Visualization of co-localization in Aβ42-administered neuroblastoma cells reveals lysosome damage and autophagosome accumulation related to cell death

Biochemical Journal

Volumn 441, Issue 2, 2012, Pages 579-590

  Soura, Violetta ^a   Stewart Parker, Maris ^a   Williams, Thomas L ^a,c   Ratnayaka, Arjuna ^a   Atherton, Joe ^a   Gorringe, Kirsti ^a   Tuffin, Jack ^a   Darwent, Elisabeth ^a   Rambaran, Roma ^a   Klein, William ^b   Lacor, Pascale ^b   Staras, Kevin ^a   Thorpe, Julian ^a   Serpell, Louise C ^a  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b NORTHWESTERN UNIVERSITY   (United States)

^c DREXEL UNIVERSITY   (United States)

Author keywords

Alzheimer's disease; Amyloid peptide (1 42) (A 42); Autophagosome; Lysosome; Oligomer

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; CATHEPSIN D; CLATHRIN; OLIGOMER;

ARTICLE; AUTOPHAGOSOME; CELL DEATH; CYTOTOXICITY; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOGOLD ELECTRON MICROSCOPY; INTERNALIZATION; LYSOSOME; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LOCALIZATION;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AUTOPHAGY; CATHEPSIN D; CELL LINE, TUMOR; CLATHRIN; HIPPOCAMPUS; HUMANS; LYSOSOMES; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; NEUROBLASTOMA; PEPTIDE FRAGMENTS;

EID: 84555187703     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110749     Document Type: Article

References (41)

1. Selkoe, D. J. (1991) The molecular pathology of Alzheimer's disease. Neuron 6, 487-498
2. Bitan, G., Frandinger, E. A., Spring, S. and Teplow, D. (2005) Neurotoxic protein oligomers: what you see is not always what you get. Amyloid 2, 88-95 (Pubitemid 40978716)
3. Glabe, C. G. and Kayed, R. (2006) Common structure and toxic function of amyloid oligomers implies a common mechanism of pathogenesis. Neurology 66, S74-S78 (Pubitemid 43739989)
4. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cotman, C. W. and Glabe, C. G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489 (Pubitemid 36444329)
5. Yang, A. J., Chandswangbhuvana, D., Shu, T., Henschen, A. and Glabe, C. G. (1999) Intracellular accumulation of insoluble, newly synthesized Aßn-42 in amyloid precursor protein-transfected cells that have been treated with Aβ1-42. J. Biol. Chem. 274, 20650-20656
6. Williams, T. L., Day, I. J. and Serpell, L. C. (2010) The effect of Alzheimer's aβ aggregation state on the permeation of biomimetic lipid vesicles. Langmuir 26, 17260-17268
7. Liu, R. Q., Zhou, Q. H., Ji, S. R., Zhou, Q., Feng, D., Wu, Y. and Sui, S. F. (2010) Membrane localization of β-amyloid 1-42 in lysosomes: a possible mechanism for lysosome labilization. J. Biol. Chem. 285, 19986-19996
8. 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. et al. (1998) Diffusible, nonfibrillar ligands derived from Aβ1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453
9. Chen, L., Yamada, K., Nabeshima, T. and Sokabe, M. (2006) α7 Nicotinic acetylcholine receptor as a target to rescue deficit in hippocampal LTP induction in β-amyloid infused rats. Neuropharmacology 50, 254-268 (Pubitemid 43100011)
10. Vitolo, O. V., Sant'Angelo, A., Costanzo, V., Battaglia, F., Arancio, O. and Shelanski, M. (2002) Amyloid β-peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling. Proc. Natl. Acad. Sci. U.S.A. 99, 13217-13221
11. Lambert, M. P., Velasco, P. T., Chang, L., Viola, K. L., Fernandez, S., Lacor, P. N., Khuon, D., Gong, Y., Bigio, E. H., Shaw, P. et al. (2007) Monoclonal antibodies that target pathological assemblies of Aβ. J. Neurochem. 100, 23-35 (Pubitemid 46085837)
12. Lacor, P. N., Buniel, M. C., Furlow, P. W., Clemente, A. S., Velasco, P. T., Wood, M., Viola, K. L. and Klein, W. L. (2007) Aβ oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J. Neurosci. 27, 796-807 (Pubitemid 46174498)
13. Naslund, J., Jensen, M., Tjernberg, L., Thyberg, J., Terenius, L. and Nordstedt, C. (1994) The metabolic pathway generating p3, an Aβ-peptide fragment, is probably non-amyloidogenic. Biochem. Biophys. Res. Commun. 204, 780-787 (Pubitemid 24343988)
14. Skovronsky, D. M., Doms, R. W. and Lee, V. M. (1998) Detection of a novel intraneuronal pool of insoluble amyloid β protein that accumulates with time in culture. J. Cell Biol. 141, 1031-1039 (Pubitemid 28243969)
15. Gouras, G. K., Almeida, C. G. and Takahashi, R. H. (2005) Intraneuronal Aβ accumulation and origin of plaques in Alzheimer's disease. Neurobiol. Aging 26, 1235-1244 (Pubitemid 41338539)
16. Takahashi, R. H., Milner, T. A., Li, F., Nam, E. E., Edgar, M. A., Yamaguchi, H., Beal, M. F., Xu, H., Greengard, P. and Gouras, G. K. (2002) Intraneuronal Alzheimer aβ42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am. J. Pathol. 161, 1869-1879 (Pubitemid 35265544)
17. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Rowan, M. J. and Selkoe, D. J. (2002) Amyloid-β oligomers: their production, toxicity and therapeutic inhibition. Biochem. Soc. Trans. 30, 552-557 (Pubitemid 35001597)
18. Lesne, S., Koh, M. T., Kotilinek, L., Kayed, R., Glabe, C. G., Yang, A., Gallagher, M. and Ashe, K. H. (2006) A specific amyloid-β protein assembly in the brain impairs memory. Nature 440, 352-357
19. Shankar, G. M., Li, S., Mehta, T. H., Garcia-Munoz, A., Shepardson, N. E., Smith, I., Brett, F. M., Farrell, M. A., Rowan, M. J., Lemere, C. A. et al. (2008) Amyloid-β protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat. Med. 14, 837-842
20. Nixon, R. A., Wegiel, J., Kumar, A., Yu, W. H., Peterhoff, C., Cataldo, A. and Cuervo, A. M. (2005) Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J. Neuropathol. Exp. Neurol. 64, 113-122 (Pubitemid 40349309)
21. Salama, R. H., Muramatsu, H., Shimizu, E., Hashimoto, K., Ohgake, S., Watanabe, H., Komatsu, N., Okamura, N., Koike, K., Shinoda, N. et al. (2005) Increased midkine levels in sera from patients with Alzheimer's disease. Prog. Neuropsychopharmacol. Biol. Psychiatry 29, 611-616
22. Ling, D., Song, H. J., Garza, D., Neufeld, T. P. and Salvaterra, P. M. (2009) Aβ42-induced neurodegeneration via an age-dependent autophagic-lysosomal injury in Drosophila . PLoS ONE 4, e4201
23. Nixon, R. A. (2007) Autophagy, amyloidogenesis and Alzheimer disease. J. Cell Sci. 120, 4081-4091
24. Lee, J. H., Yu, W. H., Kumar, A., Lee, S., Mohan, P. S., Peterhoff, C. M., Wolfe, D. M., Martinez-Vicente, M., Massey, A. C., Sovak, G. et al. (2010) Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 141, 1146-1158
25. Yang, D. S., Stavrides, P., Mohan, P. S., Kaushik, S., Kumar, A., Ohno, M., Schmidt, S. D., Wesson, D., Bandyopadhyay, U., Jiang, Y. et al. (2011) Reversal of autophagy dysfunction in the TgCRND8 mouse model of Alzheimer's disease ameliorates amyloid pathologies and memory deficits. Brain 134, 258-277
26. Williams, T. L., Johnson, B. R., Urbanc, B., Jenkins, A. T., Connell, S. D. and Serpell, L. C. (2011) Aβ42 oligomers, but not fibrils, simultaneously bind to and cause damage to ganglioside-containing lipid membranes. Biochem. J. 439, 67-77
27. Capone, R., Quiroz, F. G., Prangkio, P., Saluja, I., Sauer, A. M., Bautista, M. R., Turner, R. S., Yang, J. and Mayer, M. (2009) Amyloid-β-induced ion flux in artificial lipid bilayers and neuronal cells: resolving a controversy. Neurotox. Res. 16, 1-13
28. Broersen, K., Jonckheere, W., Rozenski, J., Vandersteen, A., Pauwels, K., Pastore, A., Rousseau, F. and Schymkowitz, J. (2011) A standardized and biocompatible preparation of aggregate-free amyloid β peptide for biophysical and biological studies of Alzheimer's disease. Protein Eng. Des. Sel. 24, 743-750
29. Thorpe, J. R., Rulten, S. L. and Kay, J. E. (1999) Binding of a putative and a known chaperone protein revealed by immunogold labeling transmission electron microscopy: a suggested use of chaperones as probes for the distribution of their target proteins. J. Histochem. Cytochem. 47, 1633-1640
30. Thorpe, J. R. (1999) The application of LR gold resin for immunogold labeling. Methods Mol. Biol. 117, 99-110
31. Hoshino, M. and Kobayashi, H. (1971) The use of glycol methacrylate as an embedding medium for the histochemical demonstration of acid phosphatase activity. J. Histochem. Cytochem. 19, 575-577
32. Wu, F. and Yao, P. J. (2009) Clathrin-mediated endocytosis and Alzheimer's disease: an update. Ageing Res. Rev. 8, 147-149
33. Yu, W. H., Kumar, A., Peterhoff, C., Shapiro Kulnane, L., Uchiyama, Y., Lamb, B. T., Cuervo, A. M. and Nixon, R. A. (2004) Autophagic vacuoles are enriched in amyloid precursor protein-secretase activities: implications for β-amyloid peptide over-production and localization in Alzheimer's disease. Int. J. Biochem. Cell Biol. 36, 2531-2540 (Pubitemid 39119764)
34. Abramoff, M. D., Magelhaes, P. J. and Ram, S. J. (2004) Image processing with ImageJ. Biophotonics Int. 11, 36-42
35. Song, M. S., Baker, G. B., Todd, K. G. and Kar, S. (2011) Inhibition of β-amyloid-1-42 internalization attenuates neuronal death by stabilizing the endosomal-lysosomal system in rat cortical cultured neurons. Neuroscience 178, 181-188
36. Bishop, M. T., Kovacs, G. G., Sanchez-Juan, P. and Knight, R. S. (2008) Cathepsin D SNP associated with increased risk of variant Creutzfeldt-Jakob disease. BMC Med. Genet. 9, 31
37. Benes, P., Vetvicka, V. and Fusek, M. (2008) Cathepsin D: many functions of one aspartic protease. Crit. Rev. Oncol. Hematol. 68, 12-28
38. Umeda, T., Tomiyama, T., Sakama, N., Tanaka, S., Lambert, M. P., Klein, W. L. and Mori, H. (2011) Intraneuronal amyloid β oligomers cause cell death via endoplasmic reticulum stress, endosomal/lysosomal leakage, and mitochondrial dysfunction in vivo. J. Neurosci. Res. 89, 1031-1042
39. Yu, W. H., Cuervo, A. M., Kumar, A., Peterhoff, C. M., Schmidt, S. D., Lee, J. H., Mohan, P. S., Mercken, M., Farmery, M. R., Tjernberg, L. O. et al. (2005) Macroautophagy: a novel β-amyloid peptide-generating pathway activated in Alzheimer's disease. J. Cell Biol. 171, 87-98 (Pubitemid 41434604)
40. Boland, B. and Nixon, R. A. (2006) Neuronal macroautophagy: from development to degeneration. Mol. Aspects Med. 27, 503-519 (Pubitemid 44466657)
41. Walsh, D. M., Klyubin, I., Fadeeva, J. V., Cullen, W. K., Anwyl, R., Wolfe, M. S., Rowan, M. J. and Selkoe, D. J. (2002) Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 416, 535-539 (Pubitemid 34288854)