Intraneuronally injected amyloid beta inhibits long-term potentiation in rat hippocampal slices

Journal of Neurophysiology

Volumn 107, Issue 9, 2012, Pages 2526-2531

  Nomura, Izumi ^a,b   Takechi, Hajime ^a   Kato, Nobuo ^b  

^a KYOTO UNIVERSITY   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

Alzheimer's disease; Metabotropic glutamate receptor; P38 MAPK; Whole cell patch clamp

Indexed keywords

2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42];

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; LONG TERM POTENTIATION; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION;

AMYLOID BETA-PEPTIDES; ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; INJECTIONS, INTRAVENTRICULAR; LONG-TERM POTENTIATION; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; RATS, WISTAR;

EID: 84860540570     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00589.2011     Document Type: Article

References (51)

1. Ango F, Prézeau L, Muller T, Tu JC, Xiao B, Worley PF, Pin JP, Bockaert J, Fagni L. Agonist-independent activation of metabotropic glutamate receptors by the intracellular protein Homer. Nature 411: 962-965, 2001.
2. Barry AE, Klyubin I, Mc Donald JM, Mably AJ, Farrell MA, Scott M, Walsh DM, Rowan MJ. Alzheimer's disease brain-derived amyloid-β-mediated inhibition of LTP in vivo is prevented by immunotargeting cellular prion protein. J Neurosci 31: 7259-7263, 2011.
3. Benilova I, De Strooper B. Prion protein in Alzheimer's pathogenesis: a hot and controversial issue. EMBO Mol Med 2: 289-290, 2010.
4. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM. Intraneuronal Aβ causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45: 675-688, 2005.
5. Brakeman PR, Lanahan AA, O'Brien R, Roche K, Barnes CA, Huganir RL, Worley PF. Homer: a protein that selectively binds metabotropic glutamate receptors. Nature 386: 284-288, 1997.
6. Chen L, Yamada K, Nabeshima T, Sokabe M. Alpha7 Nicotinic acetylcholine receptor as a target to rescue deficit in hippocampal LTP induction in beta-amyloid infused rats. Neuropharmacology 50: 254-268, 2006.
7. Chui DH, Tanahashi H, Ozawa K, Ikeda S, Checler F, Ueda O, Suzuki H, Araki W, Inoue H, Shirotani K, Takahashi K, Gallyas F, Tabira T. Transgenic mice with Alzheimer presenilin 1 mutations show accelerated neurodegeneration without amyloid plaque formation. Nat Med 5: 560-564, 1999.
8. Crouch PJ, Harding SM, White AR, Camakaris J, Bush AI, Masters CL. Mechanisms of A beta mediated neurodegeneration in Alzheimer's disease. Int J Biochem Cell Biol 40: 181-198, 2008.
9. Deane R, Du Yan S, Submamaryan RK, LaRue B, Jovanovic S, Hogg E, Welch D, Manness L, Lin C, Yu J, Zhu H, Ghiso J, Frangione B, Stern A, Schmidt AM, Armstrong DL, Arnold B, Liliensiek B, Nawroth P, Hofman F, Kindy M, Stern D, Zlokovic B. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med 9: 907-913, 2003.
10. Giménez-Llort L, Blázquez G, Cañete T, Johansson B, Oddo S, Tobeña A, LaFerla FM, Fernández-Teruel A. Modeling behavioral and neuronal symptoms of Alzheimer's disease in mice: a role for intraneuronal amyloid. Neurosci Biobehav Rev 31: 125-147, 2007.
11. Gong B, Cao Z, Zheng P, Vitolo OV, Liu S, Staniszewski A, Moolman D, Zhang H, Shelanski M, Arancio O. Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell 126: 775-788, 2006.
12. Gouras GK, Almeida CG, Takahashi RH. Intraneuronal Abeta accumulation and origin of plaques in Alzheimer's disease. Neurobiol Aging 26: 1235-1244, 2005.
13. Gouras GK, Tsai J, Naslund J, Vincent B, Edgar M, Checler F, Greenfield JP, Haroutunian V, Buxbaum JD, Xu H, Greengard P, Relkin NR. Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 156: 15-20, 2000.
14. Glabe C. Intracellular mechanisms of amyloid accumulation and pathogenesis in Alzheimer's disease. J Mol Neurosci 17: 137-145, 2001.
15. Hsieh H, Boehm J, Sato C, Iwatsubo T, Tomita T, Sisodia S, Malinow R. AMPAR removal underlies Aβ-induced synaptic depression and dendritic spine loss. Neuron 52: 831-843, 2006.
16. Itoh A, Akaike T, Sokabe M, Nitta A, Iida R, Olariu A, Yamada K, Nabeshima T. Impairments of long-term potentiation in hippocampal slices of beta-amyloid-infused rats. Eur J Pharmacol 382: 167-175, 1999.
17. Jacobsen JS, Wu CC, Redwine JM, Comery TA, Arias R, Bowlby M, Martone R, Morrison JH, Pangalos MN, Reinhart PH, Bloom FE. Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 103: 5161-5166, 2006.
18. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, Iwatsubo T, Sisodia S, Malinow R. APP processing and synaptic function. Neuron 37: 925-937, 2003.
19. Kato N. Neurophysiological mechanisms of electroconvulsive therapy for depression. Neurosci Res 64: 3-611, 2009.
20. Kato A, Ozawa F, Saitoh Y, Hirai K, Inokuchi K. Vesl, a gene encoding VASP/Ena family related protein, is upregulated during seizure, long-term potentiation and synaptogenesis. FEBS Lett 412: 183-189, 1997.
21. Kienlen-Campard P, Miolet S, Tasiaux B, Octave JN. Intracellular amyloidbeta 1-42, but not extracellular soluble amyloid-beta peptides, induces neuronal apoptosis. J Biol Chem 277: 15666-15670, 2002.
22. Klyubin I, Walsh DM, Cullen WK, Fadeeva JV, Anwyl R, Selkoe DJ, Rowan MJ. Soluble Arctic amyloid beta protein inhibits hippocampal long-term potentiation in vivo. Eur J Neurosci 19: 2839-2846, 2004.
23. LaFerla FM, Green KN, Oddo S. Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neursci 8: 499-509, 2007.
24. Laurén J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-βoligomers. Nature 457: 1128-1132, 2009.
25. Li M, Chen L, Lee DH, Yu LC, Zhang Y. The role of intracellular amyloid beta in Alzheimer's disease. Prog Neurobiol 83: 131-139, 2007.
26. Ma T, Hoeffer CA, Wong H, Massaad CA, Zhou P, Iadecola C, Murphy MP, Pautler RG, Klann E. Amyloid β-induced impairments in hippocampal synaptic plasticity are rescued by decreasing mitochondrial superoxide. J Neurosci 31: 5589-5595, 2011.
27. Martin LJ, Pardo CA, Cork LC, Price DL. Synaptic pathology and glial responses to neuronal injury precede the formation of senile plaques and amyloid deposits in the aging cerebral cortex. Am J Pathol 145: 1358-1381, 1994.
28. Nalbantoglu J, Tirado-Santiago G, Lahsaïni A, Poirier J, Goncalves O, Verge G, Momoli F, Welner SA, Massicotte G, Julien JP, Shapiro ML. Impaired learning and LTP in mice expressing the carboxy terminus of the Alzheimer amyloid precursor protein. Nature 387: 500-505, 1997.
29. Nomura I, Kato N, Kita T, Takechi H. Mechanism of impairment of long-term potentiation by amyloid beta is independent of NMDA receptors or voltage-dependent calcium channels in hippocampal CA1 pyramidal neurons. Neurosci Lett 391: 1-2, 2005.
30. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, Metherate R, Mattson MP, Akbari Y, LaFerla FM. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 39: 409-421, 2003.
31. Origlia N, Righi M, Capsoni S, Cattaneo A, Fang F, Stern DM, Chen JX, Schmidt AM, Arancio O, Yan SD, Domenici L. Receptor for advanced glycation end product-dependent activation of p38 mitogen-activated protein kinase contributes to amyloid-beta-mediated cortical synaptic dysfunction. J Neurosci 28: 3521-3530, 2008.
32. Puzzo D, Vitolo O, Trinchese F, Jacob JP, Palmeri A, Arancio O. Amyloid-beta peptide inhibits activation of the nitric oxide/cGMP/cAMPresponsive element-binding protein pathway during hippocampal synaptic plasticity. J Neurosci 25: 6887-6897, 2005.
33. Renner M, Lacor PN, Velasco PT, Xu J, Contractor A, Klein WL, Triller A. Deleterious effects of amyloid beta oligomers acting as an extracellular scaffold for mGluR5. Neuron 66: 739-754, 2010.
34. Sakagami Y, Yamamoto K, Sugiura S, Inokuchi K, Hayashi T, Kato N. Essential roles of Homer-1a in homeostatic regulation of pyramidal cell excitability: a possible link to clinical benefits of electroconvulsive shock. Eur J Neurosci 21: 3229-3239, 2005.
35. Saleshando G, O'Connor JJ. SB203580, the p38 mitogen-activated protein kinase inhibitor blocks the inhibitory effect of beta-amyloid on long-term potentiation in the rat hippocampus. Neurosci Lett 288: 119-122, 2000.
36. Selkoe DJ. Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav Brain Res 192: 106-113, 2008.
37. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, Brett FM, Farrell MA, Rowan MJ, Lemere CA, Regan CM, Walsh DM, Sabatini BL, Selkoe DJ. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 14: 837-842, 2008.
38. Small DH, Mok SS, Bornstein JC. Alzheimer's disease and Abeta toxicity: from top to bottom. Nat Rev Neurosci 2: 595-598, 2001.
39. Snyder EM, Nong Y, Almeida CG, Paul S, Moran T, Choi EY, Nairn AC, Salter MW, Lombroso PJ, Gouras GK, Greengard P. Regulation of NMDA receptor trafficking by amyloid-β. Nat Neurosci 8: 1051-1058, 2005.
40. Townsend M, Mehta T, Selkoe DJ. Soluble Abeta inhibits specific signal transduction cascades common to the insulin receptor pathway. J Biol Chem 282: 33305-33312, 2007.
41. Tseng BP, Kitazawa M, LaFerla FM. Amyloid beta-peptide: the inside story. Curr Alzheimer Res 1: 231-239, 2004.
42. Walsh DM, Klyubin I, Fadeeva JV, Cullen WK, Anwyl R, Wolfe MS, Rowan MJ, Selkoe DJ. Naturally secreted oligomers of amyloid β protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416: 535-539, 2002.
43. Wang HY, Lee DH, D'Andrea MR, Peterson PA, Shank RP, Reitz AB. β-Amyloid1-42 binds to alpha7 nicotinic acetylcholine receptor with high affinity. Implications for Alzheimer's disease pathology. J Biol Chem 275: 5626-5632, 2000.
44. Wang Q, Rowan MJ, Anwyl R. 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, 2004b.
45. Wang Q, Walsh DM, Rowan MJ, Selkoe DJ, Anwyl R. 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, 2004a.
46. Wang Q, Wu J, Rowan MJ, Anwyl R. Beta-amyloid inhibition of long-term potentiation is mediated via tumor necrosis factor. Eur J Neurosci 22: 2827-2832, 2005.
47. Winton MJ, Lee EB, Sun E, Wong MM, Leight S, Zhang B, Trojanowski JQ, Lee VM. Intraneuronal APP, not free Aβ peptides in 3xTg-AD mice: implications for tau versus Aβ-mediated Alzheimer neurodegeneration. J Neurosci 31: 7691-7699, 2011.
48. Wirths O, Dins A, Bayer TA. AβPP accumulation and/or intraneuronal amyloid-β accumulation? The 3xTg-AD mouse model revisited. J Alzheimers Dis 28: 897-904, 2012.
49. Wirths O, Multhaup G, Bayer TA. A modified beta-amyloid hypothesis: intraneuronal accumulation of the beta-amyloid peptide-the first step of a fatal cascade. J Neurochem 91: 513-520, 2004.
50. Yamamoto K, Ueta Y, Wang L, Yamamoto R, Inoue N, Inokuchi K, Aiba A, Yonekura H, Kato N. Suppression of a neocortical potassium channel activity by intracellular amyloid-β and its rescue with Homer1a. J Neurosci 31: 11100-11109, 2011.
51. Zhang Y, McLaughlin R, Goodyer C, LeBlanc A. Selective cytotoxicity of intracellular amyloid beta peptide1-42 through p53 and Bax in cultured primary human neurons. J Cell Biol 156: 519-529, 2002.