Novel APP/Aβ mutation K16N produces highly toxic heteromeric Aβ oligomers

EMBO Molecular Medicine

Volumn 4, Issue 7, 2012, Pages 647-659

  Kaden, Daniela ^a,b   Harmeier, Anja ^a,k   Weise, Christoph ^a   Munter, Lisa M ^a   Althoff, Veit ^a   Rost, Benjamin R ^b   Hildebrand, Peter W ^b   Schmitz, Dietmar ^b,c   Schaefer, Michael ^d   Lurz, Rudi ^e   Skodda, Sabine ^f   Yamamoto, Raina ^g   Arlt, Sönke ^h,i   Finckh, Ulrich ^f,i   Multhaup, Gerd ^a,b,j  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^d UNIVERSITY OF LEIPZIG   (Germany)

^e MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^f RUHR UNIVERSITY BOCHUM   (Germany)

^g Laboratoriumsmedizin Dortmund   (Germany)

^h UNIVERSITY OF HAMBURG   (Germany)

ⁱ Alzheimer Research Group Hamburg   (Germany)

^j MCGILL UNIVERSITY   (Canada)

^k F HOFFMANN LA ROCHE LTD   (Switzerland)

more..

Author keywords

Aggregation; Alzheimer disease; Amyloid beta toxicity; APP processing; Neprilysin

Indexed keywords

ALPHA SECRETASE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; ASPARAGINE; LYSINE; MEMBRANE METALLOENDOPEPTIDASE; OLIGOMER;

ALZHEIMER DISEASE; AMINO ACID SUBSTITUTION; ANAMNESIS; ARTICLE; AUTOSOMAL DOMINANT INHERITANCE; CASE REPORT; CONTROLLED STUDY; DEMENTIA; HETEROZYGOTE; HUMAN; HUMAN CELL; MISSENSE MUTATION; NERVE CELL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CLEAVAGE; PROTEIN STABILITY; WILD TYPE;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; AMYLOID BETA-PEPTIDES; AMYLOID PRECURSOR PROTEIN SECRETASES; CELL LINE, TUMOR; HEK293 CELLS; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; NEPRILYSIN; PEPTIDE FRAGMENTS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRANSFECTION;

EID: 84863472459     PISSN: 17574676     EISSN: 17574684     Source Type: Journal    
DOI: 10.1002/emmm.201200239     Document Type: Article

References (40)

1. Betts V, Leissring MA, Dolios G, Wang R, Selkoe DJ, Walsh DM (2008) Aggregation and catabolism of disease-associated intra-Abeta mutations: reduced proteolysis of AbetaA21G by neprilysin. Neurobiol Dis 31: 442- 450
2. Carson JA, Turner AJ (2002) Beta-amyloid catabolism: Roles for neprilysin (NEP) and other metallopeptidases? J Neurochem 81: 1- 8
3. Chen YR, Glabe CG (2006) Distinct early folding and aggregation properties of Alzheimer amyloid-beta peptides Abeta40 and Abeta42: stable trimer or tetramer formation by Abeta42. J Biol Chem 281: 24414- 24422
4. De Jonghe C, Zehr C, Yager D, Prada CM, Younkin S, Hendriks L, Van Broeckhoven C, Eckman CB (1998) Flemish and Dutch mutations in amyloid beta precursor protein have different effects on amyloid beta secretion. Neurobiol Dis 5: 281- 286
5. Di Fede G, Catania M, Morbin M, Rossi G, Suardi S, Mazzoleni G, Merlin M, Giovagnoli AR, Prioni S, Erbetta A, et al (2009) A recessive mutation in the APP gene with dominant-negative effect on amyloidogenesis. Science 323: 1473- 1477
6. Furukawa K, Sopher BL, Rydel RE, Begley JG, Pham DG, Martin GM, Fox M, Mattson MP (1996) Increased activity-regulating and neuroprotective efficacy of alpha-secretase-derived secreted amyloid precursor protein conferred by a C-terminal heparin-binding domain. J Neurochem 67: 1882- 1896
7. Guerreiro RJ, Baquero M, Blesa R, Boada M, Bras JM, Bullido MJ, Calado A, Crook R, Ferreira C, Frank A, et al (2010) Genetic screening of Alzheimer's disease genes in Iberian and African samples yields novel mutations in presenilins and APP. Neurobiol Aging 31: 725- 731
8. Haass C, Hung AY, Selkoe DJ, Teplow DB (1994) Mutations associated with a locus for familial Alzheimer's disease result in alternative processing of amyloid beta-protein precursor. J Biol Chem 269: 17741- 17748
9. Hardy J (2006) A hundred years of Alzheimer's disease research. Neuron 52: 3- 13
10. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297: 353- 356
11. Harmeier A, Wozny C, Rost BR, Munter LM, Hua H, Georgiev O, Beyermann M, Hildebrand PW, Weise C, Schaffner W, et al (2009) Role of amyloid-beta glycine 33 in oligomerization, toxicity, and neuronal plasticity. J Neurosci 29: 7582- 7590
12. Howell S, Nalbantoglu J, Crine P (1995) Neutral endopeptidase can hydrolyze beta-amyloid(1-40) but shows no effect on beta-amyloid precursor protein metabolism. Peptides 16: 647- 652
13. Iwata N, Tsubuki S, Takaki Y, Shirotani K, Lu B, Gerard NP, Gerard C, Hama E, Lee HJ, Saido TC (2001) Metabolic regulation of brain Abeta by neprilysin. Science 292: 1550- 1552
14. Iwata N, Mizukami H, Shirotani K, Takaki Y, Muramatsu S, Lu B, Gerard NP, Gerard C, Ozawa K, Saido TC (2004) Presynaptic localization of neprilysin contributes to efficient clearance of amyloid-beta peptide in mouse brain. J Neurosci 24: 991- 998
15. Kaden D, Voigt P, Munter LM, Bobowski KD, Schaefer M, Multhaup G (2009) Subcellular localization and dimerization of APLP1 are strikingly different from APP and APLP2. J Cell Sci 122: 368- 377
16. Kalbe E, Kessler J, Calabrese P, Smith R, Passmore AP, Brand M, Bullock R (2004) DemTect: a new, sensitive cognitive screening test to support the diagnosis of mild cognitive impairment and early dementia. Int J Geriatr Psychiatry 19: 136- 143
17. Kanemitsu H, Tomiyama T, Mori H (2003) Human neprilysin is capable of degrading amyloid beta peptide not only in the monomeric form but also the pathological oligomeric form. Neurosci Lett 350: 113- 116
18. Kennedy JL, Farrer LA, Andreasen NC, Mayeux R, St George-Hyslop P (2003) The genetics of adult-onset neuropsychiatric disease: Complexities and conundra? Science 302: 822- 826
19. Klein WL, Krafft GA, Finch CE (2001) Targeting small Abeta oligomers: The solution to an Alzheimer's disease conundrum? Trends Neurosci 24: 219- 224
20. Kuhn PH, Wang H, Dislich B, Colombo A, Zeitschel U, Ellwart JW, Kremmer E, Rossner S, Lichtenthaler SF (2010) ADAM10 is the physiologically relevant, constitutive alpha-secretase of the amyloid precursor protein in primary neurons. EMBO J 29: 3020- 3032
21. Kumar-Singh S, Julliams A, Nuydens R, Ceuterick C, Labeur C, Serneels S, Vennekens K, Van Osta P, Geerts H, De Strooper B, et al (2002) In vitro studies of Flemish, Dutch, and wild-type beta-amyloid provide evidence for two-staged neurotoxicity. Neurobiol Dis 11: 330- 340
22. Kuperstein I, Broersen K, Benilova I, Rozenski J, Jonckheere W, Debulpaep M, Vandersteen A, Segers-Nolten I, Van Der Werf K, Subramaniam V, et al (2010) Neurotoxicity of Alzheimer's disease Abeta peptides is induced by small changes in the Abeta42 to Abeta40 ratio. EMBO J 29: 3408- 3420
23. Luhrs T, Ritter C, Adrian M, Riek-Loher D, Bohrmann B, Dobeli H, Schubert D, Riek R (2005) 3D structure of Alzheimer's amyloid-beta(1-42) fibrils. Proc Natl Acad Sci USA 102: 17342- 17347
24. Morelli L, Llovera R, Gonzalez SA, Affranchino JL, Prelli F, Frangione B, Ghiso J, Castano EM (2003) Differential degradation of amyloid beta genetic variants associated with hereditary dementia or stroke by insulin-degrading enzyme. J Biol Chem 278: 23221- 23226
25. Munter LM, Voigt P, Harmeier A, Kaden D, Gottschalk KE, Weise C, Pipkorn R, Schaefer M, Langosch D, Multhaup G (2007) GxxxG motifs within the amyloid precursor protein transmembrane sequence are critical for the etiology of Abeta42. EMBO J 26: 1702- 1712
26. Murakami K, Irie K, Morimoto A, Ohigashi H, Shindo M, Nagao M, Shimizu T, Shirasawa T (2002) Synthesis, aggregation, neurotoxicity, and secondary structure of various A beta 1-42 mutants of familial Alzheimer's disease at positions 21-23. Biochem Biophys Res Commun 294: 5- 10
27. Nilsberth C, Westlind-Danielsson A, Eckman CB, Condron MM, Axelman K, Forsell C, Stenh C, Luthman J, Teplow DB, Younkin SG, et al (2001) The 'Arctic' APP mutation (E693G) causes Alzheimer's disease by enhanced Abeta protofibril formation. Nat Neurosci 4: 887- 893
28. Portelius E, Westman-Brinkmalm A, Zetterberg H, Blennow K (2006) Determination of beta-amyloid peptide signatures in cerebrospinal fluid using immunoprecipitation-mass spectrometry. J Proteome Res 5: 1010- 1016
29. Sahlin C, Lord A, Magnusson K, Englund H, Almeida CG, Greengard P, Nyberg F, Gouras GK, Lannfelt L, Nilsson LN (2007) The Arctic Alzheimer mutation favors intracellular amyloid-beta production by making amyloid precursor protein less available to alpha-secretase. J Neurochem 101: 854- 862
30. Schmechel A, Zentgraf H, Scheuermann S, Fritz G, Pipkorn R, Reed J, Beyreuther K, Bayer TA, Multhaup G (2003) Alzheimer beta-amyloid homodimers facilitate A beta fibrillization and the generation of conformational antibodies. J Biol Chem 278: 35317- 35324
31. Selkoe DJ (2001a) Alzheimer's disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J Alzheimers Dis 3: 75- 80
32. Selkoe DJ (2001b) Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 81: 741- 766
33. Shirotani K, Tsubuki S, Iwata N, Takaki Y, Harigaya W, Maruyama K, Kiryu-Seo S, Kiyama H, Iwata H, Tomita T, et al (2001) Neprilysin degrades both amyloid beta peptides 1-40 and 1-42 most rapidly and efficiently among thiorphan- and phosphoramidon-sensitive endopeptidases. J Biol Chem 276: 21895- 21901
34. Stenh C, Nilsberth C, Hammarback J, Engvall B, Naslund J, Lannfelt L (2002) The Arctic mutation interferes with processing of the amyloid precursor protein. Neuroreport 13: 1857- 1860
35. Steven AC, Trus BL, Maizel JV, Unser M, Parry DA, Wall JS, Hainfeld JF, Studier FW (1988) Molecular substructure of a viral receptor-recognition protein. The gp17 tail-fiber of bacteriophage T7. J Mol Biol 200: 351- 365
36. Van Broeckhoven C, Haan J, Bakker E, Hardy JA, Van Hul W, Wehnert A, Vegter-Van der Vlis M, Roos RA (1990) Amyloid beta protein precursor gene and hereditary cerebral hemorrhage with amyloidosis (Dutch). Science 248: 1120- 1122
37. Van Nostrand WE, Melchor JP, Cho HS, Greenberg SM, Rebeck GW (2001) Pathogenic effects of D23N Iowa mutant amyloid beta-protein. J Biol Chem 276: 32860- 32866
38. 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
39. Yang HC, Chai X, Mosior M, Kohn W, Boggs LN, Erickson JA, McClure DB, Yeh WK, Zhang L, Gonzalez-DeWhitt P, et al (2004) Biochemical and kinetic characterization of BACE1: investigation into the putative species-specificity for beta- and beta'-cleavage sites by human and murine BACE1. J Neurochem 91: 1249- 1259
40. Younkin SG (1998) The role of Abeta 42 in Alzheimer's disease. J Physiol Paris 92: 289- 292