Intracellular accumulation of amyloid-β (Aβ) protein plays a major role in Aβ-induced alterations of glutamatergic synaptic transmission and plasticity

Journal of Neuroscience

Volumn 34, Issue 38, 2014, Pages 12893-12903

  Ripoli, Cristian ^a   Cocco, Sara ^a   Li Puma, Domenica D ^a   Piacentini, Roberto ^a   Mastrodonato, Alessia ^a   Scala, Federico ^a   Puzzo, Daniela ^b   D’Ascenzo, Marcello ^a   Grassi, Claudio ^a  

^a CATHOLIC UNIVERSITY   (Italy)

^b UNIVERSITY OF CATANIA   (Italy)

Author keywords

6E10; Amyloid protein; Autaptic hippocampal neurons; Intraneuronal accumulation; Synaptic transmission; Whole cell LTP

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4', 6 DIAMIDINO 2 PHENYLINDOLE; AMPA RECEPTOR; AMYLIN; AMYLOID BETA PROTEIN [1-40]; AMYLOID BETA PROTEIN [1-42]; ENHANCED GREEN FLUORESCENT PROTEIN; FLUORESCEIN ISOTHIOCYANATE; MICROTUBULE ASSOCIATED PROTEIN 2; MONOCLONAL ANTIBODY; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); GLUTAMIC ACID; PEPTIDE FRAGMENT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS ASSAY; ARTICLE; BIOACCUMULATION; BRAIN ELECTROPHYSIOLOGY; CELL SUSPENSION; CONTROLLED STUDY; DENDRITIC SPINE; EXTRACELLULAR SPACE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL NEURONAL CULTURE; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INTERNALIZATION; INTRACELLULAR SIGNALING; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; MOUSE; NERVE CELL PLASTICITY; NICK END LABELING; NONHUMAN; PATCH CLAMP TECHNIQUE; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SYNAPTIC TRANSMISSION; WESTERN BLOTTING; 6E10; AMYLOID-Β PROTEIN; ANIMAL; AUTAPTIC HIPPOCAMPAL NEURONS; DRUG EFFECT; EXCITATORY POSTSYNAPTIC POTENTIAL; HIPPOCAMPUS; INTRACELLULAR SPACE; INTRANEURONAL ACCUMULATION; METABOLISM; MICROINJECTION; PHYSIOLOGY; PRIMARY CELL CULTURE; WHOLE-CELL LTP;

6E10; AMYLOID-Β PROTEIN; AUTAPTIC HIPPOCAMPAL NEURONS; INTRANEURONAL ACCUMULATION; SYNAPTIC TRANSMISSION; WHOLE-CELL LTP;

AMYLOID BETA-PEPTIDES; ANIMALS; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; INTRACELLULAR SPACE; LONG-TERM POTENTIATION; MALE; MICE; MICROINJECTIONS; NEURONAL PLASTICITY; PEPTIDE FRAGMENTS; PRIMARY CELL CULTURE; SYNAPTIC TRANSMISSION;

EID: 84907149261     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1201-14.2014     Document Type: Article

References (62)

1. Almeida CG, Tampellini D, Takahashi RH, Greengard P, Lin MT, Snyder EM, Gouras GK (2005) Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol Dis 20:187-198. CrossRef Medline
2. Attar A, Ripoli C, Riccardi E, Maiti P, Li Puma DD, Liu T, Hayes J, Jones MR, Lichti-Kaiser K, Yang F, Gale GD, Tseng CH, Tan M, Xie CW, Straudinger JL, Klärner FG, Schrader T, Frautschy SA, Grassi C, Bitan G (2012) Protection of primary neurons and mouse brain from Alzheimer’s pathology by molecular tweezers. Brain 135:3735-3748. CrossRef Medline
3. Bayer TA, Wirths O (2010) Intracellular accumulation of amyloid-beta-a predictor for synaptic dysfunction and neuron loss in Alzheimer’s disease. Front Aging Neurosci 2:8. CrossRef Medline
4. Benilova I, De Strooper B (2013) Neuroscience. Promiscuous Alzheimer’s amyloid: yet another partner. Science 341:1354-1355. CrossRef Medline
5. Benilova I, Karran E, De Strooper B (2012) The toxic Aβ oligomer and Alzheimer’s disease: an emperor in need of clothes. Nat Neurosci 15:349-357. CrossRef Medline
6. 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. CrossRef Medline
7. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM (2005) Intraneuronal Aβ causes the onset of early Alzheimer’s disease-related cognitive deficits in transgenic mice. Neuron 45:675-688. CrossRef Medline
8. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39. CrossRef Medline
9. Bonda DJ, Lee HP, Lee HG, Friedlich AL, Perry G, Zhu X, Smith MA (2010) Novel therapeutics for Alzheimer’s disease: an update. Curr Opin Drug Discov Devel 13:235-246. Medline
10. Cissé M, Halabisky B, Harris J, Devidze N, Dubal DB, Sun B, Orr A, Lotz G, Kim DH, Hamto P, Ho K, Yu GQ, Mucke L (2011) Reversing EphB2 depletion rescues cognitive functions in Alzheimer model. Nature 469: 47-52. CrossRef Medline
11. Clementi ME, Pezzotti M, Orsini F, Sampaolese B, Mezzogori D, Grassi C, Giardina B, Misiti F (2006) Alzheimer’s amyloid β-peptide (1-42) in-duces cell death in human neuroblastoma via bax/bcl-2 ratio increase: an intriguing role for methionine 35. Biochem Biophys Res Commun 342: 206-213. CrossRef Medline
12. De Chiara G, Marcocci ME, Civitelli L, Argnani R, Piacentini R, Ripoli C, Manservigi R, Grassi C, Garaci E, Palamara AT (2010) APP processing induced by herpes simplex virus type 1 (HSV-1) yields several APP fragments in human and rat neuronal cells. PLoS One 5:e13989. CrossRef Medline
13. De Stefano ME, Leone L, Lombardi L, Paggi P (2005) Lack of dystrophin leads to the selective loss of superior cervical ganglion neurons projecting to muscular targets in genetically dystrophic mdx mice. Neurobiol Dis 20:929-942. CrossRef Medline
14. Dineley KT, Westerman M, Bui D, Bell K, Ashe KH, Sweatt JD (2001) Betaamyloid activates the mitogen-activated protein kinase cascade via hippocampal alpha7 nicotinic acetylcholine receptors: in vitro and in vivo mechanisms related to Alzheimer’s disease. J Neurosci 21:4125-4133. Medline
15. Dougherty JJ, Wu J, Nichols RA (2003) Beta-amyloid regulation of presynaptic nicotinic receptors in rat hippocampus and neocortex. J Neurosci 23:6740-6747. Medline
16. Eimer WA, Vassar R (2013) Neuron loss in the 5XFAD mouse model of Alzheimer’s disease correlates with intraneuronal Aβ42 accumulation and Caspase-3 activation. Mol Neurodegener 8:2. CrossRef Medline
17. Fusco S, Ripoli C, Podda MV, Ranieri SC, Leone L, Toietta G, McBurney MW, Schutz G, Riccio A, Grassi C, Galeotti T, Pani G (2012) A role for neuronal cAMP Responsive Element Binding (CREB)-1 in brain responses to calorie restriction. Proc Natl Acad Sci U S A 109:621-626. CrossRef Medline
18. Gouras GK, Tsai J, Naslund J, Vincent B, Edgar M, Checler F, Greenfield JP, Haroutunian V, Buxbaum JD, Xu H, Greengard P, Relkin NR (2000) Intraneuronal Aβ42 accumulation in human brain. Am J Pathol 156:15-20. CrossRef Medline
19. Gouras GK, Tampellini D, Takahashi RH, Capetillo-Zarate E (2010) Intraneuronal beta-amyloid accumulation and synapse pathology in Alzheimer’s disease. Acta Neuropathol 119:523-541. CrossRef Medline
20. Gouras GK, Willén K, Tampellini D (2012) Critical role of intraneuronal Aβ in Alzheimer’s disease: technical challenges in studying intracellular Aβ. Life Sci 91:1153-1158. CrossRef Medline
21. Hashimoto M, Bogdanovic N, Volkmann I, Aoki M, Winblad B, Tjernberg LO (2010) Analysis of microdissected human neurons by a sensitive ELISA reveals a correlation between elevated intracellular concentrations of Abeta42 and Alzheimer’s disease neuropathology. Acta Neuropathol 119:543-554. CrossRef Medline
22. Hu X, Crick SL, Bu G, Frieden C, Pappu RV, Lee JM (2009) Amyloid seeds formed by cellular uptake, concentration, and aggregation of the amyloid-beta peptide. Proc Natl Acad Sci U S A 106:20324-20329. CrossRef Medline
23. Jo J, Whitcomb DJ, Olsen KM, Kerrigan TL, Lo SC, Bru-Mercier G, Dickinson B, Scullion S, Sheng M, Collingridge G, Cho K (2011) Aβ(1-42) inhibition of LTP is mediated by a signaling pathway involving caspase-3, Akt1 and GSK-3β. Nat Neurosci 14:545-547. CrossRef Medline
24. Kim T, Vidal GS, Djurisic M, William CM, Birnbaum ME, Garcia KC, Hyman BT, Shatz CJ (2013) Human LilrB2 is a β-amyloid receptor and its murine homolog PirB regulates synaptic plasticity in an Alzheimer’s model. Science 341:1399-1404. CrossRef Medline
25. Kimura R, MacTavish D, Yang J, Westaway D, Jhamandas JH (2012) Beta amyloid-induced depression of hippocampal long-term potentiation is mediated through the amylin receptor. J Neurosci 32:17401-17406. CrossRef Medline
26. Kuszczyk MA, Sanchez S, Pankiewicz J, Kim J, Duszczyk M, Guridi M, Asuni AA, Sullivan PM, Holtzman DM, Sadowski MJ (2013) Blocking the interaction between apolipoprotein E and Aβ reduces intraneuronal accumulation of Aβ and inhibits synaptic degeneration. Am J Pathol 182: 1750-1768. CrossRef Medline
27. LaFerla FM, Green KN, Oddo S (2007) Intracellular amyloid-β in Alzheimer’s disease. Nat Rev Neurosci 8:499-509. CrossRef Medline
28. Li S, Jin M, Zhang D, Yang T, Koeglsperger T, Fu H, Selkoe DJ (2013) Environmental novelty activates β2-adrenergic signaling to prevent the impairment of hippocampal LTP by Aβ oligomers. Neuron 77:929-941. CrossRef Medline
29. Liu Q, Kawai H, Berg DK (2001) beta-Amyloid peptide blocks the response of alpha 7-containing nicotinic receptors on hippocampal neurons. Proc Natl Acad Sci U S A 98:4734-4739. CrossRef Medline
30. Lorenzo A, Yuan M, Zhang Z, Paganetti PA, Sturchler-Pierrat C, Staufenbiel M, Mautino J, Vigo FS, Sommer B, Yankner BA (2000) Amyloid beta interacts with the amyloid precursor protein: a potential toxic mechanism in Alzheimer’s disease. Nat Neurosci 3:460-464. CrossRef Medline
31. Lustbader JW, Cirilli M, Lin C, Xu HW, Takuma K, Wang N, Caspersen C, Chen X, Pollak S, Chaney M, Trinchese F, Liu S, Gunn-Moore F, Lue LF, Walker DG, Kuppusamy P, Zewier ZL, Arancio O, Stern D, Yan SS, et al. (2004) ABAD directly links Aβ to mitochondrial toxicity in Alzheimer’s disease. Science 304:448-452. CrossRef Medline
32. Maiti P, Piacentini R, Ripoli C, Grassi C, Bitan G (2011) Surprising toxicity and assembly behaviour of amyloid β-protein oxidized to sulfone. Biochem J 433:323-332. CrossRef Medline
33. Malenka RC, Malinow R (2011) Alzheimer’s disease: recollection of lost memories. Nature 469:44-45. CrossRef Medline
34. Moreno H, Yu E, Pigino G, Hernandez AI, Kim N, Moreira JE, Sugimori M, Llinás RR (2009) Synaptic transmission block by presynaptic injection of oligomeric amyloid beta. Proc Natl Acad Sci U S A 106:5901-5906. CrossRef Medline
35. Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY, Malinow R (2014) Engineering a memory with LTD and LTP. Nature 511:348-352. CrossRef Medline
36. Nagele RG, D’Andrea MR, Anderson WJ, Wang HY (2002) Intracellular accumulation of beta-amyloid (1-42) in neurons is facilitated by the alpha 7 nicotinic acetylcholine receptor in Alzheimer’s disease. Neuroscience 110:199-211. CrossRef Medline
37. Nomura I, Takechi H, Kato N (2012) Intraneuronally injected amyloid β inhibits long-term potentiation in rat hippocampal slices. J Neurophysiol 107:2526-2531. CrossRef Medline
38. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y (1997) ‘Green mice’ as a source of ubiquitous green cells. FEBS Lett 407:313-319. CrossRef Medline
39. Origlia N, Arancio O, Domenici L, Yan SS (2009a) MAPK, beta-amyloid and synaptic dysfunction: the role of RAGE. Expert Rev Neurother 9:1635-1645. CrossRef Medline
40. Origlia N, Capsoni S, Cattaneo A, Fang F, Arancio O, Yan SD, Domenici L (2009b) Abeta-dependent Inhibition of LTP in different intracortical circuits of the visual cortex: the role of RAGE. J Alzheimers Dis 17:59-68. CrossRef Medline
41. Parihar MS, Brewer GJ (2010) Amyloid β as a modulator of synaptic plasticity. J Alzheimers Dis 22:741-763. CrossRef Medline
42. Pettit DL, Shao Z, Yakel JL (2001) β-Amyloid (1-42) peptide directly modulates nicotinic receptors in the rat hippocampal slice. J Neurosci 21: RC120. Medline
43. Piacentini R, Ripoli C, Leone L, Misiti F, Clementi ME, D’Ascenzo M, Giardina B, Azzena GB, Grassi C (2008a) Role of methionine 35 in the intracellular Ca 2 homeostasis dysregulation and Ca 2-dependent apoptosis induced by amyloid β-peptide in human neuroblastoma IMR32 cells. J Neurochem 107:1070-1082. CrossRef Medline
44. Piacentini R, Gangitano C, Ceccariglia S, Del Fà A, Azzena GB, Michetti F, Grassi C (2008b) Dysregulation of intracellular calcium homeostasis is responsible for neuronal death in an experimental model of selective hippocampal degeneration induced by trimethyltin. J Neurochem 105: 2109-2121. CrossRef Medline
45. Podda MV, D’Ascenzo M, Leone L, Piacentini R, Azzena GB, Grassi C (2008) Functional role of cyclic nucleotide-gated channels in rat medial vestibular nucleus neurons. J Physiol 586:803-815. Medline
46. Podda MV, Leone L, Piacentini R, Cocco S, Mezzogori D, D’Ascenzo M, Grassi C (2012) Expression of olfactory-type cyclic nucleotide-gated channels in rat cortical astrocytes. Glia 60:1391-1405. CrossRef Medline
47. Podda MV, Leone L, Barbati SA, Mastrodonato A, Li Puma DD, Piacentini R, Grassi C (2014) Extremely low-frequency electromagnetic fields enhance the survival of newborn neurons in the mouse hippocampus. Eur J Neurosci 39:893-903. CrossRef Medline
48. Ripoli C, Piacentini R, Riccardi E, Leone L, Li Puma DD, Bitan G, Grassi C (2013) Effects of different amyloid β-protein analogues on synaptic function. Neurobiol Aging 34:1032-1044. CrossRef Medline
49. Russell CL, Semerdjieva S, Empson RM, Austen BM, Beesley PW, Alifragis P (2012) Amyloid-β acts as a regulator of neurotransmitter release disrupting the interaction between synaptophysin and VAMP2. PLoS One 7:e43201. CrossRef Medline
50. Selkoe DJ (2002) Alzheimer’s disease is a synaptic failure. Science 298:789-791. CrossRef Medline
51. Shaked GM, Kummer MP, Lu DC, Galvan V, Bredesen DE, Koo EH (2006) Abeta induces cell death by direct interaction with its cognate extracellular domain on APP (APP 597-624). FASEB J 20:1254-1256. CrossRef Medline
52. Small DH, Maksel D, Kerr ML, Ng J, Hou X, Chu C, Mehrani H, Unabia S, Azari MF, Loiacono R, Aguilar MI, Chebib M (2007) The β-amyloid protein of Alzheimer’s disease binds to membrane lipids but does not bind to the alpha7 nicotinic acetylcholine receptor. J Neurochem 101: 1527-1538. CrossRef Medline
53. Snyder EM, Nong Y, Almeida CG, Paul S, Moran T, Choi EY, Nairn AC, Salter MW, Lombroso PJ, Gouras GK, Greengard P (2005) Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci 8:1051-1058. CrossRef Medline
54. Takahashi RH, Capetillo-Zarate E, Lin MT, Milner TA, Gouras GK (2010) Co-occurrence of Alzheimer’s disease β-amyloid and tau pathologies at synapses. Neurobiol Aging 31:1145-1152. CrossRef Medline
55. Talantova M, Sanz-Blasco S, Zhang X, Xia P, Akhtar MW, Okamoto S, Dziewczapolski G, Nakamura T, Cao G, Pratt AE, Kang YJ, Tu S, Molokanova E, McKercher SR, Hires SA, Sason H, Stouffer DG, Buczynski MW, Solomon JP, Michael S, et al. (2013) Aβ induces astrocytic glutamate release, extrasynaptic NMDA receptor activation, and synaptic loss. Proc Natl Acad Sci U S A 110:E2518-E2527. CrossRef Medline
56. Tampellini D, Magrané J, Takahashi RH, Li F, Lin MT, Almeida CG, Gouras GK (2007) Internalized antibodies to the Aβ domain of APP reduce neuronal Aβ and protect against synaptic alterations. J Biol Chem 282: 18895-18906. CrossRef Medline
57. Ting JT, Kelley BG, Sullivan JM (2006) Synaptotagmin IV does not alter excitatory fast synaptic transmission or fusion pore kinetics in mammalian CNS neurons. J Neurosci 26:372-380. CrossRef Medline
58. Ting JT, Kelley BG, Lambert TJ, Cook DG, Sullivan JM (2007) Amyloid precursor protein overexpression depresses excitatory transmission through both presynaptic and postsynaptic mechanisms. Proc Natl Acad Sci U S A 104:353-358. CrossRef Medline
59. Wang HY, Lee DH, Davis CB, Shank RP (2000) Amyloid peptide Abeta(1-42) binds selectively and with picomolar affinity to alpha7 nicotinic acetylcholine receptors. J Neurochem 75:1155-1161. Medline
60. Wang Q, Walsh DM, Rowan MJ, Selkoe DJ, Anwyl R (2004) Block of longterm potentiation by naturally secreted and synthetic amyloid betapeptide in hippocampal slices is mediated via activation of the kinases c-Jun N-terminal kinase, cyclin-dependent kinase 5, and p38 mitogenactivated protein kinase as well as metabotropic glutamate receptor type 5. J Neurosci 24:3370-3378. CrossRef Medline
61. Wei W, Nguyen LN, Kessels HW, Hagiwara H, Sisodia S, Malinow R (2010) Amyloid beta from axons and dendrites reduces local spine number and plasticity. Nat Neurosci 13:190-196. CrossRef Medline
62. Zepa L, Frenkel M, Belinson H, Kariv-Inbal Z, Kayed R, Masliah E, Michaelson DM (2011) ApoE4-driven accumulation of intraneuronal oligomerized Aβ42 following activation of the amyloid cascade in vivo is mediated by a gain of function. Int J Alzheimers Dis 2011:792070. CrossRef. Medline