Neurotrophins enhance CaMKII activity and rescue amyloid-β-induced deficits in hippocampal synaptic plasticity

Journal of Alzheimer's Disease

Volumn 21, Issue 3, 2010, Pages 823-831

  Zeng, Yan ^a   Zhao, Danyun ^a   Xie, Cui Wei ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amyloid ; calcium and calmodulin dependent protein kinase II; hippocampus; long term potentiation; neurotrophins

Indexed keywords

AMPA RECEPTOR; AMYLOID BETA PROTEIN[1-42]; BRAIN DERIVED NEUROTROPHIC FACTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; NEUROTROPHIN; NEUROTROPHIN 4;

ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; BRAIN SLICE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LONG TERM POTENTIATION; MALE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 77957272505     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-100264     Document Type: Article

References (47)

1. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, Gallagher M,AsheKH (2006)A specific amyloidbeta protein assembly in the brain impairs memory. Nature 440, 352357.
2. Lacor PN, Buniel MC, Chang L, Fernandez SJ, Gong Y, Viola KL, LambertMP,Velasco PT, Bigio EH, Finch CE, Krafft GA, Klein WL (2004) Synaptic targeting by Alzheimer'srelated amyloid beta oligomers. J Neurosci 24, 1019110200. (Pubitemid 39492046)
3. 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 Abeta142 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95, 64486453. (Pubitemid 28249033)
4. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal longterm potentiation in vivo. Nature 416, 535539. (Pubitemid 34288854)
5. Shankar GM, Li S, Mehta TH, GarciaMunoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ (2008) Amyloidbeta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity andmemory. Nat Med 14, 837842.
6. Li S, Hong S, Shepardson NE, Walsh DM, Shankar GM, Selkoe D(2009) Soluble oligomers of amyloid Beta protein facilitate hippocampal longterm depression by disrupting neuronal glutamate uptake. Neuron 62, 788801.
7. 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(142) globulomer) suppress spontaneous synaptic activity by inhibition of P/Qtype calcium currents. J Neurosci 28, 788797. (Pubitemid 351159014)
8. Gortz P, Opatz J, Siebler M, Funke SA, Willbold D, LangeAsschenfeldt C (2009) Transient reduction of spontaneous neuronal network activity by sublethal amyloid beta (142) peptide concentrations. J Neural Transm 116, 351355.
9. Fradinger EA, Monien BH, Urbanc B, Lomakin A, Tan M, Li H, Spring SM, Condron MM, Cruz L, Xie CW, Benedek GB, Bitan G (2008) Cterminal peptides coassemble into Abeta42 oligomers and protect neurons against Abeta42induced neurotoxicity. Proc Natl Acad Sci U S A 105, 1417514180.
10. Selkoe DJ (2008) Soluble oligomers of the amyloid betaprotein impair synaptic plasticity and behavior. Behav Brain Res 192, 106113.
11. Venkitaramani DV, Chin J, Netzer WJ, Gouras GK, Lesne S, Malinow R, Lombroso PJ (2007) Betaamyloid modulation of synaptic transmission and plasticity. J Neurosci 27, 1183211837. (Pubitemid 350072092)
12. Chen QS, Kagan BL, Hirakura Y, Xie CW(2000) Impairment of hippocampal longterm potentiation by Alzheimer amyloid bpeptides. J Neurosci Res 60, 6572. (Pubitemid 30176750)
13. Chen QS, Wei WZ, Shimahara T, Xie CW (2002) Alzheimer amyloid bpeptide inhibits the late phase of longterm potentiation through calcineurindependent mechanisms in the hippocampal dentate gyrus. Neurobiol Learn Mem 77, 354371. (Pubitemid 34971647)
14. Knobloch M, Farinelli M, Konietzko U, Nitsch RM, Mansuy IM (2007) Abeta oligomermediated longterm potentiation impairment involves protein phosphatase 1dependent mechanisms. J Neurosci 27, 76487653. (Pubitemid 47093800)
15. Zhao D, Watson JB, Xie CW (2004) Amyloid beta prevents activation of calcium/calmodulindependent protein kinase II and AMPA receptor phosphorylation during hippocampal longterm potentiation.J Neurophysiol 92, 28532858. (Pubitemid 40340496)
16. Silva AJ, Paylor R, Wehner JM, Tonegawa S (1992) Impaired spatial learning in alphacalciumcalmodulin kinase II mutant mice. Science 257, 206210.
17. Blitzer RD, Connor JH, Brown GP, Wong T, Shenolikar S, Iyengar R, Landau EM (1998) Gating of CaMKII by cAMPregulated protein phosphatase activity during LTP. Science 280, 19401942. (Pubitemid 28299402)
18. Xie CW(2004) Calciumregulated signaling pathways: Role in amyloid betainduced synaptic dysfunction. Neuromolecular Med 6, 5364.
19. Lu B (2003) BDNF and activitydependent synaptic modulation. Learn Mem 10, 8698.
20. Wang LM, Dragich JM, Kudo T, Odom IH,Welsh DK, O'Dell TJ, Colwell CS (2009) Expression of the circadian clock gene Period2 in the hippocampus: Possible implications for synaptic plasticity and learned behaviour. ASN Neuro 1, e00012.
21. Korte M, Carroll P, Wolf E, Brem G, Thoenen H, Bonhoeffer T (1995) Hippocampal longterm potentiation is impaired in mice lacking brainderived neurotrophic factor. Proc Natl Acad Sci U S A 92, 88568860.
22. Korte M, Kang H, Bonhoeffer T, Schuman E (1998) A role for BDNF in the latephase of hippocampal longterm potentiation. Neuropharmacology 37, 553559. (Pubitemid 28306944)
23. Vyssotski AL, Dell'Omo G, Poletaeva, II, Vyssotsk DL, Minichiello L,Klein R,Wolfer DP, LippHP (2002) Longterm monitoring of hippocampusdependent behavior in naturalistic settings: mutant mice lacking neurotrophin receptor TrkB in the forebrain show spatial learning but impaired behavioral flexibility. Hippocampus 12, 2738. (Pubitemid 34211244)
24. Patterson SL, Abel T, Deuel TA, Martin KC, Rose JC, Kandel ER (1996) Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice. Neuron 16, 11371145. (Pubitemid 26227235)
25. Muller D, DjebbaraHannas Z, Jourdain P, Vutskits L, Durbec P, RougonG,Kiss JZ (2000)Brainderived neurotrophic factor restores longterm potentiation in polysialic acidneural cell adhesion moleculedeficient hippocampus. Proc Natl Acad Sci U S A 97, 43154320. (Pubitemid 30226130)
26. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, Zhen S, Teng KK, Yung WH, Hempstead BL, Lu B (2004) Cleavage of proBDNF by tPA/plasmin is essential for longterm hippocampal plasticity. Science 306, 487491. (Pubitemid 39372449)
27. Xie CW, Sayah D, Chen QS,WeiWZ, Smith D, Liu X (2000) Deficient longterm memory and longlasting longterm potentiation in mice with a targeted deletion of neurotrophin4 gene. Proc Natl Acad Sci U S A 97, 81168121. (Pubitemid 30460782)
28. Fan G, Egles C, Sun Y,Minichiello L, Renger JJ, Klein R, Liu G, Jaenisch R (2000) Knocking the NT4 gene into the BDNF locus rescues BDNF deficient mice and reveals distinct NT4 and BDNF activities. Nat Neurosci 3, 350357. (Pubitemid 30185485)
29. Gottschalk W, PozzoMiller LD, Figurov A, Lu B (1998) Presynaptic modulation of synaptic transmission and plasticity by brainderived neurotrophic factor in the developing hippocampus. J Neurosci 18, 68306839. (Pubitemid 28388014)
30. Kovalchuk Y, Hanse E,Kafitz KW, Konnerth A (2002) Postsynaptic Induction of BDNFMediated LongTerm Potentiation. Science 295, 17291734.
31. Madara JC, Levine ES (2008) Presynaptic and postsynaptic NMDAreceptorsmediate distinct effects of brainderived neurotrophic factor on synaptic transmission. J Neurophysiol 100, 31753184.
32. Strack S, Choi S, Lovinger DM, Colbran RJ (1997) Translocation of autophosphorylated calcium/calmodulindependent protein kinase II to the postsynaptic density. J Biol Chem 272, 1346713470. (Pubitemid 27224771)
33. Benfenati F, Valtorta F, Rubenstein JL, Gorelick FS, Greengard P, Czernik AJ (1992) Synaptic vesicleassociated Ca2+/calmodulindependent protein kinase II is a binding protein for synapsin I. Nature 359, 417420.
34. Derkach V, Barria A, Soderling TR (1999) Ca2+/calmodulinkinase II enhances channel conductance of alphaamino3hydroxy5methyl4isoxazolepropionate type glutamate receptors. Proc Natl Acad Sci U S A 96, 32693274. (Pubitemid 29148880)
35. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC,Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: Requirement for GluR1 and PDZ domain interaction. Science 287, 22622267. (Pubitemid 30177031)
36. Jourdain P, Fukunaga K, Muller D (2003) Calcium/calmodulindependent protein kinase II contributes to activitydependent filopodia growth and spine formation. J Neurosci 23, 1064510649. (Pubitemid 37485278)
37. Hsieh H, Boehm J, Sato C, Iwatsubo T, Tomita T, Sisodia S, Malinow R (2006) AMPAR removal underlies Abetainduced synaptic depression and dendritic spine loss. Neuron 52, 831843. (Pubitemid 44828454)
38. Gu Z, Liu W, Yan Z (2009) betaAmyloid impairs AMPA receptor trafficking and function by reducing Ca2+/calmodulindependent protein kinase II synaptic distribution. J Biol Chem 284, 1063910649.
39. Lanz TA, Carter DB, Merchant KM (2003) Dendritic spine loss in the hippocampus of young PDAPP and Tg2576 mice and its prevention by the ApoE2 genotype. Neurobiol Dis 13, 246253.
40. Reichardt LF (2006) Neurotrophinregulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 361, 15451564.
41. Thoenen H (1995) Neurotrophins and neuronal plasticity. Science 270, 593598.
42. Guo ZH,MattsonMP (2000) Neurotrophic factors protect cortical synaptic terminals against amyloid and oxidative stressinduced impairment of glucose transport, glutamate transport and mitochondrial function. Cereb Cortex 10, 5057.
43. Ferrer I, Marin C, Rey MJ, Ribalta T, Goutan E, Blanco R, Tolosa E,Marti E (1999) BDNF and fulllength and truncated TrkB expression in Alzheimer disease: Implications in therapeutic strategies. J Neuropathol Exp Neurol 58, 729739. (Pubitemid 29328502)
44. Phillips HS, Hains JM, Armanini M, Laramee GR, Johnson SA, Winslow JW (1991) BDNF mRNA is decreased in the hippocampus of individuals with Alzheimer's disease. Neuron 7, 695702.
45. TapiaArancibia L, Aliaga E, Silhol M, Arancibia S (2008) New insights into brain BDNF function in normal aging and Alzheimer disease. Brain Res Rev 59, 201220.
46. Jang SW, Liu X, Yepes M, Shepherd KR, Miller GW, Liu Y, Wilson WD, Xiao G, Blanchi B, Sun YE, Ye K (2010) A selective TrkB agonist with potent neurotrophic activities by 7,8dihydroxyflavone. Proc Natl Acad Sci U S A 107, 26872692.
47. BlurtonJones M, Kitazawa M, MartinezCoria H, Castello NA, Muller FJ, Loring JF, Yamasaki TR, Poon WW, Green KN, LaFerla FM (2009) Neural stem cells improve cognition via BDNF in a transgenic model of Alzheimer disease. Proc Natl Acad Sci U S A 106, 1359413599.