The Osaka FAD mutation E22Δ leads to the formation of a previously unknown type of amyloid β fibrils and modulates Aβ neurotoxicity

Journal of Molecular Biology

Volumn 408, Issue 4, 2011, Pages 780-791

  Ovchinnikova, Oxana Yu ^a   Finder, Verena H ^a,b   Vodopivec, Ivana ^b   Nitsch, Roger M ^b   Glockshuber, Rudi ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

aggregation; Alzheimer's disease; A ; E22 ; neurotoxicity

Indexed keywords

AMYLOID BETA PROTEIN[1-40]; AMYLOID BETA PROTEIN[1-42]; COLLAGEN FIBRIL; GLUTAMIC ACID; THIOFLAVINE;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CELL CULTURE; CONTROLLED STUDY; GENE DELETION; GENE MUTATION; JAPANESE; NERVE CELL; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RAT;

RATTUS;

EID: 79955038897     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.02.049     Document Type: Article

References (43)

1. Hardy J., and Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353 356 (Pubitemid 34790756)
2. Selkoe D.J. Cell biology of protein misfolding: the examples of Alzheimer's and Parkinson's diseases Nat. Cell Biol. 6 2004 1054 1061 (Pubitemid 39468006)
3. Suzuki N., Cheung T.T., Cai X.D., Odaka A., Otvos L. Jr, and Eckman C. An increased percentage of long amyloid beta protein secreted by familial amyloid beta protein precursor (beta APP717) mutants Science 264 1994 1336 1340
4. Jensen M., Schroder J., Blomberg M., Engvall B., Pantel J., and Ida N. Cerebrospinal fluid A beta42 is increased early in sporadic Alzheimer's disease and declines with disease progression Ann. Neurol. 45 1999 504 511 (Pubitemid 29165817)
5. Tomiyama T., Nagata T., Shimada H., Teraoka R., Fukushima A., and Kanemitsu H. A new amyloid beta variant favoring oligomerization in Alzheimer's-type dementia Ann. Neurol. 63 2008 377 387 (Pubitemid 351499867)
6. Irie K., Murakami K., Masuda Y., Morimoto A., Ohigashi H., and Ohashi R. Structure of beta-amyloid fibrils and its relevance to their neurotoxicity: implications for the pathogenesis of Alzheimer's disease J. Biosci. Bioeng. 99 2005 437 447 (Pubitemid 40874521)
7. Sherrington R., Rogaev E.I., Liang Y., Rogaeva E.A., Levesque G., and Ikeda M. Cloning of a gene bearing missense mutations in early-onset familial Alzheimer's disease Nature 375 1995 754 760
8. Levy-Lahad E., Wasco W., Poorkaj P., Romano D.M., Oshima J., and Pettingell W.H. Candidate gene for the chromosome 1 familial Alzheimer's disease locus Science 269 1995 973 977
9. Hendriks L., van Duijn C.M., Cras P., Cruts M., Van Hul W., and van Harskamp F. Presenile dementia and cerebral haemorrhage linked to a mutation at codon 692 of the beta-amyloid precursor protein gene Nat. Genet. 1 1992 218 221
10. Levy E., Carman M.D., Fernandez-Madrid I.J., Power M.D., Lieberburg I., and van Duinen S.G. Mutation of the Alzheimer's disease amyloid gene in hereditary cerebral hemorrhage, Dutch type Science 248 1990 1124 1126
11. Tagliavini F., Rossi G., Padovani A., Magoni M., Andora G., and Sgarzi M. A new βPP mutation related to hereditary cerebral haemorrhage Alzheimer's Rep. 2 1999 S28
12. Nilsberth C., Westlind-Danielsson A., Eckman C.B., Condron M.M., Axelman K., and Forsell C. The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Abeta protofibril formation Nat. Neurosci. 4 2001 887 893 (Pubitemid 32801591)
13. Grabowski T.J., Cho H.S., Vonsattel J.P., Rebeck G.W., and Greenberg S.M. Novel amyloid precursor protein mutation in an Iowa family with dementia and severe cerebral amyloid angiopathy Ann. Neurol. 49 2001 697 705 (Pubitemid 32530235)
14. Wakutani Y., Watanabe K., Adachi Y., Wada-Isoe K., Urakami K., and Ninomiya H. Novel amyloid precursor protein gene missense mutation (D678N) in probable familial Alzheimer's disease J. Neurol. Neurosurg. Psychiatry 75 2004 1039 1042 (Pubitemid 38869622)
15. Janssen J.C., Beck J.A., Campbell T.A., Dickinson A., Fox N.C., and Harvey R.J. Early onset familial Alzheimer's disease: mutation frequency in 31 families Neurology 60 2003 235 239 (Pubitemid 36152015)
16. Di Fede G., Catania M., Morbin M., Rossi G., Suardi S., and Mazzoleni G. A recessive mutation in the APP gene with dominant-negative effect on amyloidogenesis Science 323 2009 1473 1477
17. Finder V.H., and Glockshuber R. Amyloid-beta aggregation Neurodegener. Dis. 4 2007 13 27
18. Takuma H., Teraoka R., Mori H., and Tomiyama T. Amyloid-beta E22Delta variant induces synaptic alteration in mouse hippocampal slices NeuroReport 19 2008 615 619 (Pubitemid 351489355)
19. Tomiyama T., Matsuyama S., Iso H., Umeda T., Takuma H., and Ohnishi K. A mouse model of amyloid beta oligomers: their contribution to synaptic alteration, abnormal tau phosphorylation, glial activation, and neuronal loss in vivo J. Neurosci. 30 2010 4845 4856
20. Nishitsuji K., Tomiyama T., Ishibashi K., Ito K., Teraoka R., and Lambert M.P. The E693Delta mutation in amyloid precursor protein increases intracellular accumulation of amyloid beta oligomers and causes endoplasmic reticulum stress-induced apoptosis in cultured cells Am. J. Pathol. 174 2009 957 969
21. Nagata T., Tominaga T., Mori H., Yaguchi T., and Nishizaki T. DCP-LA neutralizes mutant amyloid beta peptide-induced impairment of long-term potentiation and spatial learning Behav. Brain Res. 206 2010 151 154
22. Finder V.H., Vodopivec I., Nitsch R.M., and Glockshuber R. The recombinant amyloid-beta peptide Abeta1-42 aggregates faster and is more neurotoxic than synthetic Abeta1-42 J. Mol. Biol. 396 2010 9 18
23. Wu C., Wang Z., Lei H., Duan Y., Bowers M.T., and Shea J.E. The binding of thioflavin T and its neutral analog BTA-1 to protofibrils of the Alzheimer's disease Abeta(16-22) peptide probed by molecular dynamics simulations J. Mol. Biol. 384 2008 718 729
24. Khurana R., Coleman C., Ionescu-Zanetti C., Carter S.A., Krishna V., and Grover R.K. Mechanism of thioflavin T binding to amyloid fibrils J. Struct. Biol. 151 2005 229 238 (Pubitemid 41338730)
25. Groenning M., Olsen L., van de Weert M., Flink J.M., Frokjaer S., and Jorgensen F.S. Study on the binding of thioflavin T to beta-sheet-rich and non-beta-sheet cavities J. Struct. Biol. 158 2007 358 369 (Pubitemid 46766672)
26. Groenning M., Norrman M., Flink J.M., van de Weert M., Bukrinsky J.T., Schluckebier G., and Frokjaer S. Binding mode of thioflavin T in insulin amyloid fibrils J. Struct. Biol. 159 2007 483 497 (Pubitemid 47351257)
27. Lührs T., Ritter C., Adrian M., Riek-Loher D., Bohrmann B., and Dobeli H. 3D structure of Alzheimer's amyloid-beta(1-42) fibrils Proc. Natl Acad. Sci. USA 102 2005 17342 17347
28. Petkova A.T., Ishii Y., Balbach J.J., Antzutkin O.N., Leapman R.D., Delaglio F., and Tycko R. A structural model for Alzheimer's beta-amyloid fibrils based on experimental constraints from solid state NMR Proc. Natl Acad. Sci. USA 99 2002 16742 16747 (Pubitemid 36034043)
29. Morimoto A., Irie K., Murakami K., Masuda Y., Ohigashi H., and Nagao M. Analysis of the secondary structure of beta-amyloid (Abeta42) fibrils by systematic proline replacement J. Biol. Chem. 279 2004 52781 52788 (Pubitemid 39656654)
30. Williams A.D., Portelius E., Kheterpal I., Guo J.T., Cook K.D., Xu Y., and Wetzel R. Mapping Abeta amyloid fibril secondary structure using scanning proline mutagenesis J. Mol. Biol. 335 2004 833 842 (Pubitemid 38352823)
31. Masuda Y., Irie K., Murakami K., Ohigashi H., Ohashi R., and Takegoshi K. Verification of the turn at positions 22 and 23 of the beta-amyloid fibrils with Italian mutation using solid-state NMR Bioorg. Med. Chem. 13 2005 6803 6809 (Pubitemid 41571226)
32. Meinhardt J., Sachse C., Hortschansky P., Grigorieff N., and Fandrich M. Abeta(1-40) fibril polymorphism implies diverse interaction patterns in amyloid fibrils J. Mol. Biol. 386 2009 869 877
33. Fändrich M., Meinhardt J., and Grigorieff N. Structural polymorphism of Alzheimer Abeta and other amyloid fibrils Prion 3 2009 89 93
34. Kim W., and Hecht M.H. Mutations enhance the aggregation propensity of the Alzheimer's A beta peptide J. Mol. Biol. 377 2008 565 574
35. Melchor J.P., McVoy L., and Van Nostrand W.E. Charge alterations of E22 enhance the pathogenic properties of the amyloid beta-protein J. Neurochem. 74 2000 2209 2212 (Pubitemid 30217679)
36. Clements A., Walsh D.M., Williams C.H., and Allsop D. Effects of the mutations Glu22 to Gln and Ala21 to Gly on the aggregation of a synthetic fragment of the Alzheimer's amyloid beta/A4 peptide Neurosci. Lett. 161 1993 17 20 (Pubitemid 23311054)
37. Miravalle L., Tokuda T., Chiarle R., Giaccone G., Bugiani O., and Tagliavini F. Substitutions at codon 22 of Alzheimer's Abeta peptide induce diverse conformational changes and apoptotic effects in human cerebral endothelial cells J. Biol. Chem. 275 2000 27110 27116
38. Kirkitadze M.D., Condron M.M., and Teplow D.B. Identification and characterization of key kinetic intermediates in amyloid beta-protein fibrillogenesis J. Mol. Biol. 312 2001 1103 1119 (Pubitemid 32980329)
39. Fraser P.E., Nguyen J.T., Inouye H., Surewicz W.K., Selkoe D.J., Podlisny M.B., and Kirschner D.A. Fibril formation by primate, rodent, and Dutch-hemorrhagic analogues of Alzheimer amyloid beta-protein Biochemistry 31 1992 10716 10723
40. Baumketner A., Krone M.G., and Shea J.E. Role of the familial Dutch mutation E22Q in the folding and aggregation of the 15-28 fragment of the Alzheimer amyloid-beta protein Proc. Natl Acad. Sci. USA 105 2008 6027 6032 (Pubitemid 351758393)
41. Cheng I.H., Scearce-Levie K., Legleiter J., Palop J.J., Gerstein H., and Bien-Ly N. Accelerating amyloid-beta fibrillization reduces oligomer levels and functional deficits in Alzheimer disease mouse models J. Biol. Chem. 282 2007 23818 23828 (Pubitemid 47328006)
42. De Ferrari G.V., Mallender W.D., Inestrosa N.C., and Rosenberry T.L. Thioflavin T is a fluorescent probe of the acetylcholinesterase peripheral site that reveals conformational interactions between the peripheral and acylation sites J. Biol. Chem. 276 2001 23282 23287
43. Pool M., Thiemann J., Bar-Or A., and Fournier A.E. NeuriteTracer: a novel ImageJ plugin for automated quantification of neurite outgrowth J. Neurosci. Methods 168 2008 134 139