrich V, Grimm C, Draguhn A, Barghorn S, Lehmann A, Schoemaker H, Hillen H, Gross G, Ebert U, Bruehl C. 2008. Amyloid beta oligomers (A beta(1-42) globulomer) suppress spontaneous synaptic activity by inhibition of P/Q-type calcium currents. J Neurosci 28:788-797.
83. Nobili F, Copello F, Vitali P, Prastaro T, Carozzo S, Perego G, Rodriguez G. 1999. Timing of disease progression by quantitative EEG in Alzheimer's patients. J Clin Neurophysiol 16:566-573.
84. Nowotny P, Kwon JM, Chakraverty S, Nowotny V, Morris JC, Goate AM. 2001. Association studies using novel polymorphisms in BACE1 and BACE2. NeuroReport 12:1799-1802.
85. Otsu N. 1979. A threshold selection method from gray-level histograms. IEEE Trans Syst Man Cybern 9:62-66.
86. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, Yoo J, Ho KO, Yu GQ, Kreitzer A, Finkbeiner S, Noebels JL, Mucke L. 2007. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 55:697-711.
87. Parent A, Linden DJ, Sisodia SS, Borchelt DR. 1999. Synaptic transmission and hippocampal long-term potentiation in transgenic mice expressing FAD-linked presenilin 1. Neurobiol Dis 6: 56-62.
88. Patton RL, Kalback WM, Esh CL, Kokjohn TA, Van Vickle GD, Luehrs DC, Kuo YM, Lopez J, Brune D, Ferrer I, Masliah E, Newel AJ, Beach TG, Castaño EM, Roher AE. 2006. Amyloidbeta peptide remnants in AN-1792-immunized Alzheimer's disease patients: A biochemical analysis. Am J Pathol 169:1048-1063.
89. Paxinos G, Watson C. 1998. The Rat Brain in Stereotaxic Coordinates, 4th ed. San Diego, CA: Academic Press.
90. Peña F, Alavez-Pérez N. 2006. Epileptiform activity induced by pharmacologic reduction of M-current in the developing hippocampus in vitro. Epilepsia 47:47-54.
91. Peña F, Ramirez JM. 2002. Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. J Neurosci 22:11055-11064.
92. Peña F, Ramirez JM. 2004. Substance P-mediated modulation of pacemaker properties in the mammalian respiratory network. J Neurosci 24:7549-7556.
93. Peña F, Tapia R. 1999. Relationships among seizures, extracellular amino acid changes, and neurodegeneration induced by 4-aminopyridine in rat hippocampus: A microdialysis and electroencephalographic study. J Neurochem 72:2006-2014.
94. Peña F, Tapia R. 2000. Seizures and neurodegeneration induced by 4-aminopyridine in rat hippocampus in vivo: Role of glutamateand GABA-mediated neurotransmission and of ion channels. Neuroscience 101:547-561.
95. Peña F, Bargas J, Tapia R. 2002. Paired pulse facilitation is turned into paired pulse depression in hippocampal slices after epilepsy induced by 4-aminopyridine in vivo. Neuropharmacology 42:807-812.
96. Peña F, Parkis MA, Tryba AK, Ramirez JM. 2004. Differential contribution of pacemarker properties to the generation of respiratory rhythms during normoxia and hypoxia. Neuron 43:105-117.
97. Peña F, Guitérrez-Lerma AI, Quiroz-Baez R, Arias C. 2006. The role of b-amyloid protein in synaptic function: Implications for Alzheimer's disease therapy. Curr Neuropharmacol 4:149-163.
98. Pike CJ, Walencewicz-Wasserman AJ, Kosmoski J, Cribbs DH, Glabe CG, Cotman CW. 1995. Structure-activity analyses of beta-amyloid peptides: Contributions of the beta 25-35 region to aggregation and neurotoxicity. J Neurochem 64:253-265.
99. Praticò D, Uryu K, Sung S, Tang S, Trojanowski JQ, Lee VM. 2002. Aluminum modulates brain amyloidosis through oxidative stress in APP transgenic mice. FASEB J 16:1138-1140.
100. Ramsden M, Plant LD, Webster NJ, Vaughan PF, Henderson Z, Pearson HA. 2001. Differential effects of unaggregated and aggregated amyloid b-protein (1-40) on K+ channel currents in primary cultures of rat cerebellar granule and cortical neurons. J Neurochem 79:699-712.
101. Risse SC, Lampe TH, Bird TD, Nochlin D, Sumi SM, Keenan T, Cubberley L, Peskind E, Raskind MA. 1990. Myoclonus, seizures, and paratonia in Alzheimer disease. Alzheimer Dis Assoc Disord 4:217-225.
102. Roder S, Danober L, Pozza MF, Lingenhoehl K, Wiederhold KH, Olpe HR. 2003. Electrophysiological studies on the hippocampus and prefrontal cortex assessing the effects of amyloidosis in amyloid precursor protein 23 transgenic mice. Neuroscience 120:705-720.
103. Romcy-Pereira RN, de Araujo DB, Leite JP, Garcia-Cairasco N. 2008. A semi-automated algorithm for studying neuronal oscillatory patterns: A wavelet-based time frequency and coherence analysis. J Neurosci Methods 167:384-392.
104. Romito-DiGiacomo RR, Menegay H, Cicero SA, Herrup K. 2007. Effects of Alzheimer's disease on different cortical layers: The role of intrinsic differences in Abeta susceptibility. J Neurosci 27:8496-8504.
105. Rowan MJ, Klyubin I, Wang Q, Anwyl R. 2004. Mechanisms of the inhibitory effects of amyloid beta-protein on synaptic plasticity. Exp Gerontol 39:1661-1667.
106. Rowan MJ, Klyubin I, Wang Q, Hu NW, Anwyl R. 2007. Synaptic memory mechanisms: Alzheimer's disease amyloid beta-peptideinduced dysfunction. Biochem Soc Trans 35:1219-1223.
107. Sabo S, Lambert MP, Kessey K, Wade W, Krafft G, Klein WL. 1995. Interaction of β-amyloid peptides with integrins in a human nerve cell line. Neurosci Lett 184:25-28.
108. Schreiter-Gasser U, Gasser T, Ziegler P. 1994. Quantitative EEG analysis in early onset Alzheimer's disease: Correlations with severity clinical characteristics visual EEG, CCT. Electroencephalogr Clin Neurophysiol 90:267-272.
109. Selkoe DJ. 2003. Aging amyloid and Alzheimer's disease: A perspective in honor of Carl Cotman. Neurochem Res 28:1705-1713.
110. Shinkai Y, Yoshimura M, Morishima-Kawashima M, Ito Y, Shimada H, Yanagisawa K, Ihara Y. 1997. Amyloid beta-protein deposition in the leptomeninges and cerebral cortex. Ann Neurol 42:899-908.
111. Shirazi SK, Wood JG. 1993. The protein tyrosine kinase fyn in Alzheimer's disease pathology. NeuroReport 4:435-437.
112. Small DH. 2008. Network dysfunction in Alzheimer's disease: Does synaptic scaling drive disease progression? Trends Mol Med 14:103-108.
113. Smith WW, Gorospe M, Kusiak JW. 2006. Signaling mechanisms underlying Abeta toxicity: Potential therapeutic targets for Alzheimer's disease. CNS Neurol Disord Drug Targets 5:355-361.
114. Steinerman JR, Irizarry M, Scarmeas N, Raju S, Brandt J, Albert M, Blacker D, Hyman B, Stern Y. 2008. Distinct pools of beta-amyloid in Alzheimer disease-affected brain: A clinicopathologic study. Arch Neurol 65:906-912.
115. Stepanichev MIu, Lazareva NA, Onufriev MV, Mitrokhina OS, Moiseeva IuV, Guliaeva NV. 1997. The effect of the administration of beta-amyloid peptide fragment (25-35) on behavior in rats. Zh Vyssh Nerv Deiat Im I P Pavlova 47:597-600.
116. Stepanichev MY, Moiseeva YV, Lazareva NA, Onufriev MV, Gulyaeva NV. 2003. Single intracerebroventricular administration of amyloid-beta (25-35) peptide induces impairment in short-term rather than long-term memory in rats. Brain Res Bull 61:197-205.
117. Stepanichev MY, Zdobnova IM, Zarubenko II, Moiseeva YV, Lazareva NA, Onufriev MV, Gulyaeva NV. 2004. Amyloid-beta(25-35)-induced memory impairments correlate with cell loss in rat hippocampus. Physiol Behav 80:647-655.
118. Stephan A, Laroche S, Davis S. 2001. Generation of aggregated beta-amyloid in the rat hippocampus impairs synaptic transmission and plasticity and causes memory deficits. J Neurosci 21:5703-5714.
119. Sun MK, Alkon DL. 2002. Impairment of hippocampal CA1 heterosynaptic transformation and spatial memory by beta-amyloid (25-35). J Neurophysiol 87:2441-2449.
120. Tohda C, Matsumoto N, Zou K, Meselhy MR, Komatsu K. 2004. Abeta(25-35)-induced memory impairment, axonal atrophy, and synaptic loss are ameliorated by M1, A metabolite of protopanaxadiol-type saponins. Neuropsychopharmacology 29:860-868.
121. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R. 1991. Physical basis of cognoscitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognoscitive impairment. Ann Neurol 30:572-580.
122. Traub RD, Jefferys JG, Whittington MA. 1999. Functionally relevant and functionally disruptive (epileptic) synchronized oscillations in brain slices. Adv Neurol 79:709-724.
123. Tsai LH, Lee MS, Cruz J. 2004. Cdk5 a therapeutic target for Alzheimer's disease? Biochim Biophys Acta 1697:137-142.
124. Umemori H, Wanaka A, Kato H, Takeuchi M, Tohyama M, Yamamoto T. 1999. Specific expressions of Fyn and Lyn lymphocyte antigen receptor-associated tyrosine kinases in the central nervous system. Brain Res Mol Brain Res 16:303-310.
125. Varadarajan S, Kanski J, Aksenova M, Lauderback C, Butterfield DA. 2001. Different mechanisms of oxidative stress and neurotoxicity for Alzheimer's A beta(1-42) and A beta(25-35). J Am Chem Soc 123:5625-5631.
126. Vilchis-Landeros MM, Montiel JL, Mendoza V, Mendoza-Hernández G, López-Casillas F. 2001. Recombinant soluble betaglycan is a potent and isoform-selective transforming growth factor-beta neutralizing agent. Biochem J 355:215-222.
127. Walsh DM, Klyubin I, Fadeeva JV, Rowan MJ, Selkoe DJ. 2002. Amyloid-beta oligomers: Their production toxicity and therapeutic inhibition. Biochem Soc Trans 30:552-557.
128. Wang J, Dickson DW, Trojanowski JQ, Lee VM. 1999. The levels of soluble versus insoluble brain Abeta distinguish Alzheimer's disease from normal and pathologic aging. Exp Neurol 158:328-337.
129. Wang J, Ikonen S, Gurevicius K, van Groen T, Tanila H. 2002. Alteration of cortical EEG in mice carrying mutated human APP transgene. Brain Res 943:181-190.
130. Wang Q, Rowan MJ, Anwyl R. 2004a. Beta-amyloid-mediated inhibition of NMDA receptor-dependent long-term potentiation induction involves activation of microglia and stimulation of inducible nitric oxide synthase and superoxide. J Neurosci 24:6049-6056.
131. Wang Q, Walsh DM, Rowan MJ, Selkoe DJ, Anwyl R. 2004b. Block of long-term potentiation by naturally secreted and synthetic amyloid beta-peptide in hippocampal slices is mediated via activation of the kinases c-Jun N-terminal kinase cyclin-dependent kinase 5 and p38 mitogen-activated protein kinase as well as metabotropic glutamate receptor type 5. J Neurosci 24:3370-3378.
132. Westmark CJ, Westmark PR, Beard AM, Hildebrandt SM, Malter JS. 2008. Seizure susceptibility and mortality in mice that over-express amyloid precursor protein. Int J Clin Exp Pathol 1:157-168.
133. White JA, Budde T, Kay AR. 1995. A bifurcation analysis of neuronal subthreshold oscillations. Biophys J 69:1203-1217.
134. Wu J, Anwyl R, Rowan MJ. 1995. Beta-amyloid-(1-40) increases long-term potentiation in rat hippocampus in vitro. Eur J Pharmacol 284:R1-R3.
135. Yaar M, Zhai S, Pilch PF, Doyle SM, Eisenhauer PB, Fine RE, Gilchrest BA. 1997. Binding of beta-amyloid to the p75 neurotrophin receptor induces apoptosis. A possible mechanism for Alzheimer's disease. J Clin Invest 100:2333-2340.
136. Yagi T, Shigetani Y, Okado N, Tokunaga T, Ikawa Y, Aizawa S. 1993. Regional localization of Fyn in adult brain; studies with mice in which fyn gene was replaced by lacZ. Oncogene 8:3343-3351.
137. Yagi T, Shigetani Y, Furuta Y, Nada S, Okado N, Tokunaga T, Ikawa Y. 1994. Fyn expression during neurogenesis in mouse embryo. Oncogene 9:2433-2440.
138. Yamaguchi Y, Kawashima S. 2001. Effects of amyloid-beta-(25-35) on passive avoidance, radial-arm maze learning and choline acetyltransferase activity in the rat. Eur J Pharmacol 412:265-272.
139. Yanker BA, Duffy LK, Kirschner DA. 1990 Neurotrophic and neurotoxic effects of amyloid beta protein: Reversal by tachykinin neuropeptides. Science 250:279-282.
140. Ye CP, Selkoe DJ, Hartley DM. 2003. Protofibrils of amyloid bprotein inhibit specific K1currents in neocortical cultures. Neurobiol Dis 13:177-190.
141. Yoshida M, Alonso A. 2007. Cell-type specific modulation of intrinsic firing properties and subthreshold membrane oscillations by the M(Kv7)-current in neurons of the entorhinal cortex. J Neurophysiol 98:2779-2794.
142. Yu SP, Farhangrazi ZS, Ying HS, Yeh CH, Choi DW. 1998. Enhancement of outward potassium current may participate in B-amyloid peptide-induced cortical neuronal death. Neurobiol Dis 5:81-88.