Membrane lipid composition and its physicochemical properties define cell vulnerability to aberrant protein oligomers

Journal of Cell Science

Volumn 125, Issue 10, 2012, Pages 2416-2427

  Evangelisti, Elisa ^a   Cecchi, Cristina ^a   Cascella, Roberta ^a   Sgromo, Caterina ^a   Becatti, Matteo ^a   Dobson, Christopher M ^b   Chiti, Fabrizio ^a   Stefani, Massimo ^a  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Amyloid oligomer cytotoxicity; Amyloid polymorphisms; HypF N aggregate toxicity; Membrane cholesterol; Membrane GM1

Indexed keywords

AMYLOID BETA PROTEIN; CALCIUM ION; CASPASE 3; CELL PROTEIN; CHOLESTEROL; GANGLIOSIDE GM1; MEMBRANE LIPID; OLIGOMER; PROTEIN HYPF N; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; ARTICLE; CELL FUNCTION; CELL MEMBRANE; CELL ULTRASTRUCTURE; CYTOTOXICITY; HOMEOSTASIS; HUMAN; HUMAN CELL; LIPID COMPOSITION; MEMBRANE PERMEABILITY; PHYSICAL CHEMISTRY; PRIORITY JOURNAL;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; CELL LINE, TUMOR; CELL MEMBRANE; CHOLESTEROL; G(M1) GANGLIOSIDE; HUMANS; MEMBRANE LIPIDS; PHYSICOCHEMICAL PHENOMENA;

PROKARYOTA;

EID: 84864810728     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.098434     Document Type: Article

References (55)

1. Ariga, T., Kobayashi, K., Hasegawa, A., Kiso, M., Ishida, H. and Miyatake, T. (2001). Characterization of high-affinity binding between gangliosides and amyloid beta-protein. Arch. Biochem. Biophys. 388, 225-230.
2. Bolognesi, B., Kumita, J. R., Barros, T. P., Esbjorner, E. K., Luheshi, L. M., Crowther, D. C., Wilson, M. R., Dobson, C. M., Favrin, G. and Yerbury, J. J. (2010). ANS binding reveals common features of cytotoxic amyloid species. ACS Chem. Biol. 5, 735-740.
3. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
4. Butterfield, D. A., Drake, J., Pocernich, C. and Castegna, A. (2001). Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid beta-peptide. Trends Mol. Med. 7, 548-554.
5. Campioni, S., Mannini, B., Zampagni, M., Pensalfini, A., Parrini, C., Evangelisti, E., Relini, A., Stefani, M., Dobson, C. M., Cecchi, C. et al. (2010). A causative link between the structure of aberrant protein oligomers and their toxicity. Nat. Chem. Biol. 6, 140-147.
6. Caughey, B. and Lansbury, P. T., Jr (2003). Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26, 267-298.
7. Cecchi, C., Baglioni, S., Fiorillo, C., Pensalfini, A., Liguri, G., Nosi, D., Rigacci, S., Bucciantini, M. and Stefani, M. (2005). Insights into the molecular basis of the differing susceptibility of varying cell types to the toxicity of amyloid aggregates. J. Cell Sci. 118, 3459-3470.
8. Cecchi, C., Nichino, D., Zampagni, M., Bernacchioni, C., Evangelisti, E., Pensalfini, A., Liguri, G., Gliozzi, A., Stefani,M. and Relini, A. (2009). A protective role for lipid raft cholesterol against amyloid-induced membrane damage in human neuroblastoma cells. Biochim. Biophys. Acta 1788, 2204-2216.
9. Chiti, F. and Dobson, C. M. (2006). Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75, 333-366.
10. Danzer, K. M., Haasen, D., Karow, A. R., Moussaud, S., Habeck, M., Giese, A., Kretzschmar, H., Hengerer, B. and Kostka, M. (2007). Different species of alphasynuclein oligomers induce calcium influx and seeding. J. Neurosci. 27, 9220-9232.
11. Demuro, A., Mina, E., Kayed, R., Milton, S. C., Parker, I. and Glabe, C. G. (2005). Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers. J. Biol. Chem. 280, 17294-17300.
12. Diociaiuti, M., Polzi, L. Z., Valvo, L., Malchiodi-Albedi, F., Bombelli, C. and Gaudiano, M. C. (2006). Calcitonin forms oligomeric pore-like structures in lipid membranes. Biophys. J. 91, 2275-2281.
13. Drabikowski, W., Lagwińska, E. and Sarzala, M. G. (1973). Filipin as a fluorescent probe for the location of cholesterol in the membranes of fragmented sarcoplasmic reticulum. Biochim. Biophys. Acta 291, 61-70.
14. Ehehalt, R., Keller, P., Haass, C., Thiele, C. and Simons, K. (2003). Amyloidogenic processing of the Alzheimer beta-amyloid precursor protein depends on lipid rafts. J. Cell Biol. 160, 113-123.
15. Endo, A., Kuroda, M. and Tanzawa, K. (1976). Competitive inhibition of 3-hydroxy-3-methylglutaryl coenzyme A reductase by ML-236A and ML-236B fungal metabolites, having hypocholesterolemic activity. FEBS Lett. 72, 323-326.
16. Fujita, A., Cheng, J., Hirakawa, M., Furukawa, K., Kusunoki, S. and Fujimoto, T. (2007). Gangliosides GM1 and GM3 in the living cell membrane form clusters susceptible to cholesterol depletion and chilling. Mol. Biol. Cell 18, 2112-2122.
17. Gong, Y., Chang, L., Viola, K. L., Lacor, P. N., Lambert, M. P., Finch, C. E., Krafft, G. A. and Klein, W. L. (2003). Alzheimer's disease-affected brain: presence of oligomeric A beta ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc. Natl. Acad. Sci. USA 100, 10417-10422.
18. Gorbenko, G. P. and Kinnunen, P. K. (2006). The role of lipid-protein interactions in amyloid-type protein fibril formation. Chem. Phys. Lipids 141, 72-82.
19. Hyun, D. H., Lee, M., Hattori, N., Kubo, S., Mizuno, Y., Halliwell, B. and Jenner, P. (2002). Effect of wild-type or mutant Parkin on oxidative damage, nitric oxide, antioxidant defenses, and the proteasome. J. Biol. Chem. 277, 28572-28577.
20. Kakio, A., Nishimoto, S., Yanagisawa, K., Kozutsumi, Y. and Matsuzaki, K. (2002). Interactions of amyloid beta-protein with various gangliosides in raft-like membranes: importance of GM1 ganglioside-bound form as an endogenous seed for Alzheimer amyloid. Biochemistry 41, 7385-7390.
21. Kaminski Schierle, G. S., van de Linde, S., Erdelyi, M., Esbjörner, E. K., Klein, T., Rees, E., Bertoncini, C. W., Dobson, C.M., Sauer, M. and Kaminski, C. F. (2011). In situ measurements of the formation and morphology of intracellular b-amyloid fibrils by super-resolution fluorescence imaging. J. Am. Chem. Soc. 133, 12902-12905.
22. 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.
23. Kayed, R., Sokolov, Y., Edmonds, B., McIntire, T. M., Milton, S. C., Hall, J. E. and Glabe, C. G. (2004). Permeabilization of lipid bilayers is a common conformationdependent activity of soluble amyloid oligomers in protein misfolding diseases. J. Biol. Chem. 279, 46363-46366.
24. Koffie, R. M., Meyer-Luehmann, M., Hashimoto, T., Adams, K. W., Mielke, M. L., Garcia-Alloza, M., Micheva, K. D., Smith, S. J., Kim, M. L., Lee, V. M. et al. (2009). Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proc. Natl. Acad. Sci. USA 106, 4012-4017.
25. Kourie, J. I. (2001). Mechanisms of amyloid beta protein-induced modification in ion transport systems: implications for neurodegenerative diseases. Cell. Mol. Neurobiol. 21, 173-213.
26. Lacor, P. N., Buniel, M. C., Chang, L., Fernandez, S. J., Gong, Y., Viola, K. L., Lambert, M. P., Velasco, P. T., Bigio, E. H., Finch, C. E. et al. (2004). Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J. Neurosci. 24, 10191-10200.
27. Lambert, M. P., Viola, K. L., Chromy, B. A., Chang, L., Morgan, T. E., Yu, J., Venton, D. L., Krafft, G. A., Finch, C. E. and Klein, W. L. (2001). Vaccination with soluble Abeta oligomers generates toxicity-neutralizing antibodies. J. Neurochem. 79, 595-605.
28. Lee, S., Fernandez, E. J. and Good, T. A. (2007). Role of aggregation conditions in structure, stability, and toxicity of intermediates in the Abeta fibril formation pathway. Protein Sci. 16, 723-732.
29. Lin, M. S., Chen, L. Y., Wang, S. S., Chang, Y. and Chen, W. Y. (2008). Examining the levels of ganglioside and cholesterol in cell membrane on attenuation the toxicity of beta-amyloid peptide. Colloids Surf. B Biointerfaces. 65, 173-177.
30. Lingwood, D. and Simons, K. (2010). Lipid rafts as a membrane-organizing principle. Science 327, 46-50.
31. Malchiodi-Albedi, F., Contrusciere, V., Raggi, C., Fecchi, K., Rainaldi, G., Paradisi, S., Matteucci, A., Santini, M. T., Sargiacomo, M., Frank, C. et al. (2010). Lipid raft disruption protects mature neurons against amyloid oligomer toxicity. Biochim. Biophys. Acta 1802, 406-415.
32. Martins, I. C., Kuperstein, I., Wilkinson, H., Maes, E., Vanbrabant, M., Jonckheere, W., Van Gelder, P., Hartmann, D., D'Hooge, R., De Strooper, B. et al. (2008). Lipids revert inert Abeta amyloid fibrils to neurotoxic protofibrils that affect learning in mice. EMBO J. 27, 224-233.
33. Matsuzaki, K., Kato, K. and Yanagisawa, K. (2010). Abeta polymerization through interaction with membrane gangliosides. Biochim. Biophys. Acta 1801, 868-877.
34. McLaurin, J., Franklin, T., Fraser, P. E. and Chakrabartty, A. (1998). Structural transitions associated with the interaction of Alzheimer beta-amyloid peptides with gangliosides. J. Biol. Chem. 273, 4506-4515.
35. onsson, J. E. and Fredman, P. (2005). Structural membrane alterations in Alzheimer brains found to be associated with regional disease development; increased density of gangliosides GM1 and GM2 and loss of cholesterol in detergent-resistant membrane domains. J. Neurochem. 92, 171-182.
36. Mukai, H., Isagawa, T., Goyama, E., Tanaka, S., Bence, N. F., Tamura, A., Ono, Y. and Kopito, R. R. (2005). Formation of morphologically similar globular aggregates from diverse aggregation-prone proteins in mammalian cells. Proc. Natl. Acad. Sci. USA 102, 10887-10892.
37. Nekooki-Machida, Y., Kurosawa, M., Nukina, N., Ito, K., Oda, T. and Tanaka, M. (2009). Distinct conformations of in vitro and in vivo amyloids of huntingtin-exon1 show different cytotoxicity. Proc. Natl. Acad. Sci. USA 106, 9679-9684.
38. Okada, T., Ikeda, K., Wakabayashi, M., Ogawa, M. and Matsuzaki, K. (2008). Formation of toxic Abeta(1-40) fibrils on GM1 ganglioside-containing membranes mimicking lipid rafts: polymorphisms in Abeta(1-40) fibrils. J. Mol. Biol. 382, 1066-1074.
39. Olzscha, H., Schermann, S. M., Woerner, A. C., Pinkert, S., Hecht, M. H., Tartaglia, G. G., Vendruscolo, M., Hayer-Hartl, M., Hartl, F. U. and Vabulas, R. M. (2011). Amyloid-like aggregates sequester numerous metastable proteins with essential cellular functions. Cell 144, 67-78.
40. Pensalfini, A., Zampagni, M., Liguri, G., Becatti, M., Evangelisti, E., Fiorillo, C., Bagnoli, S., Cellini, E., Nacmias, B., Sorbi, S. et al. (2011). Membrane cholesterol enrichment prevents Ab-induced oxidative stress in Alzheimer's fibroblasts. Neurobiol. Aging 32, 210-222.
41. Sethuraman, A. and Belfort, G. (2005). Protein structural perturbation and aggregation on homogeneous surfaces. Biophys. J. 88, 1322-1333.
42. Silveira, J. R., Raymond, G. J., Hughson, A. G., Race, R. E., Sim, V. L., Hayes, S. F. and Caughey, B. (2005). The most infectious prion protein particles. Nature 437, 257-261.
43. Stefani, M. (2008). Protein folding and misfolding on surfaces. Int. J. Mol. Sci. 9, 2515-2542.
44. Stefani, M. and Dobson, C. M. (2003). Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81, 678-699.
45. Tamboli, I. Y., Prager, K., Barth, E., Heneka, M., Sandhoff, K. and Walter, J. (2005). Inhibition of glycosphingolipid biosynthesis reduces secretion of the bamyloid precursor protein and amyloid b-peptide. J. Biol. Chem. 280, 28110-28117.
46. Wakabayashi, M. and Matsuzaki, K. (2007). Formation of amyloids by Abeta-(1-42) on NGF-differentiated PC12 cells: roles of gangliosides and cholesterol. J. Mol. Biol. 371, 924-933.
47. Wakabayashi, M. and Matsuzaki, K. (2009). Ganglioside-induced amyloid formation by human islet amyloid polypeptide in lipid rafts. FEBS Lett. 583, 2854-2858.
48. Wang, S. S., Good, T. A. and Rymer, D. L. (2005). The influence of phospholipid membranes on bovine calcitonin peptide's secondary structure and induced neurotoxic effects. Int. J. Biochem. Cell Biol. 37, 1656-1669.
49. Weisblum, B. and Haenssler, E. (1974). Fluorometric properties of the bibenzimidazole derivative Hoechst 33258, a fluorescent probe specific for AT concentration in chromosomal DNA. Chromosoma 46, 255-260.
50. Xue, W. F., Hellewell, A. L., Gosal, W. S., Homans, S. W., Hewitt, E. W. and Radford, S. E. (2009). Fibril fragmentation enhances amyloid cytotoxicity. J. Biol. Chem. 284, 34272-34282.
51. Yamamoto, N., Matsubara, T., Sato, T. and Yanagisawa, K. (2008). Age-dependent high-density clustering of GM1 ganglioside at presynaptic neuritic terminals promotes amyloid b-protein fibrillogenesis. Biochim. Biophys. Acta 1778, 2717-2726.
52. Yancey, P. G., Rodrigueza, W. V., Kilsdonk, E. P., Stoudt, G. W., Johnson, W. J., Phillips, M. C. and Rothblat, G. H. (1996). Cellular cholesterol efflux mediated by cyclodextrins. Demonstration of kinetic pools and mechanism of efflux. J. Biol. Chem. 271, 16026-16034.
53. Zampagni, M., Cascella, R., Casamenti, F., Grossi, C., Evangelisti, E., Wright, D., Becatti, M., Liguri, G., Mannini, B., Campioni, S. et al. (2011). A comparison of the biochemical modifications caused by toxic and non-toxic protein oligomers in cells. J. Cell. Mol. Med. 15, 2106-2116.
54. Zhou, M., Diwu, Z., Panchuk-Voloshina, N. and Haugland, R. P. (1997). A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal. Biochem. 253, 162-168.
55. Zhu, M., Souillac, P. O., Ionescu-Zanetti, C., Carter, S. A. and Fink, A. L. (2002). Surface-catalyzed amyloid fibril formation. J. Biol. Chem. 277, 50914-50922.