Intracellular accumulation of aggregated pyroglutamate amyloid beta: Convergence of aging and Aβ pathology at the lysosome

Age

Volumn 35, Issue 3, 2013, Pages 673-687

  De Kimpe, Line ^a   Van Haastert, Elise S ^b   Kaminari, Archontia ^a   Zwart, Rob ^a   Rutjes, Helma ^c   Hoozemans, Jeroen J M ^b   Scheper, Wiep ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Hycult Biotech   (Netherlands)

Author keywords

Alzheimer's disease; Lysosomal pathology; Pyroglutamate amyloid beta

Indexed keywords

AMYLOID BETA PROTEIN; GLYCOPROTEIN; PYROGLUTAMATE AMYLOID BETA PROTEIN; PYROGLUTAMATE AMYLOID BETA PROTEIN[3-42]; UNCLASSIFIED DRUG;

ADULT; AGE DISTRIBUTION; AGED; AGING; ALZHEIMER DISEASE; ARTICLE; AUTOPSY; BRAIN NERVE CELL; BRAIN TISSUE; CELL COMPARTMENTALIZATION; CELL LOSS; CELL MEMBRANE PERMEABILITY; CELL METABOLISM; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GLIA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; LYSOSOME MEMBRANE; MALE; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; TEMPORAL CORTEX;

ADULT; AGED; AGED, 80 AND OVER; AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; BRAIN; DISEASE PROGRESSION; FEMALE; HUMANS; INTRACELLULAR FLUID; LYSOSOMES; MALE; MIDDLE AGED; NEURONS; PEPTIDE FRAGMENTS;

EID: 84880570156     PISSN: 01619152     EISSN: 15744647     Source Type: Journal    
DOI: 10.1007/s11357-012-9403-0     Document Type: Article

References (37)

1. Boya P, Andreau K, Poncet D, Zamzami N, Perfettini JL, Metivier D, Ojcius DM, Jaattela M, Kroemer G (2003) Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J Exp Med 197:1323-1334
2. Chafekar SM, Hoozemans JJ, Zwart R, Baas F, Scheper W (2007) Abeta 1-42 induces mild endoplasmic reticulum stress in an aggregation state-dependent manner. Antioxid Redox Signal 9:2245-2254
3. Chafekar SM, Baas F, Scheper W (2008) Oligomer-specific Abeta toxicity in cell models is mediated by selective uptake. Biochim Biophys Acta 1782:523-531
4. Chondrogianni N, Fragoulis EG, Gonos ES (2002) Protein degradation during aging: the lysosome-, the calpain- and the proteasome-dependent cellular proteolytic systems. Biogerontology 3:121-123
5. Christensen DZ, Schneider-Axmann T, Lucassen PJ, Bayer TA, Wirths O (2010) Accumulation of intraneuronal Abeta correlates with ApoE4 genotype. Acta Neuropathol 119:555-566
6. Cramer PE, Cirrito JR, Wesson DW, Lee CY, Karlo JC, Zinn AE, Casali BT, Restivo JL, Goebel WD, James MJ, Brunden KR, Wilson DA, Landreth GE (2012) ApoE-directed therapeutics rapidly clear β-amyloid and reverse deficits in AD mouse models. Science. doi: 10.1126/science.1217697
7. De Kimpe L, Scheper W (2010) From alpha to omega with Abeta: targeting the multiple molecular appearances of the pathogenic peptide in Alzheimer's disease. Curr Med Chem 17:198-212
8. Ditaranto K, Tekirian TL, Yang AJ (2001) Lysosomal membrane damage in soluble Abeta-mediated cell death in Alzheimer's disease. Neurobiol Dis 8:19-31
9. Giunta B, Fernandez F, Nikolic WV, Obregon D, Rrapo E, Town T, Tan J (2008) Inflammaging as a prodrome to Alzheimer's disease. J Neuroinflammation 5:51-66
10. Haass C, Selkoe DJ (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide. Nat Rev Mol Cell Biol 8:101-112
11. Hardy J, Selkoe DJ (2002) The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297:353-356
12. Hoozemans JJ, Chafekar SM, Baas F, Eikelenboom P, Scheper W (2006) Always around, never the same: pathways of amyloid beta induced neurodegeneration throughout the pathogenic cascade of Alzheimer's disease. Curr Med Chem 13:2599-2605
13. Kayed R, Head E, Thompson JL, McIntire TM, Milton SC, Cotman CW, Glabe CG (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300:486-489
14. Kirkegaard T, Roth AG, Petersen NH, Mahalka AK, Olsen OD, Moilanen I, Zylicz A, Knudsen J, Sandhoff K, Arenz C, Kinnunen PK, Nylandsted J, Jaattela M (2010) Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 463:549-553
15. Kuo YM, Webster S, Emmerling MR, De LN, Roher AE (1998) Irreversible dimerization/tetramerization and post-translational modifications inhibit proteolytic degradation of A beta peptides of Alzheimer's disease. Biochim Biophys Acta 1406:291-298
16. Lee JH, Yu WH, Kumar A, Lee S, Mohan PS, Peterhoff CM, Wolfe DM, Martinez-Vicente M, Massey AC, Sovak G, Uchiyama Y, Westaway D, Cuervo AM, Nixon RA (2010) Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141:1146-1158
17. Ling D, Salvaterra PM (2011) Brain aging and Abeta(1-42) neurotoxicity converge via deterioration in autophagy-lysosomal system: a conditional Drosophila model linking Alzheimer's neurodegeneration with aging. Acta Neuropathol 121:83-91
18. Nielsen HM, Veerhuis R, Holmqvist B, Janciauskiene S (2009) Binding and uptake of A beta1-42 by primary human astrocytes in vitro. Glia 57:978-988
19. Nielsen HM, Mulder SD, Belien JA, Musters RJ, Eikelenboom P, Veerhuis R (2010) Astrocytic A beta 1-42 uptake is determined by A beta-aggregation state and the presence of amyloid-associated proteins. Glia 58:1235-1246
20. Nijholt DA, de Graaf TR, van Haastert ES, Oliveira AO, Berkers CR, Zwart R, Ovaa H, Baas F, Hoozemans JJ, Scheper W (2011) Endoplasmic reticulum stress activates autophagy but not the proteasome in neuronal cells: implications for Alzheimer's disease. Cell Death Differ 18:1071-81
21. Nixon RA (2007) Autophagy, amyloidogenesis and Alzheimer disease. J Cell Sci 120:4081-4091
22. Nixon RA, Yang DS, Lee JH (2008) Neurodegenerative lysosomal disorders: a continuum from development to late age. Autophagy 4:590-599
23. Reits E, Griekspoor A, Neijssen J, Groothuis T, Jalink K, van Veelen P, Janssen H, Calafat J, Drijfhout JW, Neefjes J (2003) Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity 18:97-108
24. Russo C, Violani E, Salis S, Venezia V, Dolcini V, Damonte G, Benatti U, D'Arrigo C, Patrone E, Carlo P, Schettini G (2002) Pyroglutamate-modified amyloid beta-peptides - AbetaN3(pE) - strongly affect cultured neuron and astrocyte survival. J Neurochem 82:1480-1489
25. Saido TC, Yamao-Harigaya W, Iwatsubo T, Kawashima S (1996) Amino- and carboxyl-terminal heterogeneity of beta-amyloid peptides deposited in human brain. Neurosci Lett 215:173-176
26. Sasaki N, Toki S, Chowei H, Saito T, Nakano N, Hayashi Y, Takeuchi M, Makita Z (2001) Immunohistochemical distribution of the receptor for advanced glycation end products in neurons and astrocytes in Alzheimer's disease. Brain Res 888:256-262
27. Scheper W, Zwart R, Baas F (2004) Rab6 membrane association is dependent of Presenilin 1 and cellular phosphorylation events. Brain Res Mol Brain Res 122:17-23
28. Schilling S, Hoffmann T, Manhart S, Hoffmann M, Demuth HU (2004) Glutaminyl cyclases unfold glutamyl cyclase activity under mild acid conditions. FEBS Lett 563:191-196
29. Schilling S, Lauber T, Schaupp M, Manhart S, Scheel E, Bohm G, Demuth HU (2006) On the seeding and oligomerization of pGlu-amyloid peptides (in vitro). Biochemistry 45:12393-12399
30. Schilling S, Zeitschel U, Hoffmann T, Heiser U, Francke M, Kehlen A, Holzer M, Hutter-Paier B, Prokesch M, Windisch M, Jagla W, Schlenzig D, Lindner C, Rudolph T, Reuter G, Cynis H, Montag D, Demuth HU, Rossner S (2008) Glutaminyl cyclase inhibition attenuates pyroglutamate Abeta and Alzheimer's disease-like pathology. Nat Med 14:1106-1111
31. Walsh DM, Tseng BP, Rydel RE, Podlisny MB, Selkoe DJ (2000) The oligomerization of amyloid beta-protein begins intracellularly in cells derived from human brain. Biochemistry 39:10831-10839
32. Watabe K, Osborne D, Kim SU (1989) Phagocytic activity of human adult astrocytes and oligodendrocytes in culture. J Neuropathol Exp Neurol 48:499-506
33. Wirths O, Multhaup G, Czech C, Blanchard V, Moussaoui S, Tremp G, Pradier L, Beyreuther K, Bayer TA (2001) Intraneuronal Abeta accumulation precedes plaque formation in beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 306:116-120
34. Wirths O, Breyhan H, Cynis H, Schilling S, Demuth HU, Bayer TA (2009) Intraneuronal pyroglutamate-Abeta 3-42 triggers neurodegeneration and lethal neurological deficits in a transgenic mouse model. Acta Neuropathol 118:487-496
35. Wirths O, Erck C, Martens H, Harmeier A, Geumann C, Jawhar S, Kumar S, Multhaup G, Walter J, Ingelsson M, Degerman-Gunnarsson M, Kalimo H, Huitinga I, Lannfelt L, Bayer TA (2010) Identification of low molecular weight pyroglutamate abeta oligomers in Alzheimer disease: a novel tool for therapy and diagnosis. J Biol Chem 285:41517-24
36. Yang DS, Stavrides P, Mohan PS, Kaushik S, Kumar A, Ohno M, Schmidt SD, Wesson D, Bandyopadhyay U, Jiang Y, Pawlik M, Peterhoff CM, Yang AJ, Wilson DA, St George-Hyslop P, Westaway D, Mathews PM, Levy E, Cuervo AM, Nixon RA (2011) Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 134:258-277
37. Youssef I, Florent-Bechard S, Malaplate-Armand C, Koziel V, Bihain B, Olivier JL, Leininger-Muller B, Kriem B, Oster T, Pillot T (2008) N-truncated amyloid-beta oligomers induce learning impairment and neuronal apoptosis. Neurobiol Aging 29:1319-1333