The prion protein ligand, stress-inducible phosphoprotein 1, regulates amyloid-β oligomer toxicity

Journal of Neuroscience

Volumn 33, Issue 42, 2013, Pages 16552-16564

  Ostapchenko, Valeriy G ^a,b   Beraldo, Flavio H ^a,b   Mohammad, Amro H ^a,b   Xie, Yu Feng ^a,b   Hirata, Pedro H F ^a,c   Magalhaes, Ana C ^a,b   Lamour, Guillaume ^d,e   Li, Hongbin ^d   Maciejewski, Andrzej ^b   Belrose, Jillian C ^a,b   Teixeira, Bianca L ^c   Fahnestock, Margaret ^f   Ferreira, Sergio T ^g   Cashman, Neil R ^e   Hajj, Glaucia N M ^c   Jackson, Michael F ^a,b,h   Choy, Wing Yiu ^b   MacDonald, John F ^a,b   Martins, Vilma R ^c   Prado, Vania F ^a,b   Prado, Marco A M ^a,b   more..

^a ROBARTS RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c A C CAMARGO CANCER CENTER   (Brazil)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^f MCMASTER UNIVERSITY   (Canada)

^g FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^h UNIVERSITY OF MANITOBA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PROTEIN; NICOTINIC RECEPTOR; OLIGOMER; PHOSPHOPROTEIN; STAUROSPORINE; STRESS INDUCIBLE PHOSPHOPROTEIN 1; SYNAPTOPHYSIN; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; AGE; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CELL DEATH; CELL VIABILITY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTROPHYSIOLOGY; EMBRYO; HUMAN; HUMAN CELL; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURFACE PLASMON RESONANCE; SYNAPTIC POTENTIAL; UPREGULATION; WESTERN BLOTTING;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; ASTROCYTES; BRAIN; CELLS, CULTURED; HEAT-SHOCK PROTEINS; HIPPOCAMPUS; MICE; NEURONS; PROTEIN BINDING; PRPC PROTEINS; SIGNAL TRANSDUCTION;

EID: 84885453518     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3214-13.2013     Document Type: Article

References (78)

1. Ambegaokar SS, Jackson GR (2011) Functional genomic screen and network analysis reveal novel modifiers of tauopathy dissociated from tau phosphorylation. Hum Mol Genet 20:4947-4977. CrossRef Medline
2. Balducci C, Beeg M, Stravalaci M, Bastone A, Sclip A, Biasini E, Tapella L, Colombo L, Manzoni C, Borsello T, Chiesa R, Gobbi M, Salmona M, Forloni G (2010) Synthetic amyloid-beta oligomers impair long-term memory independently of cellular prion protein. Proc Natl Acad Sci U S A 107:2295-2300. CrossRef Medline
3. 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. CrossRef Medline
4. Bate C, Williams A (2011) Amyloid-beta-induced synapse damage is mediated via cross-linkage of cellular prion proteins. J Biol Chem 286:37955-37963. CrossRef Medline
5. Benilova I, De Strooper B (2010) Prion protein in Alzheimer's pathogenesis: a hot and controversial issue. EMBO Mol Med 2:289-290. CrossRef Medline
6. Beraldo FH, Soares IN, Goncalves DF, Fan J, Thomas AA, Santos TG, Mohammad AH, Roffé M, Calder MD, Nikolova S, Hajj GN, Guimaraes AL, Massensini AR, Welch I, Betts DH, Gros R, Drangova M, Watson AJ, Bartha R, Prado VF, et al. (2013) Stress-inducible phosphoprotein 1 has unique cochaperone activity during development and regulates cellular response to ischemia via the prion protein. FASEB J 27:3594-3607. CrossRef Medline
7. Beraldo FH, Arantes CP, Santos TG, Queiroz NG, Young K, Rylett RJ, Markus RP, Prado MA, Martins VR (2010) Role of alpha7 nicotinic acetylcholine receptor in calcium signaling induced by prion protein interaction with stress-inducible protein 1. J Biol Chem 285:36542-36550. CrossRef Medline
8. Beraldo FH, Arantes CP, Santos TG, Machado CF, Roffe M, Hajj GN, Lee KS, Magalhães AC, Caetano FA, Mancini GL, Lopes MH, Américo TA, Magdesian MH, Ferguson SS, Linden R, Prado MA, Martins VR (2011) Metabotropic glutamate receptors transduce signals for neurite outgrowth after binding of the prion protein to laminin gamma1 chain. FASEB J 25:265-279. CrossRef Medline
9. Brinker A, Scheufler C, Von Der Mulbe F, Fleckenstein B, Herrmann C, Jung G, Moarefi I, Hartl FU (2002) Ligand discrimination by TPR domains. Relevance and selectivity of EEVD-recognition in Hsp70 x Hop x Hsp90 complexes. J Biol Chem 277:19265-19275. CrossRef Medline
10. Caetano FA, Lopes MH, Hajj GN, Machado CF, Pinto Arantes C, Magalhães AC, Vieira Mde P, Américo TA, Massensini AR, Priola SA, Vorberg I, Gomez MV, Linden R, Prado VF, Martins VR, Prado MA (2008) Endocytosis of prion protein is required for ERK1/2 signaling induced by stress-inducible protein 1. J Neurosci 28:6691-6702. CrossRef Medline
11. Caetano FA, Beraldo FH, Hajj GN, Guimaraes AL, Jürgensen S, Wasilewska-Sampaio AP, Hirata PH, Souza I, Machado CF, Wong DY, De Felice FG, Ferreira ST, Prado VF, Rylett RJ, Martins VR, Prado MA (2011) Amyloid-beta oligomers increase the localization of prion protein at the cell surface. J Neurochem 117:538-553. CrossRef Medline
12. Chen S, Yadav SP, Surewicz WK (2010) Interaction between human prion protein and amyloid-beta (Abeta) oligomers: role OF N-terminal residues. J Biol Chem 285:26377-26383. CrossRef Medline
13. Chiarini LB, Freitas AR, Zanata SM, Brentani RR, Martins VR, Linden R (2002) Cellular prion protein transduces neuroprotective signals. EMBO J 21:3317-3326. CrossRef Medline
14. Chung E, Ji Y, Sun Y, Kascsak RJ, Kascsak RB, Mehta PD, Strittmatter SM, Wisniewski T (2010) Anti-PrPC monoclonal antibody infusion as a novel treatment for cognitive deficits in an Alzheimer's disease model mouse. BMC Neurosci 11:130. CrossRef Medline
15. 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-beta peptide oligomers. J Neurochem 115:1520-1529. CrossRef Medline De
16. Felice FG, Velasco PT, Lambert MP, Viola K, Fernandez SJ, Ferreira ST, Klein WL (2007) Abeta oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J Biol Chem 282:11590-11601. CrossRef Medline De
17. Felice FG, Vieira MN, Bomfim TR, Decker H, Velasco PT, Lambert MP, Viola KL, Zhao WQ, Ferreira ST, Klein WL (2009) Protection of synapses against Alzheimer's-linked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc Natl Acad Sci U S A 106: 1971-1976. CrossRef Medline
18. Dineley KT, Westerman M, Bui D, Bell K, Ashe KH, Sweatt JD (2001) β-Amyloid activates the mitogen-activated protein kinase cascade via hippocampal α7 nicotinic acetylcholine receptors: in vitro and in vivo mechanisms related to Alzheimer's disease. J Neurosci 21:4125-4133. Medline
19. Dziewczapolski G, Glogowski CM, Masliah E, Heinemann SF (2009) Deletion of the α7 nicotinic acetylcholine receptor gene improves cognitive deficits and synaptic pathology in a mouse model of Alzheimer's disease. J Neurosci 29:8805-8815. CrossRef Medline
20. Ferreira ST, Klein WL (2011) The Abeta oligomer hypothesis for synapse failure and memory loss in Alzheimer's disease. Neurobiol Learn Mem 96:529-543. CrossRef Medline
21. Figueiredo CP, Clarke JR, Ledo JH, Ribeiro FC, Costa CV, Melo HM, Mota-Sales AP, Saraiva LM, Klein WL, Sebollela A, De Felice FG, Ferreira ST (2013) Memantine rescues transient cognitive impairment caused by high-molecular-weight abeta oligomers but not the persistent impairment induced by low-molecular-weight oligomers. J Neurosci 33:9626-9634. CrossRef Medline
22. Fischer MJ (2010) Amine coupling through EDC/NHS: a practical approach. Methods Mol Biol 627:55-73. CrossRef Medline
23. Freir DB, Nicoll AJ, Klyubin I, Panico S, Mc Donald JM, Risse E, Asante EA, Farrow MA, Sessions RB, Saibil HR, Clarke AR, Rowan MJ, Walsh DM, Collinge J (2011) Interaction between prion protein and toxic amyloid beta assemblies can be therapeutically targeted at multiple sites. Nat Commun 2:336. CrossRef Medline
24. Gimbel DA, Nygaard HB, Coffey EE, Gunther EC, Laurén J, Gimbel ZA, Strittmatter SM (2010) Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J Neurosci 30:6367-6374. CrossRef Medline
25. Gu Z, Yakel JL (2011) Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity. Neuron 71:155-165. CrossRef Medline
26. Hajj GN, Arantes CP, Dias MV, Roffé M, Costa-Silva B, Lopes MH, Porto-Carreiro I, Rabachini T, Lima FR, Beraldo FH, Prado MM, Linden R, Martins VR (2013) The unconventional secretion of stress-inducible protein 1 by a heterogeneous population of extracellular vesicles. Cell Mol Life Sci 70:3211-3227. CrossRef Medline
27. Hernandez CM, Dineley KT (2012) α7 nicotinic acetylcholine receptors in Alzheimer's disease: neuroprotective, neurotrophic or both? Curr Drug Targets 13:613-622. CrossRef Medline
28. Hernandez CM, Kayed R, Zheng H, Sweatt JD, Dineley KT (2010) Loss of α7 nicotinic receptors enhances β-amyloid oligomer accumulation, exacerbating early-stage cognitive decline and septohippocampal pathology in a mouse model of Alzheimer's disease. J Neurosci 30:2442-2453. CrossRef Medline
29. Hung LW, Ciccotosto GD, Giannakis E, Tew DJ, Perez K, Masters CL, Cappai R, Wade JD, Barnham KJ (2008) Amyloid-α peptide (A+) neurotoxicity is modulated by the rate of peptide aggregation: Aβ dimers and trimers correlate with neurotoxicity. J Neurosci 28:11950-11958. CrossRef Medline
30. Ittner LM, Ke YD, Delerue F, Bi M, Gladbach A, van Eersel J, Wölfing H, Chieng BC, Christie MJ, Napier IA, Eckert A, Staufenbiel M, Hardeman E, Götz J (2010) Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 142:387-397. CrossRef Medline
31. Jankowsky JL, Slunt HH, Ratovitski T, Jenkins NA, Copeland NG, Borchelt DR (2001) Co-expression of multiple transgenes in mouse CNS: a comparison of strategies. Biomol Eng 17:157-165. CrossRef Medline
32. Kessels HW, Nguyen LN, Nabavi S, Malinow R (2010) The prion protein as a receptor for amyloid-beta. Nature 466:E3-E4; discussion E4-E5. CrossRef Medline
33. Khachaturian ZS (1985) Diagnosis of Alzheimer's disease. Arch Neurol 42: 1097-1105. CrossRef Medline
34. Kudo W, Lee HP, Zou WQ, Wang X, Perry G, Zhu X, Smith MA, Petersen RB, Lee HG (2012) Cellular prion protein is essential for oligomeric amyloid-beta-induced neuronal cell death. Hum Mol Genet 21:1138-1144. CrossRef Medline
35. 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 Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci U S A 95:6448-6453. CrossRef Medline
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 Abeta with pathological tau changes in Alzheimer's disease. J Neurosci 32:16857-16871a. CrossRef Medline
37. Laurén J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457:1128-1132. CrossRef Medline
38. Lee KS, Magalhães AC, Zanata SM, Brentani RR, Martins VR, Prado MA (2001) Internalization of mammalian fluorescent cellular prion protein and N-terminal deletion mutants in living cells. J Neurochem 79:79-87. CrossRef Medline
39. 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: 788-801. CrossRef Medline
40. Lima FR, Arantes CP, Muras AG, Nomizo R, Brentani RR, Martins VR (2007) Cellular prion protein expression in astrocytes modulates neuronal survival and differentiation. J Neurochem 103:2164-2176. CrossRef Medline
41. Linden R, Martins VR, Prado MA, Cammarota M, Izquierdo I, Brentani RR (2008) Physiology of the prion protein. Physiol Rev 88:673-728. CrossRef Medline
42. Lopes MH, Hajj GN, Muras AG, Mancini GL, Castro RM, Ribeiro KC, Brentani RR, Linden R, Martins VR (2005) Interaction of cellular prion and stress-inducible protein 1 promotes neuritogenesis and neuroprotection by distinct signaling pathways. J Neurosci 25:11330-11339. CrossRef Medline
43. Magdesian MH, Nery AA, Martins AH, Juliano MA, Juliano L, Ulrich H, Ferreira ST (2005) Peptide blockers of the inhibition of neuronal nicotinic acetylcholine receptors by amyloid beta. J Biol Chem 280:31085-31090. CrossRef Medline
44. Martins VR, Beraldo FH, Hajj GN, Lopes MH, Lee KS, Prado MA, Linden R (2010) Prion protein: orchestrating neurotrophic activities. Curr Issues Mol Biol 12:63-86. Medline
45. Martyn AC, De Jaeger X, Magalhães AC, Kesarwani R, Gonçalves DF, Raulic S, Guzman MS, Jackson MF, Izquierdo I, Macdonald JF, Prado MA, Prado VF (2012) Elimination of the vesicular acetylcholine transporter in the forebrain causes hyperactivity and deficits in spatial memory and long-term potentiation. Proc Natl Acad Sci U S A 109:17651-17656. CrossRef Medline Mc
46. Khann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM (1984) Clinical diagnosis of Alzheimer's disease: report of the NINCDSADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology 34:939-944. CrossRef Medline
47. Michalski B, FahnestockM (2003) Pro-brain-derived neurotrophic factor is decreased in parietal cortex in Alzheimer's disease. Brain Res Mol Brain Res 111:148-154. CrossRef Medline
48. Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394:192-195. CrossRef Medline
49. Mucke L, Selkoe DJ (2012) Neurotoxicity of amyloid beta-protein: synaptic and network dysfunction. Cold Spring Harb Perspect Med 2:a006338. CrossRef Medline
50. Orr-Urtreger A, Göldner FM, Saeki M, Lorenzo I, Goldberg L, De Biasi M, Dani JA, Patrick JW, Beaudet AL (1997) Mice deficient in the α7 neuronal nicotinic acetylcholine receptor lack α-bungarotoxin binding sites and hippocampal fast nicotinic currents. J Neurosci 17:9165-9171. Medline
51. Ostapchenko VG, Makarava N, Savtchenko R, Baskakov IV (2008) The polybasic N-terminal region of the prion protein controls the physical properties of both the cellular and fibrillar forms of PrP. J Mol Biol 383:1210-1224. CrossRef Medline
52. Ostapchenko VG, Beraldo FH, Guimaraes AL, Mishra S, Guzman M, Fan J, Martins VR, Prado VF, Prado MA (2013) Increased prion protein processing and expression of metabotropic glutamate receptor 1 in a mouse model of Alzheimer's disease. J Neurochem. Advance online publication. Retrieved September 12, 2013. doi:10.1111/jnc.12296. CrossRef Medline
53. 2+ release inducing mitochondrial fragmentation in hippocampal neurons and prevent RyR-mediated dendritic spine remodeling produced by BDNF. Antioxid Redox Signal 14:1209-1223. CrossRef Medline
54. Paula-Lima AC, Brito-Moreira J, Ferreira ST (2013) Deregulation of excitatory neurotransmission underlying synapse failure in Alzheimer's disease. J Neurochem 126:191-202. CrossRef Medline
55. Prado VF, Martins-Silva C, de Castro BM, Lima RF, Barros DM, Amaral E, Ramsey AJ, Sotnikova TD, Ramirez MR, Kim HG, Rossato JI, Koenen J, Quan H, Cota VR, Moraes MF, Gomez MV, Guatimosim C, Wetsel WC, Kushmerick C, Pereira GS, Gainetdinov RR, Izquierdo I, Caron MG, Prado MA (2006) Mice deficient for the vesicular acetylcholine transporter are myasthenic and have deficits in object and social recognition. Neuron 51:601-612. CrossRef Medline
56. Querfurth HW, LaFerla FM (2010) Alzheimer's disease. N Engl J Med 362: 329-344. CrossRef Medline
57. Resenberger UK, Harmeier A, Woerner AC, Goodman JL, Müller V, Krishnan R, Vabulas RM, Kretzschmar HA, Lindquist S, Hartl FU, Multhaup G, Winklhofer KF, Tatzelt J (2011) The cellular prion protein mediates neurotoxic signalling of beta-sheet-rich conformers independent of prion replication. EMBO J 30:2057-2070. CrossRef Medline
58. Resenberger UK, Müller V, Munter LM, Baier M, Multhaup G, Wilson MR, Winklhofer KF, Tatzelt J (2012) The heat shock response is modulated by and interferes with toxic effects of scrapie prion protein and amyloid beta. J Biol Chem 287:43765-43776. CrossRef Medline
59. Roffé M, Beraldo FH, Bester R, Nunziante M, Bach C, Mancini G, Gilch S, Vorberg I, Castilho BA, Martins VR, Hajj GN (2010) Prion protein interaction with stress-inducible protein 1 enhances neuronal protein synthesis via mTOR. Proc Natl Acad Sci U S A 107:13147-13152. CrossRef Medline
60. Roffé M, Hajj GN, Azevedo HF, Alves VS, Castilho BA (2013) IMPACT is a developmentally regulated protein in neurons that opposes the eukaryotic initiation factor 2alpha kinase GCN2 in the modulation of neurite outgrowth. J Biol Chem 288:10860-10869. CrossRef Medline
61. Romano SA, Cordeiro Y, Lima LM, Lopes MH, Silva JL, Foguel D, Linden R (2009) Reciprocal remodeling upon binding of the prion protein to its signaling partner hop/STI1. FASEB J 23:4308-4316. CrossRef Medline
62. Santos TG, Beraldo FH, Hajj GN, Lopes MH, Roffe M, Lupinacci FC, Ostapchenko VG, Prado VF, Prado MA, Martins VR (2013) Laminingamma1 chain and stress inducible protein 1 synergistically mediate PrPC-dependent axonal growth via Ca2+ mobilization in dorsal root ganglia neurons. J Neurochem 124:210-223. CrossRef Medline
63. Sebollela A, Freitas-Correa L, Oliveira FF, Paula-Lima AC, Saraiva LM, Martins SM, Mota LD, Torres C, Alves-Leon S, de Souza JM, Carraro DM, Brentani H, De Felice FG, Ferreira ST (2012) Amyloid-beta oligomers induce differential gene expression in adult human brain slices. J Biol Chem 287:7436-7445. CrossRef Medline
64. Shen H, Kihara T, Hongo H, Wu X, Kem WR, Shimohama S, Akaike A, Niidome T, Sugimoto H (2010) Neuroprotection by donepezil against glutamate excitotoxicity involves stimulation of alpha7 nicotinic receptors and internalization of NMDA receptors. Br J Pharmacol 161:127-139. CrossRef Medline
65. 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
66. Solforosi L, Criado JR, McGavern DB, Wirz S, Sánchez-Alavez M, Sugama S, DeGiorgio LA, Volpe BT, Wiseman E, Abalos G, Masliah E, Gilden D, Oldstone MB, Conti B, Williamson RA (2004) Cross-linking cellular prion protein triggers neuronal apoptosis in vivo. Science 303:1514-1516. CrossRef Medline
67. Southworth DR, Agard DA (2011) Client-loading conformation of the Hsp90 molecular chaperone revealed in the cryo-EM structure of the human Hsp90:Hop complex. Mol Cell 42:771-781. CrossRef Medline
68. Townsend M, Shankar GM, Mehta T, Walsh DM, Selkoe DJ (2006) Effects of secreted oligomers of amyloid beta-protein on hippocampal synaptic plasticity: a potent role for trimers. J Physiol 572:477-492. CrossRef Medline
69. Tsutsui S, Hahn JN, Johnson TA, Ali Z, Jirik FR (2008) Absence of the cellular prion protein exacerbates and prolongs neuroinflammation in experimental autoimmune encephalomyelitis. Am J Pathol 173:1029-1041. CrossRef Medline
70. Um JW, Nygaard HB, Heiss JK, Kostylev MA, Stagi M, Vortmeyer A, Wisniewski T, Gunther EC, StrittmatterSM (2012) Alzheimer amyloid-beta oligomer bound to postsynaptic prion protein activates Fyn to impair neurons. Nat Neurosci 15:1227-1235. CrossRef Medline
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. CrossRef Medline
72. Wang HY, Lee DH, D'Andrea MR, Peterson PA, Shank RP, Reitz AB (2000) beta-Amyloid(1-42) binds to alpha7 nicotinic acetylcholine receptor with high affinity. Implications for Alzheimer's disease pathology. J Biol Chem 275:5626-5632. CrossRef Medline
73. Wang HY, Stucky A, Liu J, Shen C, Trocme-Thibierge C, Morain P (2009) Dissociating α-amyloid from α7 nicotinic acetylcholine receptor by a novel therapeutic agent, S 24795, normalizes α7 nicotinic acetylcholine and NMDA receptor function in Alzheimer's disease brain. J Neurosci 29:10961-10973. CrossRef Medline
74. Wang HY, Bakshi K, Frankfurt M, Stucky A, Goberdhan M, Shah SM, Burns LH (2012) Reducing amyloid-related Alzheimer's disease pathogenesis by a small molecule targeting filamin A. J Neurosci 32:9773-9784. CrossRef Medline
75. Xie L, Helmerhorst E, Taddei K, Plewright B, Van Bronswijk W, Martins R (2002) Alzheimer's α-amyloid peptides compete for insulin binding to the insulin receptor. J Neurosci 22:RC221(1-5). Medline
76. You H, Tsutsui S, Hameed S, Kannanayakal TJ, Chen L, Xia P, Engbers JD, Lipton SA, Stys PK, Zamponi GW (2012) Abeta neurotoxicity depends on interactions between copper ions, prion protein, and N-methyl-Daspartate receptors. Proc Natl Acad Sci U S A 109:1737-1742. CrossRef Medline
77. Zanata SM, Lopes MH, Mercadante AF, Hajj GN, Chiarini LB, Nomizo R, Freitas AR, Cabral AL, Lee KS, Juliano MA, de Oliveira E, Jachieri SG, Burlingame A, Huang L, Linden R, Brentani RR, Martins VR (2002) Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J 21:3307-3316. CrossRef Medline
78. Zhang B, Gaiteri C, Bodea LG, Wang Z, McElwee J, Podtelezhnikov AA, Zhang C, Xie T, Tran L, Dobrin R, Fluder E, Clurman B, Melquist S, Narayanan M, Suver C, Shah H, Mahajan M, Gillis T, Mysore J, MacDonald ME, et al. (2013) Integrated systems approach identifies genetic nodes and networks in late-onset Alzheimer's disease. Cell 153:707-720. CrossRef Medline