Influence of oligomeric and fibrillar lysozyme on physical properties of model membranes
Keywords:
amyloid lysozyme, oligomers, fibrils, pyrene, Laurdan, membrane fluidity, dehydration
Abstract
A pathological hallmark of more than 20 human diseases including Alzheimer’s disease, Parkinson’s
disease, type II diabetes is the deposition in organs and tissues of insoluble highly ordered protein
aggregates, called amyloid fibrils. It is becoming widely recognized that toxicity of amyloid species is
related to their interactions with cell membranes. In the present study we focused our efforts on the
examination of the influence of amyloid fibrils and their precursors (oligomeric aggregates) of lysozyme
on the structural and physical properties of the model membranes composed of phosphatidylcholine and
its mixture with cholesterol. For evaluating the extent of lipid bilayer modifications, we used fluorescence
spectroscopy technique. The results of pyrene excimerization measurements showed that amyloid protein
reduces membrane fluidity. Analysis of Laurdan emission spectra revealed the ability of lysozyme
aggregates to produce bilayer dehydration. The most pronounced membrane-modifying effects were
observed in the case of oligomeric lysozyme. Significantly less influence of pathogenic protein
aggregates on the physical properties of cholesterol-containing vesicles confirmed the hypothesis on the
preventive role of cholesterol in amyloid-related diseases.
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References
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2. Butterflied S.M., Laushel H.A. Amyloidogenic protein-membrane interactions: mechanistic insight from model systems // Angew. Chem. Int. Ed. – 2010. – V. 49. – P. 5628-5654.
3. Kayed R., Head E., Thompson J.L., McIntire T.M, Milton S.C., Cotman C.W. Common structure of so-luble amyloid oligomers implies common mechanism of pathogenesis // Science. – 2003. – V. 300. – P. 486-489.
4. Glabe C.G. Common mechanisms of amyloid oligomer pathogenesis in degenerative disease // Neuro-biol. Aging. – 2006. – V. 27. – P. 570-575.
5. Chiti F., Webster P., Taddei N., Clark A., Stefani M., Ramoni G., Dobson C. M. Designing conditions for in vitro formation of amyloid protofilaments and fibrils // Proc. Nat. Acad. Sci. U.S.A. – 1999. - V. 96. – P. 3590–3594.
6. Tycko R. Progress towards a molecular-level structural understanding of amyloid fibrils // Curr. Opin. Struct. Biol. – 2004. – V. 14. – P. 96-103.
7. Stefani M. Protein Folding and Misfolding on Surfaces // Int. J. Mol. Sci. – 2008. – V. 9. – P. 2515-2542.
8. Capone R., Garcia Quiroz F., Prangkio P., Saluja I., Sauer A.M., Bautista M.R., Turner R.S., Yang J., Mayer M. Amyloid-β-Induced Ion Flux in Artificial Lipid Bilayers and Neuronal Cells: Resolving a Controversy // Neurotox. Res. – 2009. – V. 16. – P. 1-13.
9. Kayed R., Sokolov Y., Edmonds B., McIntire T.M, Milton S.C., Hall J.E., Glabe C.G. Permeabilization of Lipid bilayers Is a Common conformation-dependent activity of Soluble amyloid oligomers in pro-tein misfolding diseases // J. Biol. Chem. – 2004. – V. 279, № 45. – P. 46363–46366.
10. Valincius G., Heinrich F., Budvytyte R. Soluble Amyloid b-Oligomers Affect Dielectric Membrane Properties by Bilayer Insertion and Domain Formation: Implications for Cell Toxicity // Biophys. J. – 2008. – V. 95. – P. 4845–4861.
11. Van Rooijen B.D., Claessens M.M.A.E., Subramaniam V. Membrane Permeabilization by Oligomeric α-Synuclein: In Search of the Mechanism // PLoS ONE. – 2010. – V. 5(12): e14292.
12. Cehhi C., Baglioni S., Fiorillo C., Pensalfini A., Liguri G., Nosi D., Rigacci S., Bucciantini M., Stefani M. Insights into the molecular basis of the differing susceptibility of varying cell types to the toxicity of amyloid aggregates // J. Cell Sci. – 2005. – V. 118. – P. 3459-3470.
13. Ma X, Sha Y., Lin K., Nie S. The Effect of Fibrillar Aβ1-40 on Membrane Fluidity and Permeability // Protein Pept. Lett. – 2002. – V. 9, No 2. – P. 173-178.
14. Novitskaya V., Bocharova O.V., Bronstein I., Baskakov I.V. Amyloid fibrils of mammalian prion pro-tein are highly toxic to cultured cells and primary neurons // J. Biol. Chem. – 2006. – V. 281. – P. 13828–13836.
15. Gharibyan A.L., Zamotin V., Yanamandra K, Moskaleva O.S., Margulis B.A., Kostanyan I.A., Moro-zova-Roche L.A. Lysozyme amyloid oligomers and fibrils induce cellular death via different apop-totic/necrotic pathways // J. Mol. Biol. – 2007. – V.365. – P. 1337-13349.
16. Wang S. S.-S., Liu K.-N. Membrane dipole potential of interaction between amyloid protein and phos-pholipid membranes is dependent on protein aggregation state // J. Chin. Inst. Chem. Eng. – 2008. – V. 39. – P. 321-328.
17. Huang B., He J., Ren J., Yan X.-Y., Zeng C.-M. Cellular membrane disruption by amyloid fibrils in-volved intermolecular disulfide cross-linking // Biochemistry. – 2009. – V. 48. P. 5794–5800.
18. Jayasinghe S.A., Langen R. Membrane interaction of islet amyloid polypeptide // Biochim. Biophys. Acta. – 2007. – V. 1768. – P. 2002–2009.
19. Friedman R., Pellarin R., Caflisch A. Amyloid Aggregation on Lipid Bilayers and Its Impact on Mem-brane Permeability // J. Mol. Biol. – 2009. – V. 387 (2). – P. 407-415.
20. Stefani M. Biochemical and biophysical features of both oligomer/fibril and cell membrane in amyloid cytotoxicity // FEBS Journal. – 2010. – V. 277. – P. 4602–4613.
21. Lee Y.J., Savtchenko R., Ostapchenko V.G., Makarava N., Baskakov I.V. Molecular Structure of Amy-loid Fibrils Controls the Relationship between Fibrillar Size and Toxicity // PLoS ONE. – 2011. – V. 6(5): e20244.
22. Mossuto M.F., Dhulesia A., Devlin G., Frare E., Kumita J.R., Polverino de Laureto P., Dumoulin M., Fontana A., Dobson C.M., Salvatella X. The Non-Core Regions of Human Lysozyme Amyloid Fibrils Influence Cytotoxicity // J. Mol. Biol. – 2010. – V. 402(5-2). – P. 783–796.
23. Holley M., Eginton C., Schaefer D., Brown L. R. Characterization of amyloidogenesis of hen egg ly-sozyme in concentrated ethanol solution // Biochem. Biophys. Res. Commun. – 2008. – V. 373. – P. 164-168.
24. Parasassi T., Krasnowska E.K, Bagatolli L., Gratton E. Laurdan and Prodan as polarity-sensitive fluo-rescent membrane probes // J. Fluorescence.– 1998. – V. 8. – P. 365-373.
25. Lakowicz J. R. Principles of Fluorescent Spectroscopy, third ed., Springer, New York. 2006.
26. Novikov E.G., Visser N.V., Malevitskaia V.G., Borst W., van Hoek A., Visser A. Molecular dynamics of monopyrenyl lipids in liposomes from global analysis of time-resolved fluorescence of pyrene monomer and excimer emission // Langmuir. – 2000. – V. 16. – P. 8749-8754.
27. Lheurerx G.P., Fragata M., Monomeric and aggregated pyrene and 16-(1-pyrenyl)hexadecanoic acid in small, unilamellar phosphatidylcholine vesicles and ethanol-buffer solutions // J. Photochem. Photobiol. B: Biol. – 1989. – V. 3. – P. 53-63.
28. Kremer J.J., Pallitto M.M., Sklansky D.J., Murphy R.M. Correlation of beta-amyloid aggregate size and hydrophobicity with decreased bilayer fluidity of model membranes // Biochemistry. – 2000. – V. 39 (33). – P. 10309-10318.
29. Widenbrant M.J.O., Rajadas J., Sutardja C., Fuller G.G. Lipid-Induced b-Amyloid Peptide Assemblage Fragmentation // Biophys. J. – 2006. – V. 91. – P. 4071–4080.
30. Askarova S., Yang X., Lee J. C.-M. Impacts of Membrane Biophysics in Alzheimer’s Disease: From Amyloid Precursor Protein Processing to Aβ Peptide-Induced Membrane Changes // Int. J. Alzheimer’s Dis. – 2011. – V. 2011. – ID 134971.
31. Muller W.E., Kirsch C., Eckert G.P. Membrane-disordering effects of b-amyloid peptides // Biochem. Soc. Trans. – 2001. V. 29. – P. 617-624.
32. Sponne I., Fifre A., Koziel V., Oster T., Oliver J.-L., Pilot T. Membrane cholesterol interferes with neu-ronal apoptosis induced by soluble oligomers but not fibrils of amyloid-β peptide // FASEB J. – 2004. V. 18. – P. 836-838.
33. Eckert G.P., Kirsch C., Muller W.E. Brain-membrane cholesterol in Alzheimer’s disease // Journal of Nutrition, Health and Aging. – 2003. – V. 7 (1). – P. 18–23.
34. Wolozin B. Cholesterol and the Biology of Alzheimer’s Disease // Neuron. – 2004. – V. 41. – P. 7–10.
35. Micelli S., Meleleo D., Picciarelli V., Gallucci E. Effect of Sterols on b-Amyloid Peptide AβP 1–40) Channel Formation and their Properties in Planar Lipid Membranes // Biophys. J. – 2004. – V. 86. – P. 2231–2237.
Cited
How to Cite
Kastorna, A. P., Trusova, V. M., & Gorbenko, G. P. (1). Influence of oligomeric and fibrillar lysozyme on physical properties of model membranes. Biophysical Bulletin, 1(26). Retrieved from https://periodicals.karazin.ua/biophysvisnyk/article/view/2709
Section
Cell biophysics
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