Glimepiride protects neurons against amyloid-β-induced synapse damage

Neuropharmacology

Volumn 101, Issue , 2016, Pages 225-236

  Osborne, Craig ^a   West, Ewan ^a   Nolan, William ^a   McHale Owen, Harriet ^a   Williams, Alun ^b   Bate, Clive ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Alzheimer's disease; Amyloid ; Glimepiride; Glycosylphosphatidylinositols; Phospholipase A2; Prion; Synapses; Synaptophysin

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; CHOLESTEROL; CYSTEINE STRING PROTEIN; CYTOPLASMIC PHOSPHOLIPASE A2; GANGLIOSIDE; GLIMEPIRIDE; GLYCOSYLPHOSPHATIDYLINOSITOL ANCHORED PROTEIN; PHOSPHOLIPASE A2; PRION PROTEIN; SYNAPSIN I; SYNAPTOPHYSIN; UNCLASSIFIED DRUG; AMYLOID BETA-PROTEIN (1-42); IMMUNOSUPPRESSIVE AGENT; PEPTIDE FRAGMENT; PRION; SULFONYLUREA DERIVATIVE;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN NERVE CELL; CELL MEMBRANE; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN TISSUE; LIPID RAFT; MEMBRANE DAMAGE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANE; CELL CULTURE; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; MEMBRANE STRUCTURE; METABOLISM; NERVE CELL; PATHOLOGY; PRION; SYNAPTOSOME; TEMPORAL LOBE;

AGED; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; CELL MEMBRANE STRUCTURES; CELLS, CULTURED; CHOLESTEROL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; IMMUNOSUPPRESSIVE AGENTS; NEURONS; PEPTIDE FRAGMENTS; PHOSPHOLIPASES A2; PRIONS; SULFONYLUREA COMPOUNDS; SYNAPTOPHYSIN; SYNAPTOSOMES; TEMPORAL LOBE;

EID: 84943327547     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2015.09.030     Document Type: Article

References (61)

1. J.A. Allen, R.A. Halverson-Tamboli, and M.M. Rasenick Lipid raft microdomains and neurotransmitter signalling Nat. Rev. Neurosci. 8 2007 128 140
2. E. Barboni, B.P. Rivero, A.J. George, S.R. Martin, D.V. Renoup, E.F. Hounsell, P.C. Barber, and R.J. Morris The glycophosphatidylinositol anchor affects the conformation of Thy-1 protein J. Cell Sci. 108 1995 487 497
3. 1-42 Neuropharmacology 53 2007 222 231
4. C. Bate, and A. Williams Amyloid-β-induced synapse damage is mediated via cross-linkage of the cellular prion protein J. Biol. Chem. 286 2011 37955 37963
5. C. Bate, and A. Williams Neurodegeneration induced by the clustering of sialylated glycosylphosphatidylinositols of prion proteins J. Biol. Chem. 287 2012 7935 7944
6. Sc formation and protects against prion mediated neurotoxicity PLoS One 4 2009 e8221
7. 2 inhibitors protect against prion and Aβ mediated synapse degeneration Mol. Neurodegener. 5 2010 13
8. M.L. Becker, L.E. Visser, P.H. Trienekens, A. Hofman, R.H.N. van Schaik, and B. Stricker Cytochrome P450 2C9∗2 and∗3 polymorphisms and the dose and effect of sulfonylurea in type II diabetes mellitus Clin. Pharmacol. Ther. 83 2007 288 292
9. D.A. Brown, and E. London Structure and function of sphingolipid- and cholesterol-rich membrane rafts J. Biol. Chem. 275 2000 17221 17224
10. A.M. Calella, M. Farinelli, M. Nuvolone, O. Mirante, R. Moos, J. Falsig, I.M. Mansuy, and A. Aguzzi Prion protein and Aβ-related synaptic toxicity impairment EMBO Mol. Med. 2 2010 306 314
11. B. Chesebro, M. Trifilo, R. Race, K. Meade-White, C. Teng, R. LaCasse, L. Raymond, C. Favara, G. Baron, S. Priola, B. Caughey, E. Masliah, and M. Oldstone Anchorless prion protein results in infectious amyloid disease without clinical scrapie Science 308 2005 1435 1439
12. B. De Strooper, R. Vassar, and T. Golde The secretases: enzymes with therapeutic potential in Alzheimer disease Nat. Rev. Neurol. 6 2010 99 107
13. C. Desbene, C. Malaplate-Armand, I. Youssef, P. Garcia, C. Stenger, M. Sauvee, N. Fischer, D. Rimet, V. Koziel, M.C. Escanye, T. Oster, B. Kriem, F.T. Yen, T. Pillot, and J.L. Olivier Critical role of cPLA(2) in Abeta oligomer-induced neurodegeneration and memory deficit Neurobiol. Aging 33 1123 2012 e1117 1129
14. C.G. Glabe Structural classification of toxic amyloid oligomers J. Biol. Chem. 283 2008 29639 29643
15. M.O.W. Grimm, H.S. Grimm, and T. Hartmann Amyloid beta as a regulator of lipid homeostasis Trends Mol. Med. 13 2007 337 344
16. K.H. Gylys, J.A. Fein, F. Yang, C.A. Miller, and G.M. Cole Increased cholesterol in A[beta]-positive nerve terminals from Alzheimer's disease cortex Neurobiol. Aging 28 2007 8 17
17. C. Haass, and D.J. Selkoe Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide Nat. Rev. Mol. Cell Biol. 8 2007 101 112
18. J. Hardy, and D.J. Selkoe The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353 356
19. H. Jick, G.L. Zornberg, S.S. Jick, S. Seshadri, and D.A. Drachman Statins and the risk of dementia Lancet 356 2000 1627 1631
20. T. Kawarabayashi, M. Shoji, L.H. Younkin, L. Wen-Lang, D.W. Dickson, T. Murakami, E. Matsubara, K. Abe, K.H. Ashe, and S.G. Younkin Dimeric amyloid β protein rapidly accumulates in lipid rafts followed by apolipoprotein E and phosphorylated Tau accumulation in the Tg2576 mouse model of Alzheimer's disease J. Neurosci. 24 2004 3801 3809
21. 1-42 are potent central nervous system neurotoxins Proc. Natl. Acad. Sci. U. S. A. 95 1998 6448 6453
22. J. Lauren, D.A. Gimbel, H.B. Nygaard, J.W. Gilbert, and S.M. Strittmatter Cellular prion protein mediates impairment of synaptic plasticity by amyloid-β oligomers Nature 457 2009 1128 1132
23. S.J. Lee, U. Liyanage, P.E. Bickel, W. Xia, P.T. Lansbury Jr., and K.S. Kosik A detergent-insoluble membrane compartment contains A beta in vivo Nat. Med. 4 1998 730 734
24. D.F. Legler, M.A. Doucey, P. Schneider, L. Chapatte, F.C. Bender, and C. Bron Differential insertion of GPI-anchored GFPs into lipid rafts of live cells FASEB J. 19 2005 73 75
25. C. Lesuisse, and L.J. Martin Long-term culture of mouse cortical neurons as a model for neuronal development, aging, and death J. Neurobiol. 51 2002 9 23
26. G. Li, E.B. Larson, J.A. Sonnen, J.B. Shofer, E.C. Petrie, A. Schantz, E.R. Peskind, M.A. Raskind, J.C.S. Breitner, and T.J. Montine Statin therapy is associated with reduced neuropathologic changes of Alzheimer disease Neurology 69 2007 878 885
27. R. Linden, Y. Cordeiro, and L.M. Lima Allosteric function and dysfunction of the prion protein Cell Mol. Life Sci. 69 2012 1105 1124
28. A. Lorenzo, M. Yuan, Z. Zhang, P.A. Paganetti, C. Sturchler-Pierrat, M. Staufenbiel, J. Mautino, F.S. Vigo, B. Sommer, and B.A. Yankner Amyloid beta interacts with the amyloid precursor protein: a potential toxic mechanism in Alzheimer's disease Nat. Neurosci. 3 2000 460 464
29. S. Mayor, and M. Rao Rafts: scale-dependent, active lipid organization at the cell surface Traffic 5 2004 231 240
30. S. Mayor, and H. Riezman Sorting GPI-anchored proteins Nat. Rev. Mol. Cell Biol. 5 2004 110 120
31. J.M. Mc Donald, G.M. Savva, C. Brayne, A.T. Welzel, G. Forster, G.M. Shankar, D.J. Selkoe, P.G. Ince, and D.M. Walsh The presence of sodium dodecyl sulphate-stable Aβ dimers is strongly associated with Alzheimer-type dementia Brain 133 2010 1328 1341
32. C.A. McLean, R.A. Cherny, F.W. Fraser, S.J. Fuller, M.J. Smith, K. Beyreuther, A.I. Bush, and C.L. Masters Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease Ann. Neurol. 46 1999 860 866
33. S. Mouillet-Richard, M. Ermonval, C. Chebassier, J.L. Laplanche, S. Lehmann, J.M. Launay, and O. Kellermann Signal transduction through prion protein Science 289 2000 1925 1928
34. S. Movahedi, and N.M. Hooper Insulin stimulates the release of the glycosyl phosphatidylinositol-anchored membrane dipeptidase from 3T3-L1 adipocytes through the action of a phospholipase C Biochem. J. 326 Pt 2 1997 531 537
35. G. Müller, E.A. Dearey, A. Korndorfer, and W. Bandlow Stimulation of a glycosyl-phosphatidylinositol-specific phospholipase by insulin and the sulfonylurea, glimepiride, in rat adipocytes depends on increased glucose transport J. Cell Biol. 126 1994 1267 1276
36. G. Müller, C. Jung, S. Wied, S. Welte, and W. Frick Insulin-mimetic signaling by the sulfonylurea glimepiride and phosphoinositolglycans involves distinct mechanisms for redistribution of lipid raft components Biochemistry 40 2001 14603 14620
37. G. Müller, A. Schulz, S. Wied, and W. Frick Regulation of lipid raft proteins by glimepiride- and insulin-induced glycosylphosphatidylinositol-specific phospholipase C in rat adipocytes Biochem. Pharmacol. 69 2005 761 780
38. H. Nakamura, S. Wakita, A. Suganami, Y. Tamura, K. Hanada, and T. Murayama Modulation of the activity of cytosolic phospholipase A2alpha (cPLA2alpha) by cellular sphingolipids and inhibition of cPLA2alpha by sphingomyelin J. Lipid Res. 51 2010 720 728
39. E.A. Nalefski, L.A. Sultzman, D.M. Martin, R.W. Kriz, P.S. Towler, J.L. Knopf, and J.D. Clark Delineation of two functionally distinct domains of cytosolic phospholipase A2, a regulatory Ca(2+)-dependent lipid-binding domain and a Ca(2+)-independent catalytic domain J. Biol. Chem. 269 1994 18239 18249
40. J. Naslund, V. Haroutunian, R. Mohs, K.L. Davis, P. Davies, P. Greengard, and J.D. Buxbaum Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline JAMA 283 2000 1571 1577
41. N. Oshima, M. Morishima-Kawashima, H. Yamaguchi, M. Yoshimura, S. Sugihara, K. Khan, D. Games, D. Schenk, and Y. Ihara Accumulation of amyloid β-protein in the low-density membrane domain accurately reflects the extent of β-amyloid deposition in the brain Am. J. Pathol. 158 2001 2209 2218
42. F. Perini, B. Frangione, and F. Prelli Prion protein released by platelets Lancet 347 1996 1635 1636
43. L.J. Pike Lipid rafts: heterogeneity on the high seas Biochem. J. 378 2004 281 292
44. L. Puglielli, R.E. Tanzi, and D.M. Kovacs Alzheimer's disease: the cholesterol connection Nat. Neurosci. 6 2003 345 351
45. L. Rajendran, and K. Simons Lipid rafts and membrane dynamics J. Cell Sci. 118 2005 1099 1102
46. M. Renner, P.N. Lacor, P.T. Velasco, J. Xu, A. Contractor, W.L. Klein, and A. Triller Deleterious effects of amyloid [beta] oligomers acting as an extracellular scaffold for mGluR5 Neuron 66 2010 739 754
47. 2 reduction ameliorates cognitive deficits in a mouse model of Alzheimer's disease Nat. Neurosci. 11 2008 1311 1318
48. D.J. Selkoe Alzheimer's disease is a synaptic failure Science 298 2002 789 791
49. G.M. Shankar, S. Li, T.H. Mehta, A. Garcia-Munoz, N.E. Shepardson, I. Smith, F.M. Brett, M.A. Farrell, M.J. Rowan, C.A. Lemere, C.M. Regan, D.M. Walsh, B.L. Sabatini, and D.J. Selkoe Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory Nat. Med. 14 2008 837 842
50. 2 in cortical neurons J. Neurochem. 106 2008 45 55
51. N. Stahl, D.R. Borchelt, K. Hsiao, and S.B. Prusiner Scrapie prion protein contains a phosphatidylinositol glycolipid Cell 51 1987 229 240
52. J.D. Stanton, M.B. Rashid, and K. Mensa-Wilmot Cysteine-less glycosylphosphatidylinositol-specific phospholipase C is inhibited competitively by a thiol reagent: evidence for glyco-mimicry by p-chloromercuriphenylsulphonate Biochem. J. 366 2002 281 288
53. R.E. Tanzi The synaptic Aβ hypothesis of Alzheimer disease Nat. Neurosci. 8 2005 977 979
54. D.R. Taylor, and N.M. Hooper The prion protein and lipid rafts Mol. Membr. Biol. 23 2006 89 99
55. M.E. Thais, C.L. Carqueja, T.G. Santos, R.V. Silva, E. Stroeh, R.S. Machado, D.O. Wahlheim, M.M. Bianchin, A.C. Sakamoto, R.R. Brentani, V.R. Martins, R. Walz, and C.I. Tasca Synaptosomal glutamate release and uptake in mice lacking the cellular prion protein Brain Res. 1075 2006 13 19
56. J. Wang, D.W. Dickson, J.Q. Trojanowski, and V.M.Y. Lee The levels of soluble versus insoluble brain A[beta] distinguish Alzheimer's disease from normal and pathologic aging Exp. Neurol. 158 1999 328 337
57. H.-Y. Wang, D.H.S. Lee, M.R. D'Andrea, P.A. Peterson, R.P. Shank, and A.B. Reitz β-Amyloid1-42 binds to α7 nicotinic acetylcholine receptor with high affinity J. Biol. Chem. 275 2000 5626 5632
58. S.S. Wang, D.L. Rymer, and T.A. Good Reduction in cholesterol and sialic acid content protects cells from the toxic effects of beta-amyloid peptides J. Biol. Chem. 276 2001 42027 42034
59. P.R. Westmark, C.J. Westmark, A. Jeevananthan, and J.S. Malter Preparation of synaptoneurosomes from mouse cortex using a discontinuous percoll-sucrose density gradient J. Vis. Exp. 55 2011
60. R. Williamson, A. Usardi, D.P. Hanger, and B.H. Anderton Membrane-bound β-amyloid oligomers are recruited into lipid rafts by a fyn-dependent mechanism FASEB J. 22 2008 1552 1559
61. 2 mediate amyloid-β peptide-induced mitochondrial dysfunction J. Neurosci. 26 2006 11111 11119