Oligomer-specific Aβ toxicity in cell models is mediated by selective uptake

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1782, Issue 9, 2008, Pages 523-531

  Chafekar, Sidhartha M ^a   Baas, Frank ^a   Scheper, Wiep ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

amyloid; Aggregation; Alzheimer's disease; Oligomer; Toxicity; Uptake

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN (1 42); AMYLOID BETA-PROTEIN (1-42); FUSED HETEROCYCLIC RINGS; PEPTIDE FRAGMENT; TETRAMETHYLROSAMINE;

ARTICLE; CELL DIFFERENTIATION; CYTOTOXICITY; ENDOCYTOSIS; FLUORESCENCE; HELA CELL; HUMAN; HUMAN CELL; INTRACELLULAR SPACE; LYSOSOME; PRIORITY JOURNAL; PROTEIN AGGREGATION; BIOLOGICAL MODEL; CHEMISTRY; DRUG EFFECT; METABOLISM; PROTEIN QUATERNARY STRUCTURE; TUMOR CELL LINE; ULTRASTRUCTURE;

AMYLOID BETA-PROTEIN; CELL LINE, TUMOR; ENDOCYTOSIS; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; LYSOSOMES; MODELS, BIOLOGICAL; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, QUATERNARY;

EID: 50949097728     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2008.06.003     Document Type: Article

References (70)

1. Annaert W., and De Strooper B. A cell biological perspective on Alzheimer's disease. Annu. Rev. Cell Dev. Biol. 18 (2002) 25-51
2. Hutton M., Perez-Tur J., and Hardy J. Genetics of Alzheimer's disease. Essays Biochem. 33 (1998) 117-131
3. Taylor J.P., Hardy J., and Fischbeck K.H. Toxic proteins in neurodegenerative disease. Science 296 (2002) 1991-1995
4. Chromy B.A., Nowak R.J., Lambert M.P., Viola K.L., Chang L., Velasco P.T., Jones B.W., Fernandez S.J., Lacor P.N., Horowitz P., Finch C.E., Krafft G.A., and Klein W.L. Self-assembly of Abeta(1-42) into globular neurotoxins. Biochemistry 42 (2003) 12749-12760
5. Pike C.J., Burdick D., Walencewicz A.J., Glabe C.G., and Cotman C.W. Neurodegeneration induced by beta-amyloid peptides in vitro: the role of peptide assembly state. J. Neurosci. 13 (1993) 1676-1687
6. Seilheimer B., Bohrmann B., Bondolfi L., Muller F., Stuber D., and Dobeli H. The toxicity of the Alzheimer's beta-amyloid peptide correlates with a distinct fiber morphology. J. Struct. Biol. 119 (1997) 59-71
7. Scheper W., and Hol E.M. Protein quality control in Alzheimer's disease: a fatal saviour. Curr. Drug Targets CNS Neurol. Disord. 4 (2005) 283-292
8. LaFerla F.M., Green K.N., and Oddo S. Intracellular amyloid-beta in Alzheimer's disease. Nat. Rev. Neurosci. 8 (2007) 499-509
9. Cataldo A.M., Petanceska S., Terio N.B., Peterhoff C.M., Durham R., Mercken M., Mehta P.D., Buxbaum J., Haroutunian V., and Nixon R.A. Abeta localization in abnormal endosomes: association with earliest Abeta elevations in AD and Down syndrome. Neurobiol. Aging 25 (2004) 1263-1272
10. D'Andrea M.R., Nagele R.G., Wang H.Y., Peterson P.A., and Lee D.H. Evidence that neurones accumulating amyloid can undergo lysis to form amyloid plaques in Alzheimer's disease. Histopathology 38 (2001) 120-134
11. Mori C., Spooner E.T., Wisniewsk K.E., Wisniewski T.M., Yamaguch H., Saido T.C., Tolan D.R., Selkoe D.J., and Lemere C.A. Intraneuronal Abeta42 accumulation in Down syndrome brain. Amyloid 9 (2002) 88-102
12. Rodrigo J., Fernandez-Vizarra P., Castro-Blanco S., Bentura M.L., Nieto M., Gomez-Isla T., Martinez-Murillo R., MartInez A., Serrano J., and Fernandez A.P. Nitric oxide in the cerebral cortex of amyloid-precursor protein (SW) Tg2576 transgenic mice. Neuroscience 128 (2004) 73-89
13. Billings L.M., Oddo S., Green K.N., McGaugh J.L., and LaFerla F.M. Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 45 (2005) 675-688
14. Oddo S., Billings L., Kesslak J.P., Cribbs D.H., and LaFerla F.M. Abeta immunotherapy leads to clearance of early, but not late, hyperphosphorylated tau aggregates via the proteasome. Neuron 43 (2004) 321-332
15. Lansbury P.T., and Lashuel H.A. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 443 (2006) 774-779
16. Dahlgren K.N., Manelli A.M., Stine Jr. W.B., Baker L.K., Krafft G.A., and LaDu M.J. Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J. Biol. Chem. 277 (2002) 32046-32053
17. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., and Klein W.L. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 6448-6453
18. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., and Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300 (2003) 486-489
19. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., and Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416 (2002) 535-539
20. Klyubin I., Walsh D.M., Lemere C.A., Cullen W.K., Shankar G.M., Betts V., Spooner E.T., Jiang L., Anwyl R., Selkoe D.J., and Rowan M.J. Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat. Med. 11 (2005) 556-561
21. Chafekar S.M., Hoozemans J.J., Zwart R., Baas F., and Scheper W. Abeta 1-42 induces mild endoplasmic reticulum stress in an aggregation state-dependent manner. Antioxid. Redox. Signal 9 (2007) 2245-2254
22. Eikelenboom P., Bate C., Van Gool W.A., Hoozemans J.J., Rozemuller J.M., Veerhuis R., and Williams A. Neuroinflammation in Alzheimer's disease and prion disease. Glia 40 (2002) 232-239
23. Kheterpal I., Williams A., Murphy C., Bledsoe B., and Wetzel R. Structural features of the Abeta amyloid fibril elucidated by limited proteolysis. Biochemistry 40 (2001) 11757-11767
24. Hepler R.W., Grimm K.M., Nahas D.D., Breese R., Dodson E.C., Acton P., Keller P.M., Yeager M., Wang H., Shughrue P., Kinney G., and Joyce J.G. Solution state characterization of amyloid beta-derived diffusible ligands. Biochemistry 45 (2006) 15157-15167
25. Kayed R., Sokolov Y., Edmonds B., McIntire T.M., Milton S.C., Hall J.E., and Glabe C.G. Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J. Biol. Chem. 279 (2004) 46363-46366
26. Ward R.V., Jennings K.H., Jepras R., Neville W., Owen D.E., Hawkins J., Christie G., Davis J.B., George A., Karran E.H., and Howlett D.R. Fractionation and characterization of oligomeric, protofibrillar and fibrillar forms of beta-amyloid peptide. Biochem. J. 348 Pt 1 (2000) 137-144
27. Hansen S.H., Sandvig K., and van Deurs B. Molecules internalized by clathrin-independent endocytosis are delivered to endosomes containing transferrin receptors. J. Cell Biol. 123 (1993) 89-97
28. van Deurs B., Roepstorff K., Hommelgaard A.M., and Sandvig K. Caveolae: anchored, multifunctional platforms in the lipid ocean. Trends Cell Biol. 13 (2003) 92-100
29. Rodal S.K., Skretting G., Garred O., Vilhardt F., van Deurs B., and Sandvig K. Extraction of cholesterol with methyl-beta-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell. 10 (1999) 961-974
30. Subtil A., Gaidarov I., Kobylarz K., Lampson M.A., Keen J.H., and McGraw T.E. Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 6775-6780
31. Sengupta P., Garai K., Sahoo B., Shi Y., Callaway D.J., and Maiti S. The amyloid beta peptide (Abeta(1-40)) is thermodynamically soluble at physiological concentrations. Biochemistry 42 (2003) 10506-10513
32. Huang T.H., Yang D.S., Plaskos N.P., Go S., Yip C.M., Fraser P.E., and Chakrabartty A. Structural studies of soluble oligomers of the Alzheimer beta-amyloid peptide. J. Mol. Biol. 297 (2000) 73-87
33. Bateman D.A., McLaurin J., and Chakrabartty A. Requirement of aggregation propensity of Alzheimer amyloid peptides for neuronal cell surface binding. BMC Neurosci. 8 (2007) 29
34. Fiala M., Lin J., Ringman J., Kermani-Arab V., Tsao G., Patel A., Lossinsky A.S., Graves M.C., Gustavson A., Sayre J., Sofroni E., Suarez T., Chiappelli F., and Bernard G. Ineffective phagocytosis of amyloid-beta by macrophages of Alzheimer's disease patients. J. Alzheimers Dis. 7 (2005) 221-232 (discussion 255-62)
35. Koenigsknecht J., and Landreth G. Microglial phagocytosis of fibrillar beta-amyloid through a beta1 integrin-dependent mechanism. J. Neurosci. 24 (2004) 9838-9846
36. Chithrani B.D., Ghazani A.A., and Chan W.C. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 6 (2006) 662-668
37. Chithrani B.D., and Chan W.C. Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett. 7 (2007) 1542-1550
38. Wakabayashi M., Okada T., Kozutsumi Y., and Matsuzaki K. GM1 ganglioside-mediated accumulation of amyloid beta-protein on cell membranes. Biochem. Biophys. Res. Commun. 328 (2005) 1019-1023
39. Matsuzaki K., Noguch T., Wakabayashi M., Ikeda K., Okada T., Ohashi Y., Hoshino M., and Naiki H. Inhibitors of amyloid beta-protein aggregation mediated by GM1-containing raft-like membranes. Biochim. Biophys. Acta 1768 (2007) 122-130
40. Kawarabayashi T., Shoji M., Younkin L.H., Wen-Lang L., Dickson D.W., Murakami T., Matsubara E., Abe K., Ashe K.H., and Younkin S.G. Dimeric amyloid beta 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
41. Yamamoto N., Fukata Y., Fukata M., and Yanagisawa K. GM1-ganglioside-induced Abeta assembly on synaptic membranes of cultured neurons. Biochim. Biophys. Acta 1768 (2007) 1128-1137
42. Kim S.I., Yi J.S., and Ko Y.G. Amyloid beta oligomerization is induced by brain lipid rafts. J. Cell Biochem. 99 (2006) 878-889
43. Maxfield F.R., and McGraw T.E. Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5 (2004) 121-132
44. Ghosh R.N., Gelman D.L., and Maxfield F.R. Quantification of low density lipoprotein and transferrin endocytic sorting HEp2 cells using confocal microscopy. J. Cell Sci. 107 Pt 8 (1994) 2177-2189
45. Nagele R.G., D'Andrea M.R., Anderson W.J., and Wang H.Y. Intracellular accumulation of beta-amyloid(1-42) in neurons is facilitated by the alpha 7 nicotinic acetylcholine receptor in Alzheimer's disease. Neuroscience 110 (2002) 199-211
46. Wang H.Y., Lee D.H., D'Andrea M.R., Peterson P.A., Shank R.P., and Reitz A.B. beta-Amyloid(1-42) binds to alpha7 nicotinic acetylcholine receptor with high affinity. Implications for Alzheimer's disease pathology. J. Biol. Chem. 275 (2000) 5626-5632
47. Liu Z., Tearle A.W., Nai Q., and Berg D.K. Rapid activity-driven SNARE-dependent trafficking of nicotinic receptors on somatic spines. J. Neurosci. 25 (2005) 1159-1168
48. Langui D., Girardot N., El Hachimi K.H., Allinquant B., Blanchard V., Pradier L., and Duyckaerts C. Subcellular topography of neuronal Abeta peptide in APPxPS1 transgenic mice. Am. J. Pathol. 165 (2004) 1465-1477
49. Sasaki N., Toki S., Chowei H., Saito T., Nakano N., Hayashi Y., Takeuchi M., and Makita Z. Immunohistochemical distribution of the receptor for advanced glycation end products in neurons and astrocytes in Alzheimer's disease. Brain Res. 888 (2001) 256-262
50. Yang A.J., Chandswangbhuvana D., Margol L., and Glabe C.G. Loss of endosomal/lysosomal membrane impermeability is an early event in amyloid Abeta1-42 pathogenesis. J. Neurosci. Res. 52 (1998) 691-698
51. Knauer M.F., Soreghan B., Burdick D., Kosmoski J., and Glabe C.G. Intracellular accumulation and resistance to degradation of the Alzheimer amyloid A4/beta protein. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 7437-7441
52. Ditaranto K., Tekirian T.L., and Yang A.J. Lysosomal membrane damage in soluble Abeta-mediated cell death in Alzheimer's disease. Neurobiol. Dis. 8 (2001) 19-31
53. Kroemer G., and Jaattela M. Lysosomes and autophagy in cell death control. Nat. Rev. Cancer 5 (2005) 886-897
54. Cataldo A.M., Peterhoff C.M., Troncoso J.C., Gomez-Isla T., Hyman B.T., and Nixon R.A. Endocytic pathway abnormalities precede amyloid beta deposition in sporadic Alzheimer's disease and Down syndrome: differential effects of APOE genotype and presenilin mutations. Am. J. Pathol. 157 (2000) 277-286
55. Gouras G.K., Tsai J., Naslund J., Vincent B., Edgar M., Checler F., Greenfield J.P., Haroutunian V., Buxbaum J.D., Xu H., Greengard P., and Relkin N.R. Intraneuronal Abeta42 accumulation in human brain. Am. J. Pathol. 156 (2000) 15-20
56. Pasternak S.H., Bagshaw R.D., Guiral M., Zhang S., Ackerley C.A., Pak B.J., Callahan J.W., and Mahuran D.J. Presenilin-1, nicastrin, amyloid precursor protein, and gamma-secretase activity are co-localized in the lysosomal membrane. J. Biol. Chem. 278 (2003) 26687-26694
57. Mathews P.M., Guerra C.B., Jiang Y., Grbovic O.M., Kao B.H., Schmidt S.D., Dinakar R., Mercken M., Hille-Rehfeld A., Rohrer J., Mehta P., Cataldo A.M., and Nixon R.A. Alzheimer's disease-related overexpression of the cation-dependent mannose 6-phosphate receptor increases Abeta secretion: role for altered lysosomal hydrolase distribution in beta-amyloidogenesis. J. Biol. Chem. 277 (2002) 5299-5307
58. Grbovic O.M., Mathews P.M., Jiang Y., Schmidt S.D., Dinakar R., Summers-Terio N.B., Ceresa B.P., Nixon R.A., and Cataldo A.M. Rab5-stimulated up-regulation of the endocytic pathway increases intracellular beta-cleaved amyloid precursor protein carboxyl-terminal fragment levels and Abeta production. J. Biol. Chem. 278 (2003) 31261-31268
59. Koo E.H., and Squazzo S.L. Evidence that production and release of amyloid beta-protein involves the endocytic pathway. J. Biol. Chem. 269 (1994) 17386-17389
60. Cirrito J.R., Kang J.E., Lee J., Stewart F.R., Verges D.K., Silverio L.M., Bu G., Mennerick S., and Holtzman D.M. Endocytosis is required for synaptic activity-dependent release of amyloid-beta in vivo. Neuron 58 (2008) 42-51
61. Cataldo A.M., Hamilton D.J., Barnett J.L., Paskevich P.A., and Nixon R.A. Abnormalities of the endosomal-lysosomal system in Alzheimer's disease: relationship to disease pathogenesis. Adv. Exp. Med. Biol. 389 (1996) 271-280
62. Nixon R.A., Cataldo A.M., and Mathews P.M. The endosomal-lysosomal system of neurons in Alzheimer's disease pathogenesis: a review. Neurochem. Res. 25 (2000) 1161-1172
63. Yang A.J., Knauer M., Burdick D.A., and Glabe C. Intracellular A beta 1-42 aggregates stimulate the accumulation of stable, insoluble amyloidogenic fragments of the amyloid precursor protein in transfected cells. J. Biol. Chem. 270 (1995) 14786-14792
64. Mazziotti M., and Perlmutter D.H. Resistance to the apoptotic effect of aggregated amyloid-beta peptide in several different cell types including neuronal- and hepatoma-derived cell lines. Biochem. J. 332 Pt 2 (1998) 517-524
65. Cecchi C., Rosati F., Pensalfini A., Formigli L., Nosi D., Liguri G., Dichiara F., Morello M., Danza G., Pieraccini G., Peri A., Serio M., and Stefani M. Seladin-1/DHCR24protects neuroblastoma cells against Abeta toxicity by increasing membrane cholesteral content. J. Cell Mol. Med. (2008)
66. Ferrera P., Mercado-Gomez O., Silva-Aguilar M., Valverde M., and Arias C. Cholesterol potentiates beta-amyloid-induced toxicity in human neuroblastoma cells: involvement of oxidative stress. Neurochem. Res. (2008)
67. Sponne I., Fifre A., Koziel V., Oster T., Olivier J.L., and Pillot T. Membrane cholesterol interferes with neuronal apoptosis induced by soluble oligomers but not fibrils of amyloid-beta peptide. Faseb J. 18 (2004) 836-838
68. Subasinghe S., Unabia S., Barrow C.J., Mok S.S., Aguilar M.I., and Small D.H. Cholesterol is necessary both for the toxic effect of Abeta peptides on vascular smooth muscle cells and for Abeta binding to vascular smooth muscle cell membranes. J. Neurochem. 84 (2003) 471-479
69. Wang S.S., Rymer D.L., and Good T.A. Reduction in cholesterol and sialic acid content protects cells from the toxic effects of beta-amyloid peptides. J. Biol. Chem. 276 (2001) 42027-42034
70. Oddo S., Caccamo A., Smith I.F., Green K.N., and LaFerla F.M. A dynamic relationship between intracellular and extracellular pools of Abeta. Am. J. Pathol. 168 (2006) 184-194