Reciprocal disruption of neuronal signaling and Aβ production mediated by extrasynaptic NMDA receptors: A downward spiral

Cell and Tissue Research

Volumn 356, Issue 2, 2014, Pages 279-286

  Rush, Travis ^a   Buisson, Alain ^a  

^a GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

Author keywords

Amyloid beta; Amyloid precursor protein; A ; Neuronal signaling; NMDA receptors

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BETA SECRETASE; GLUN2B RECEPTOR; GLUTAMATE RECEPTOR; GLUTAMIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; UNCLASSIFIED DRUG; DOPAMINE RECEPTOR STIMULATING AGENT; MEMANTINE; N-METHYL D-ASPARTATE RECEPTOR SUBTYPE 2A; NR2B NMDA RECEPTOR; SECRETASE;

ALZHEIMER DISEASE; ASTROCYTE; CALCIUM SIGNALING; CELL ACTIVITY; CELL DEATH; CELL DISRUPTION; CELL SURVIVAL; HUMAN; INTRACELLULAR SIGNALING; MOLECULAR PATHOLOGY; NERVE CELL PLASTICITY; NERVE DEGENERATION; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HOMEOSTASIS; PROTEIN PROCESSING; PROTEIN SECRETION; REVIEW; SYNAPTIC TRANSMISSION; AGONISTS; BIOSYNTHESIS; METABOLISM; PATHOLOGY;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; CALCIUM SIGNALING; CELL SURVIVAL; DOPAMINE AGENTS; GLUTAMIC ACID; HUMANS; MEMANTINE; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84902264579     PISSN: 0302766X     EISSN: 14320878     Source Type: Journal    
DOI: 10.1007/s00441-013-1789-1     Document Type: Review

References (74)

1. Atri A, Molinuevo JL, Lemming O, Wirth Y, Pulte I, Wilkinson D (2013) Memantine in patients with Alzheimer's disease receiving donepezil: new analyses of efficacy and safety for combination therapy. Alzheimers Res Ther 5:6-17
2. Barry AE, Klyubin I, Mc Donald JM, Mably AJ, Farrell MA, Scott M, Walsh DM, Rowan MJ (2011) 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
3. Bero AW, Yan P, Roh JH, Cirrito JR, Stewart FR, Raichle ME, Lee J-M, Holtzman DM (2011) Neuronal activity regulates the regional vulnerability to amyloid-β deposition. Nature 14:750-756
4. Bero AW, Bauer AQ, Stewart FR, White BR, Cirrito JR, Raichle ME, Culver JP, Holtzman DM (2012) Bidirectional relationship between functional connectivity and amyloid-β deposition in mouse brain. J Neurosci 32:4334-4340
5. Bordji K, Becerril-Ortega J, Nicole O, Buisson A (2010) Activation of extrasynaptic, but not synaptic, NMDA receptors modifies amyloid precursor protein expression pattern and increases amyloid-β production. J Neurosci 30:15927-15942
6. Buckner RL, Snyder AZ, Shannon BJ, LaRossa G, Sachs R, Fotenos AF, Sheline YI, Klunk WE, Mathis CA, Morris JC, Mintun MA (2005) Molecular, structural, and functional characterization of Alzheimer's disease: evidence for a relationship between default activity, amyloid, and memory. J Neurosci 25:7709-7717 (Pubitemid 41208641)
7. Chatzistavraki M, Kyratzi E, Fotinopoulou A, Papazafiri P, Efthimiopoulos S (2013) Downregulation of AßPP enhances both calcium content of endoplasmic reticulum and acidic stores and the dynamics of store operated calcium channel activity. J Alzheimers Dis 34:407-415
8. Chen HS, Pellegrini JW, Aggarwal SK, Lei SZ, Warach S, Jensen FE, Lipton SA (1992) Open-channel block of N-methyl-D-aspartate (NMDA) responses by memantine: therapeutic advantage against NMDA receptor-mediated neurotoxicity. J Neurosci 12:4427-4436
9. Cheung K-H, Shineman D, Müller M, Cárdenas C, Mei L, Yang J, Tomita T, Iwatsubo T, Lee VM-Y, Foskett JK (2008) Mechanism of Ca2+ disruption in Alzheimer's disease by presenilin regulation of InsP3 receptor channel gating. Neuron 58:871-883 (Pubitemid 351842747)
10. Cirrito JR, Yamada KA, Finn MB, Sloviter RS, Bales KR, May PC, Schoepp DD, Paul SM, Mennerick S, Holtzman DM (2005) Synaptic activity regulates interstitial fluid amyloid-beta levels in vivo. Neuron 48:913-922 (Pubitemid 41814696)
11. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, Ashe KH (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8:79-84 (Pubitemid 41236735)
12. Colvin RA, Bennett JW, Colvin SL, Allen RA, Martinez J, Miner GD (1991) Na+/Ca2+ exchange activity is increased in Alzheimer's disease brain tissues. Brain Res 543:139-147
13. Decker H, Jürgensen S, Adrover MF, Brito-Moreira J, Bomfim TR, Klein WL, Epstein AL, De Felice FG, Jerusalinsky D, Ferreira ST (2010) N-methyl-D-aspartate receptors are required for synaptic targeting of Alzheimer's toxic amyloid-β peptide oligomers. J Neurochem 115:1520-1529
14. Dolev I, Fogel H, Milshtein H, Berdichevsky Y, Lipstein N, Brose N, Gazit N, Slutsky I (2013) Spike bursts increase amyloid-β 40/42 ratio by inducing a presenilin-1 conformational change. Nat Neurosci 16:587-595
15. Ferreira IL, Bajouco LM, Mota SI, Auberson YP, Oliveira CR, Rego AC (2012) Amyloid beta peptide 1-42 disturbs intracellular calcium homeostasis through activation of GluN2B-containing N-methyl-d-aspartate receptors in cortical cultures. Cell Calcium 51:95-106
16. Ferreiro E, Oliveira CR, Pereira C (2004) Involvement of endoplasmic reticulum Ca2+ release through ryanodine and inositol 1,4,5-triphosphate receptors in the neurotoxic effects induced by the amyloid-beta peptide. J Neurosci Res 76:872-880 (Pubitemid 38720693)
17. Gong Y, Chang L, Viola KL, Lacor PN, Lambert MP, Finch CE, Krafft GA, Klein WL (2003) Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci USA 100:10417-10422 (Pubitemid 37071893)
18. Green KN, LaFerla FM (2008) Linking calcium to Abeta and Alzheimer's disease. Neuron 59:190-194 (Pubitemid 352033693)
19. Grynspan F, Griffin WR, Cataldo A, Katayama S, Nixon RA (1997) Active site-directed antibodies identify calpain II as an early-appearing and pervasive component of neurofibrillary pathology in Alzheimer's disease. Brain Res 763:145-158 (Pubitemid 27364434)
20. Hardingham GE, Bading H (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11:682-696
21. Hardingham GE, Fukunaga Y, Bading H (2002) Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 5:405-414 (Pubitemid 34454245)
22. Hardy J (2006) Alzheimer's disease: the amyloid cascade hypothesis: an update and reappraisal. J Alzheimers Dis 9:151-153
23. Hardy JA, Higgins GA (1992) Alzheimer's disease: the amyloid cascade hypothesis. Science 256:184-185
24. Hoey SE, Williams RJ, Perkinton MS (2009) Synaptic NMDA receptor activation stimulates alpha-secretase amyloid precursor protein processing and inhibits amyloid-beta production. J Neurosci 29:4442-4460
25. Hoozemans JJMJ, Veerhuis RR, Rozemuller JMJ, Eikelenboom PP (2011) Soothing the inflamed brain: effect of non-steroidal anti-inflammatory drugs on Alzheimer's disease pathology. CNS Neurol Disord Drug Targets 10:57-67
26. Hu N-W, Klyubin I, Anwyl R, Anwy R, Rowan MJ (2009) GluN2B subunit-containing NMDA receptor antagonists prevent Abeta-mediated synaptic plasticity disruption in vivo. Proc Natl Acad Sci USA 106:20504-20509
27. Hussain I, Powell D, Howlett DR, Tew DG, Meek TD, Chapman C, Gloger IS, Murphy KE, Southan CD, Ryan DM, Smith TS, Simmons DL, Walsh FS, Dingwall C, Christie G (1999) Identification of a novel aspartic protease (Asp 2) as beta-secretase. Mol Cell Neurosci 14:419-427 (Pubitemid 30026585)
28. Kabogo D, Rauw G, Amritraj A, Baker G, Kar S (2010) β-amyloid- related peptides potentiate K+-evoked glutamate release from adult rat hippocampal slices. Neurobiol Aging 31:1164-1172
29. Kamenetz F, Tomita T, Hsieh H, Seabrook G, Borchelt D, Iwatsubo T, Sisodia S, Malinow R (2003) APP processing and synaptic function. Neuron 37:925-937 (Pubitemid 36398299)
30. Kervern M, Angeli A, Nicole O, Léveillé F, Parent B, Villette V, Buisson A, Dutar P (2012) Selective impairment of some forms of synaptic plasticity by oligomeric amyloid-β peptide in the mouse hippocampus: implication of extrasynaptic NMDA receptors. J Alzheimers Dis 32:183-196
31. Kessels HW, Nabavi S, Malinow R (2013) Metabotropic NMDA receptor function is required for β-amyloid-induced synaptic depression. Proc Natl Acad Sci USA 110:4033-4038
32. Khachaturian ZS (1987) Hypothesis on the regulation of cytosol calcium concentration and the aging brain. Neurobiol Aging 8:345-346
33. Kirischuk S, Verkhratsky A (1996) Calcium homeostasis in aged neurones. Life Sci 59:451-459 (Pubitemid 26246900)
34. Kirischuk S, Pronchuk N, Verkhratsky A (1992) Measurements of intracellular calcium in sensory neurons of adult and old rats. Neuroscience 50:947-951
35. Kotermanski SE, Johnson JW (2009) Mg2+ imparts NMDA receptor subtype selectivity to the Alzheimer's drug memantine. J Neurosci 29:2774-2779
36. Larson M, Sherman MA, Amar F, Nuvolone M, Schneider JA, Bennett DA, Aguzzi A, Lesné SE (2012) The complex PrP(c)-Fyn couples human oligomeric Aβ with pathological tau changes in Alzheimer's disease. J Neurosci 32:16857-71a
37. Leissring MA, Paul BA, Parker I, Cotman CW, LaFerla FM (1999) Alzheimer's presenilin-1 mutation potentiates inositol 1,4,5-trisphosphate-mediated calcium signaling in Xenopus oocytes. J Neurochem 72:1061-1068 (Pubitemid 29085020)
38. Lesné S, Ali C, Gabriel C, Croci N, MacKenzie ET, Glabe CG, Plotkine M, Marchand-Verrecchia C, Vivien D, Buisson A (2005) NMDA receptor activation inhibits alpha-secretase and promotes neuronal amyloid-beta production. J Neurosci 25:9367-9377 (Pubitemid 41464749)
39. Leveille F, Gaamouch El F, Gouix E, Lecocq M, Lobner D, Nicole O, Buisson A (2008) Neuronal viability is controlled by a functional relation between synaptic and extrasynaptic NMDA receptors. FASEB J 22:4258-4271
40. Li S, Hong S, Shepardson NE, Walsh DM, Shankar GM, Selkoe D (2009) Soluble oligomers of amyloid β protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 62:788-801
41. Li S, Jin M, Koeglsperger T, Shepardson NE, Shankar GM, Selkoe DJ (2011) Soluble Aβ oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J Neurosci 31:6627-6638
42. Liu S-J, Gasperini R, Foa L, Small DH (2010) Amyloid-beta decreases cell-surface AMPA receptors by increasing intracellular calciumand phosphorylation of GluR2. J Alzheimers Dis 21:655-666
43. Lopez JR, Lyckman A, Oddo S, LaFerla FM, Querfurth HW, Shtifman A (2008) Increased intraneuronal resting [Ca2+] in adult Alzheimer's disease mice. J Neurochem 105:262-271 (Pubitemid 351441642)
44. Mackenzie IRI, Miller LAL (1993) Senile plaques in temporal lobe epilepsy. Acta Neuropathol 87:504-510
45. Marcello E, Gardoni F, Mauceri D, Romorini S, Jeromin A, Epis R, Borroni B, Cattabeni F, Sala C, Padovani A, Di Luca M (2007) Synapse-associated protein-97 mediates alpha-secretase ADAM10 trafficking and promotes its activity. J Neurosci 27:1682-1691 (Pubitemid 46280085)
46. Martinez-Coria H, Green KN, Billings LM, Kitazawa M, Albrecht M, Rammes G, Parsons CG, Gupta S, Banerjee P, LaFerla FM (2010) Memantine improves cognition and reduces Alzheimer's-like neuropathology in transgenic mice. Am J Pathol 176:870-880
47. McLean CAC, Cherny RAR, Fraser FWF, Fuller SJS, Smith MJM, Beyreuther KK, Bush AIA, Masters CLC (1999) Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 46:860-866
48. Miñano-Molina AJ, España J, Martín E, Barneda-Zahonero B, Fadó R, Solé M, Trullás R, Saura CA, Rodríguez-Alvarez J (2011) Soluble oligomers of amyloid-β peptide disrupt membrane trafficking of α-amino-3-hydroxy-5-methylisoxazole-4- propionic acid receptor contributing to early synapse dysfunction. J Biol Chem 286:27311-27321
49. Moon M, Hong HS, Nam DW, Baik SH, Song H, Kook S-Y, Kim YS, Lee J, Mook-Jung I (2012) Intracellular amyloid-β accumulation in calcium-binding protein-deficient neurons leads to amyloid-β plaque formation in animal model of Alzheimer's disease. J Alzheimers Dis 29:615-628
50. Oulès B, Del Prete D, Greco B, Zhang X, Lauritzen I, Sevalle J, Moreno S, Paterlini-Bréchot P, Trebak M, Checler F, Benfenati F, Chami M (2012) Ryanodine receptor blockade reduces amyloid-β load and memory impairments in Tg2576 mouse model of Alzheimer disease. J Neurosci 32:11820-11834
51. Palop JJ, Chin J, Roberson ED, Wang J, Thwin MT, Bien-Ly N, Yoo J, Ho KO, Yu G-Q, 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 (Pubitemid 47321079)
52. Paula-Lima AC, Adasme T, SanMartín C, Sebollela A, Hetz C, Carrasco MA, Ferreira ST, Hidalgo C (2011) Amyloid β-peptide oligomers stimulate RyR-mediated Ca2+ release inducing mitochondrial fragmentation in hippocampal neurons and prevent RyR-mediated dendritic spine remodeling produced by BDNF. Antioxid Redox Signal 14:1209-1223
53. Querfurth HW, Selkoe DJ (1994) Calcium ionophore increases amyloid beta peptide production by cultured cells. Biochemistry 33:4550-4561 (Pubitemid 24145103)
54. Roh JH, Huang Y, Bero AW, Kasten T, Stewart FR, Bateman RJ, Holtzman DM (2012) Disruption of the sleep-wake cycle and diurnal fluctuation of β-amyloid in mice with Alzheimer's disease pathology. Sci Transl Med 4:150-122
55. Rönicke R, Mikhaylova M, Rönicke S, Meinhardt J, Schröder UH, Fändrich M, Reiser G, Kreutz MR, Reymann KG (2011) Early neuronal dysfunction by amyloid â oligomers depends on activation of NR2B-containing NMDA receptors. Neurobiol Aging 32:2219-2228
56. Sepulveda FJ, Parodi J, Peoples RW, Opazo C, Aguayo LG (2010) Synaptotoxicity of Alzheimer beta amyloid can be explained by its membrane perforating property. PLoS ONE 5:e11820
57. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL (2007) Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 27:2866-2875 (Pubitemid 46438992)
58. Soriano FX, Hardingham GE (2007) Compartmentalized NMDA receptor signalling to survival and death. J Physiol Lond 584:381-387 (Pubitemid 47578325)
59. Stutzmann GE (2004) Dysregulated IP3 signaling in cortical neurons of knock-in mice expressing an Alzheimer's-linked mutation in presenilin1 results in exaggerated Ca2+ signals and altered membrane excitability. J Neurosci 24:508-513
60. Stutzmann GE, Smith I, Caccamo A, Oddo S, LaFerla FM, Parker I (2006) Enhanced ryanodine receptor recruitment contributes to Ca2+ disruptions in young, adult, and aged Alzheimer's disease mice. J Neurosci 26:5180-5189 (Pubitemid 44315299)
61. Tackenberg C, Grinschgl S, Trutzel A, Santuccione AC, Frey MC, Konietzko U, Grimm J, Brandt R, Nitsch RM (2013) NMDA receptor subunit composition determines beta-amyloid-induced neurodegeneration and synaptic loss. Cell Death Dis 4:e608
62. Talantova M et al (2013) Aβ induces astrocytic glutamate release, extrasynaptic NMDA receptor activation, and synaptic loss. Proc Natl Acad Sci USA 110:E2518-E2527
63. Tamburri A, Dudilot A, Licea S, Bourgeois C, Boehm J (2012) NMDA-Receptor activation but not ion flux is required for amyloid-beta induced synaptic depression. PLoS ONE 8:e65350-e65350
64. Tampellini D, Rahman N, Lin MT, Capetillo-Zarate E, Gouras GK (2011) Impaired β-amyloid secretion in Alzheimer's disease pathogenesis. J Neurosci 31:15384-15390
65. Texidó L, Martín-Satué M, Alberdi E, Solsona C, Matute C (2011) Amyloid β peptide oligomers directly activate NMDA receptors. Cell Calcium 49:184-190
66. Ulrich JD, Burchett JM, Restivo JL, Schuler DR, Verghese PB, Mahan TE, Landreth GE, Castellano JM, Jiang H, Cirrito JR, Holtzman DM (2013) In vivo measurement of apolipoprotein E from the brain interstitial fluid using microdialysis. Mol Neurodegener 8:13-19
67. Vanhoutte P, Bading H (2003) Opposing roles of synaptic and extrasynaptic NMDA receptors in neuronal calcium signalling and BDNF gene regulation. Curr Opin Neurobiol 13:366-371 (Pubitemid 36792249)
68. Verges DK, Restivo JL, Goebel WD, Holtzman DM, Cirrito JR (2011) Opposing synaptic regulation of amyloid-β metabolism by NMDA receptors in vivo. J Neurosci 31:11328-11337
69. Verkhratsky A, Olabarria M, Noristani HN, Yeh C-Y, Rodriguez JJ (2010) Astrocytes in Alzheimer's disease. Neurotherapeutics 7:399-412
70. Walsh DM, Hartley DM, Condron MM, Selkoe DJ, Teplow DB (2001) In vitro studies of amyloid beta-protein fibril assembly and toxicity provide clues to the aetiology of Flemish variant (Ala692-Gly) Alzheimer's disease. Biochem J 355:869-877 (Pubitemid 32434107)
71. 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 long-term potentiation in vivo. Nature 416:535-539 (Pubitemid 34288854)
72. Wu B, Yamaguchi H, Lai FA, Shen J (2013) Presenilins regulate calcium homeostasis and presynaptic function via ryanodine receptors in hippocampal neurons. Proc Natl Acad Sci USA 110:15091-15096
73. Yoo AS, Cheng I, Chung S, Grenfell TZ, Lee H, Pack-Chung E, Handler M, Shen J, Xia W, Tesco G, Saunders AJ, Ding K, Frosch MP, Tanzi RE, Kim TW (2000) Presenilin-mediated modulation of capacitative calcium entry. Neuron 27:561-572
74. Zeiger W, Vetrivel KS, Buggia-Prévot V, Nguyen PD, Wagner SL, Villereal ML, Thinakaran G (2013) Ca2+ influx through storeoperated Ca2+ channels reduces Alzheimer disease β-amyloid peptide secretion. J Biol Chem 288:26955-26966