Protein aggregation in a membrane environment

Advances in Protein Chemistry and Structural Biology

Volumn 84, Issue , 2011, Pages 113-142

  Gorbenko, Galyna ^a   Trusova, Valeriya ^a  

^a V N KARAZIN KHARKIV NATIONAL UNIVERSITY   (Ukraine)

Author keywords

lipid bilayer; membrane mediated amyloid nucleation; protein aggregation propensity; protein structural changes

Indexed keywords

EID: 80051875060     PISSN: 18761623     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386483-3.00002-1     Document Type: Chapter

References (127)

1. B.D. Adair, and D.M. Engelman Glycophorin A helical transmembrane domains dimerize in phospholipid bilayers: a resonance energy transfer study Biochemistry 33 1994 5539 5544 (Pubitemid 24162990)
2. S. Adams, A.M. Higgins, and R.A.L. Jones Surface-mediated folding and misfolding of proteins at lipid/water interfaces Langmuir 18 2002 4854 4861 (Pubitemid 35383559)
3. C. Aisenbrey, B. Bechinger, and G. Gröbner Macromolecular crowding at membrane interfaces: adsorption and alignment of membrane peptides J. Mol. Biol. 375 2008 376 385 (Pubitemid 350199664)
4. C. Aisenbrey, T. Borowik, M. Bokvist, F. Lindström, M. Sani, and A. Olofsson Disordered proteins: biological membranes as two-dimensional aggregation matrices Cell Biochem. Biophys. 52 2008 175 189
5. C. Aisenbrey, T. Borowik, R. Byström, M. Bokvist, F. Lindström, and H. Misiak How is protein aggregation in amyloidogenic diseases modulated by biological membranes? Eur. Biophys. J. 37 2008 247 255
6. J.M. Alakoskela, A. Jutila, A.C. Simonsen, J. Pirneskoski, S. Pyhäjoki, and R. Turunen Characteristics of fibers formed by cytochrome c and induced by anionic phospholipids Biochemistry 45 2006 13447 13453 (Pubitemid 44748491)
7. A. Auger Biological membrane structure by solid-state NMR Curr. Issues Mol. Biol. 2 2000 119 124
8. A. Benda, M. Benes, V. Marecek, A. Lhotsky, W.T. Hermens, and M. Hof How to determine diffusion coefficients in planar phospholipid systems by confocal fluorescence correlation spectroscopy Langmuir 19 2003 4120 4126
9. K. Beyer Mechanistic aspects of Parkinson's disease: α-synuclein and the biomembrane Cell Biochem. Biophys. 47 2007 285 299 (Pubitemid 47338366)
10. G. Binnig, C.F. Quate, and C. Gerber Atomic force microscope Phys. Rev. Lett. 56 1986 930 933
11. J.F. Boas, S.C. Drew, and C.C. Curtain Applications of electron paramagnetic resonance to studies of neurological disease Eur. Biophys. J. 37 2008 281 294
12. M. Bogdanov, E. Mileykovskaya, and W. Dowhan Lipids in the assembly of membrane proteins and organization of protein supercomplexes: implications for lipid-linked disorders Subcell. Biochem. 49 2008 197 239
13. M. Bokvist, F. Lindström, A. Watts, and G. Gröbner Two types of Alzheimer's β-amyloid (1-40) peptide membrane interactions: aggregation preventing transmembrane anchoring versus accelerated surface fibril formation J. Mol. Biol. 335 2004 1039 1049 (Pubitemid 38091609)
14. R. Bruinsma, and P. Pincus Protein aggregation in membranes Curr. Opin. Solid State Mater. Sci. 1 1996 401 406 (Pubitemid 126407987)
15. P. Butko, F. Huang, M. Pusztai-Carey, and W.K. Surewicz Interaction of the δ-endotoxin cytA from Bacillus thuringiensis var. israelensis with lipid membranes Biochemistry 36 1997 12862 12868 (Pubitemid 27465397)
16. R. Byström, C. Aisenbrey, T. Borowik, M. Bokvist, F. Lindström, and M. Sani Disordered proteins: biological membranes as two-dimensional aggregation matrices Cell Biochem. Biophys. 52 2008 175 189
17. G. Cevc Membrane electrostatics Biochim. Biophys. Acta 1031 1990 311 382
18. F. Chiti, and C.M. Dobson Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366 (Pubitemid 44118036)
19. F. Chiti, M. Stefani, N. Taddei, G. Ramponi, and C.M. Dobson Rationalization of the effects of mutations on peptide and protein aggregation rates Nature 424 2003 805 808 (Pubitemid 37021713)
20. L.P. Choo-Smith, W. Garzon-Rodriguez, C.G. Glabe, and W.K. Surewicz Acceleration of amyloid fibril formation by specific binding of Aβ-(1-40) peptide to ganglioside-containing membrane vesicles J. Biol. Chem. 272 1997 22987 22990 (Pubitemid 27392420)
21. A. Choucair, B. Chakravarthy, J. Katsaras, and L.J. Johnston Preferential accumulation of Aβ (1-42) on gel phase domains of lipid bilayers: an AFM and fluorescence study Biochim. Biophys. Acta 1768 2007 146 154 (Pubitemid 44909080)
22. A.S. Cohen, and S.E. Calkin Electron microscopic observations on a fibrous component in amyloid of diverse origins Nature 183 1959 1202 1203
23. O. Conchillo-Solé, N.S. de Groot, F.X. Avilés, J. Vendrell, X. Daura, and S. Ventura AGGRESCAN: a server for the prediction and evaluation of "hot spots" of aggregation in polypeptides BMC Bioinformatics 8 2007 65 82
24. M. del Mar Martinez-Senac, J. Villalain, and J.C. Gomez-Fernandez Structure of the Alzheimer β-amyloid peptide (25-35) and its interaction with negatively charged phospholipid vesicles Eur. J. Biochem. 265 1999 744 753 (Pubitemid 29489007)
25. K.A. Dill Dominant forces in protein folding Biochemistry 29 1990 7133 7155 (Pubitemid 20230041)
26. c to form β-sheet using NMR structures and sequence alignments Biophys. J. 83 2002 1268 1280 (Pubitemid 34977702)
27. F. Ding, N.V. Dokholyan, S.V. Buldyrev, H.E. Stanley, and E.I. Shakhnovich Molecular dynamic simulation of the SH3 domain aggregation suggests a generic amyloidogenesis mechanism J. Mol. Biol. 324 2002 851 857 (Pubitemid 36044117)
28. C.M. Dobson Protein folding and misfolding Nature 426 2003 884 890 (Pubitemid 38056880)
29. C.M. Dobson Experimental investigation of protein folding and misfolding Methods 34 2004 4 14 (Pubitemid 38993205)
30. Ye.A. Domanov, and P.K.J. Kinnunen Islet amyloid polypeptide forms rigid lipid-protein amyloid fibrils on supported phospholipid bilayers J. Mol. Biol. 376 2008 42 54
31. C. Esposito, A.M. Tedeschi, M. Scrima, G. D'Errico, M.F. Ottaviani, and P. Rovero Exploring interaction of β-amyloid segment (25-35) with membrane models through paramagnetic probes J. Pept. Sci. 12 2006 766 774 (Pubitemid 44941578)
32. J.S. Evans Biomolecular NMR 1995 Oxford University Press Oxford
33. M.H. Fagan, and T.G. Dewey Resonance energy transfer study of membrane-bound aggregates of the sarcoplasmic reticulum calcium ATP J. Biol. Chem. 261 1986 3651 3660
34. A. Fernandez, and R.S. Berry Extent of hydrogen-bond protection in folded proteins: a constraint on packing architectures Biophys. J. 83 2002 2475 2481 (Pubitemid 35265741)
35. A. Fernandez, and R.S. Berry Proteins with H-bond packing defects are highly interactive with lipid bilayers: implications for amyloidogenesis Proc. Natl. Acad. Sci. USA 100 2003 2391 2396 (Pubitemid 36297509)
36. A. Fernandez, J. Kardos, L.R. Scott, Y. Goto, and R.S. Berry Structural defects and the diagnosis of amyloidogenic propensity Proc. Natl. Acad. Sci. USA 100 2003 6446 6451 (Pubitemid 36666601)
37. A. Fernandez, and R. Scott Dehydron: a structurally encoded signal for protein interaction Biophys. J. 85 2003 1914 1928 (Pubitemid 37052271)
38. A.L. Fink Protein aggregation: folding aggregates, inclusion bodies and amyloid Fold. Des. 3 1998 R9 R23
39. J.J. Fung, X. Deup, L. Pardo, X.J. Yao, G.L. Velez-Ruiz, and B.T. DeVree Ligand-regulated oligomerization of β2-adrenoceptors in a model lipid bilayer EMBO J. 28 2009 3315 3328
40. C.E. Giacomelli, and W. Norde Conformational changes of the amyloid beta-peptide (1-40) adsorbed on solid surfaces Macromol. Biosci. 5 2005 401 407 (Pubitemid 40813976)
41. T. Gil, J.H. Ipsen, O.G. Mouritsen, M.C. Sabra, M.M. Sperotto, and M.J. Zuckermann Theoretical analysis of protein organization in lipid membranes Biochim. Biophys. Acta 1376 1998 245 266 (Pubitemid 28517880)
42. G.P. Gorbenko Structure of cytochrome c complexes with phospholipids as revealed by resonance energy transfer Biochim. Biophys. Acta 1420 1999 1 13 (Pubitemid 29369013)
43. G.P. Gorbenko, V.M. Ioffe, and P.K.J. Kinnunen Binding of lysozyme to phospholipid bilayers: evidence for protein aggregation upon membrane association Biophys. J. 93 2007 140 153 (Pubitemid 47041658)
44. G.P. Gorbenko, and P.K.J. Kinnunen The role of lipid-protein interactions in amyloid-type protein fibril formation Chem. Phys. Lipids 141 2006 72 82 (Pubitemid 43728804)
45. S.L. Grage, S. Afonin, M. Grüne, and A.S. Ulrich Interaction of the fusogenic peptide B18 in its amyloid-state with lipid membranes studied by solid state NMR Chem. Phys. Lipids 132 2004 65 77 (Pubitemid 39458321)
46. N.J. Greenfield Using circular dichroism spectra to estimate protein secondary structure Nat. Protoc. 1 2006 2876 2890
47. S. Grudzielanek, V. Smirnovas, and R. Winter The effects of various membrane physical-chemical properties on the aggregation kinetics of insulin Chem. Phys. Lipids 149 2007 28 39 (Pubitemid 47090182)
48. J. Gsponer, and M. Vendruscolo Theoretical approaches to protein aggregation Protein Pept. Lett. 13 2006 287 293
49. C.A. Haynes, and W. Norde Structures and stabilities of adsorbed proteins J. Colloid Interface Sci. 169 1995 313 328
50. J.A. Hebda, and A.D. Miranker The interplay of catalysis and toxicity by amyloid intermediates on lipid bilayers: insights from type II diabetes Annu. Rev. Biophys. 38 2009 125 152
51. A. Hermetter, and J.R. Lakowicz The aggregation state of mellitin in lipid bilayers. An energy transfer study J. Biol. Chem. 261 1986 8243 8248 (Pubitemid 17202695)
52. S.A. Hudson, H. Ecroyd, T.W. Kee, and J.A. Carver The thioflavin T fluorescence assay for amyloid fibril detection can be biased by the presence of exogenous compounds FEBS J. 276 2009 5960 5972
53. A. Hung, M.D. Griffin, G.J. Howlett, and I. Yarovsky Effects of oxidation, pH and lipids on amyloidogenic peptide structure: implications for fibril formation Eur. Biophys. J. 38 2008 99 110
54. J. Janson, R.H. Ashley, D. Harrison, S. McIntyre, and P.C. Butler The mechanism of islet amyloid polypeptide toxicity is membrane disruption by intermediate-sized toxic amyloid particles Diabetes 48 1999 491 498 (Pubitemid 29106861)
55. E. John, and F. Jähnig Aggregation state of mellitin in lipid vesicle membranes Biophys. J. 60 1991 319 328
56. F. Kamp, and K. Beyer Binding of alpha-synuclein affects the lipid packing in bilayers of small vesicles J. Biol. Chem. 281 2006 9251 9259 (Pubitemid 43864640)
57. R. Kayed, J. Bernhagen, N. Greenfield, K. Sweimeh, H. Brunner, and W. Voelter Conformational transitions of islet amyloid polypeptide (IAPP) in amyloid formation in vitro J. Mol. Biol. 287 1999 781 795
58. J. Kazlauskaite, N. Sanghera, I. Sylvester, C. Venien-Bryan, and T.J.T. Pinheiro Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization Biochemistry 42 2003 3295 3304 (Pubitemid 36348638)
59. J.W. Kelly Towards an understanding of amyloidogenesis Nat. Struct. Biol. 9 2002 323 325 (Pubitemid 34462546)
60. S.D. Khare, and N.V. Dokholyan Molecular mechanisms of polypeptide aggregation in human diseases Curr. Protein Pept. Sci. 8 2007 573 579 (Pubitemid 351266990)
61. S.A. Kim, and P. Schwille Intracellular applications of fluorescence correlation spectroscopy: prospects for neuroscience Curr. Opin. Neurobiol. 13 2003 583 590 (Pubitemid 37431187)
62. J.D. Knight, J.A. Hebda, and A.D. Miranker Conserved and cooperative assembly of membrane-bound alpha-helical states of islet amyloid polypeptide Biochemistry 45 2006 9496 9508 (Pubitemid 44223253)
63. J.D. Knight, and A.D. Miranker Phospholipid catalysis of diabetic amyloid assembly J. Mol. Biol. 341 2004 1175 1187 (Pubitemid 39099208)
64. V. Koppaka, and P.H. Axelsen Accelerated accumulation of amyloid β proteins on oxidatively damaged lipid membranes Biochemistry 39 2000 10011 10016 (Pubitemid 30626852)
65. M.R.H. Krebs, E.H.C. Bromley, and A.M. Donald The binding of Thioflavin T to amyloid fibrils: localisation and implications J. Struct. Biol. 149 2005 30 37 (Pubitemid 40051399)
66. J.R. Lakowicz Principles of Fluorescence Spectroscopy 3rd edn. 2006 Springer New York
67. A.G. Lee How lipids affect the activities of integral membrane proteins Biochim. Biophys. Acta 1666 2004 62 87 (Pubitemid 39425199)
68. H. LeVine III Stopped-flow kinetics reveal multiple phases of Thioflavin T binding to Alzheimer β(1-40) amyloid fibrils Arch. Biochem. Biophys. 342 1997 306 316
69. M. Li, L.G. Reddy, R. Bennett, N.D. Silva, J. Larry, and R. Jones A fluorescence energy transfer method for analyzing protein oligomeric structure: application to phospholamban Biophys. J. 76 1999 2587 2599 (Pubitemid 29264618)
70. J.W. Lichtman, and J.A. Conchello Fluorescence microscopy Nat. Methods 2 2005 910 919 (Pubitemid 43108727)
71. M. Lindgren, K. Sorgjerd, and P. Hammarstrom Detection and characterization of aggregates, prefibrillar amyloidogenic oligomers, and protofibrils using fluorescence spectroscopy Biophys. J. 88 2005 4200 4212 (Pubitemid 40991131)
72. F. Lindstöm, M. Bokvist, T. Sparrman, and G. Gröbner Association of amyloid-β peptide with membrane surfaces monitored by solid state NMR Phys. Chem. Chem. Phys. 4 2002 5524 5530
73. A. Lomakin, G.B. Benedek, and D.B. Teplow Monitoring protein assembly using quasielastic light scattering spectroscopy Methods Enzymol. 309 1999 429 459 (Pubitemid 29446464)
74. D. Marsh, A. Watts, R.D. Pates, and R. Uhl EPR spin-label studies of lipid-protein interactions in membranes Biophys. J. 37 1982 265 274
75. I.C. Martins, I. Kuperstein, H. Wilkinson, E. Maes, M. Vanbrabant, and W. Jonckheere Lipids revert inert Aβ amyloid fibrils to neurotoxic protofibrils that affect learning in mice EMBO J. 27 2008 224 233
76. M. Mauro, E.F. Craparo, A. Podesta, D. Bulone, R. Carrotta, and V. Martorana Kinetics of different processes in human insulin amyloid formation J. Mol. Biol. 366 2007 258 274 (Pubitemid 46123327)
77. J. McLaurin, A.A. Darabie, and M.R. Morrison Cholesterol, a modulator of membrane-associated Aβ-fibrillogenesis Ann. N. Y. Acad. Sci. 977 2002 376 383
78. X. Meng, A.L. Fink, and V.N. Uversky The effect of membranes on the in vitro fibrillation of an amyloidogenic light chain variable domain J. Mol. Biol. 381 2008 989 999
79. F. Meyer, M. Venturoli, and B. Smit Molecular simulations of lipid-mediated protein-protein interactions Biophys. J. 95 2008 1851 1865
80. M. Morillas, W. Swietnicki, P. Gambetti, and W.K. Surewicz Membrane environment alters the conformational structure of the recombinant human prion protein J. Biol. Chem. 274 1999 36859 36865
81. A.M. Morris, M.A. Watzky, and R.G. Finke Protein aggregation kinetics, mechanism, and curve-fitting: a review of the literature Biochim. Biophys. Acta 1794 2009 375 397
82. A. Muga, J.M. Gonzalez-Manas, J.H. Lakey, F. Pattus, and W.K. Surewicz pH-dependent stability and membrane interaction of the pore-forming domain of colicin A J. Biol. Chem. 268 1993 1553 1557 (Pubitemid 23033540)
83. A. Muga, H.H. Mantsch, and W.K. Surewicz Membrane binding induces destabilization of cytochrome c structure Biochemistry 30 1991 7219 7224
84. Mulgrew-Nesbitt A., Diraviyam K., Wang J., Singh S., Murray P., Li Z., Rogers L., Mirkovi N., and Murray D. The role of electrostatics in protein-membrane interactions. Biochim. Biophys. Acta. 1761 2006 812 826 (Pubitemid 44332331)
85. L.A. Munishkina, E.M. Cooper, V.N. Uversky, and A.L. Fink The effect of macromolecular crowding on protein aggregation and amyloid fibril formation J. Mol. Recognit. 17 2004 1 9
86. K. Murakami, K. Irie, A. Morimoto, H. Ohigashi, M. Shindo, and M. Nagao Neurotoxicity and physicochemical properties of Aβ mutant peptides from cerebral amyloid angiopathy: implication for the pathogenesis of cerebral amyloid angiopathy and Alzheimer's disease J. Biol. Chem. 278 2003 46179 46187 (Pubitemid 37432769)
87. A. Naito, and I. Kawamura Solid-state NMR as a method to reveal structure and membrane-interaction of amyloidogenic proteins and peptides Biochim. Biophys. Acta 1768 2007 1900 1912 (Pubitemid 47125853)
88. M.R. Nilsson Techniques to study amyloid fibril formation in vitro Methods 34 2004 151 160 (Pubitemid 38993215)
89. A. Olofsson, T. Borowik, G. Grobner, and A.E. Sauer-Eriksson Negatively charged phospholipid membranes induce amyloid formation of medin via an alpha-helical intermediate J. Mol. Biol. 374 2007 186 194 (Pubitemid 47600226)
90. A.P. Pandey, F. Haque, J.C. Rochet, and J.S. Hovis Clustering of α-synuclein on supported lipid bilayers: role of anionic lipid, protein, and divalent ion concentration Biophys. J. 96 2009 540 551
91. N.A. Pavlov, D.I. Cherny, G. Heim, T.M. Jovin, and V. Subramaniam Amyloid fibrils from the mammalian protein prothymosin FEBS Lett. 517 2002 37 40 (Pubitemid 34327627)
92. T.J.T. Pinheiro, G.A. Elove, A. Watts, and H. Roder Structural and kinetic description of cytochrome c unfolding induced by the interaction with lipid vesicles Biochemistry 36 1997 13122 13132 (Pubitemid 27465428)
93. J.L. Popot, and D.M. Engelman Helical membrane protein folding, stability and evolution Annu. Rev. Biochem. 69 2000 881 922
94. S. Ravault, O. Soubias, O. Saurel, A. Thomas, T. Brasseur, and A. Milon Fusogenic Alzheimer's peptide fragment Aβ (29-42) in interaction with lipid bilayers: secondary structure, dynamics, and specific interaction with phosphatidylethanolamine polar heads as revealed by solid-state NMR Protein Sci. 14 2005 1181 1189 (Pubitemid 40577798)
95. A. Relini, O. Cavalleri, R. Rolandi, and A. Gliozzi The two-fold aspect of the interplay of amyloidogenic proteins with lipid membranes Chem. Phys. Lipids 158 2009 1 9
96. E. Rhoades, T.F. Ramlall, W.W. Webb, and D. Eliezery Quantification of α-synuclein binding to lipid vesicles using fluorescence correlation spectroscopy Biophys. J. 90 2006 4692 4700 (Pubitemid 43830913)
97. P. Robustelli, A. Cavalli, and M. Vendruscolo Determination of protein structures in the solid state from NMR chemical shifts Structure 16 2008 1764 1769
98. Z. Salamon, and G. Tollin Surface plasmon resonance studies of complex formation between cytochrome c and bovine cytochrome c oxidase incorporated into a supported planar lipid bilayer. I. Binding of cytochrome c to cardiolipin/phosphatidylcholine membranes in the absence of oxidase Biophys. J. 71 1996 848 857 (Pubitemid 26289168)
99. N. Sanghera, and T.J. Pinheiro Binding of prion protein to lipid membranes and implications for prion conversion J. Mol. Biol. 315 2002 1241 1256 (Pubitemid 34729301)
100. J. Seelig Thermodynamics of lipid-peptide interactions Biochim. Biophys. Acta 1666 2004 40 50 (Pubitemid 39425197)
101. L.C. Serpell Alzheimer's amyloid fibrils: structure and assembly Biochim. Biophys. Acta 1502 2000 16 30 (Pubitemid 30433852)
102. J.S. Sharp, J.A. Forrest, and R.A.L. Jones Surface denaturation and amyloid fibril formation of insulin at model lipid-water interfaces Biochemistry 41 2002 15810 15819 (Pubitemid 36062486)
103. I. Shin, D. Kreimer, I. Silman, and L. Weiner Membrane-promoted unfolding of acetylcholinesterase: a possible mechanism for insertion into the lipid bilayer Proc. Natl. Acad. Sci. USA 94 1997 2848 2852 (Pubitemid 27157227)
104. B.M. Smith, L. Oswald, and S. Franzen Single-pass attenuated total reflection Fourier transform infrared spectroscopy for the prediction of protein secondary structure Anal. Chem. 74 2002 3386 3391 (Pubitemid 34764944)
105. E. Sparr, M.F.M. Engel, D.V. Sakharov, M. Sprong, J. Jacobs, and B. de Kruijf Islet amyloid polypeptide-induced membrane leakage involves uptake of lipids by forming amyloid fibers FEBS Lett. 577 2004 117 120 (Pubitemid 39452370)
106. M. Stefani Protein misfolding and aggregation: new examples in medicine and biology of the dark side of the protein world Biochim. Biophys. Acta 1739 2004 5 25 (Pubitemid 39647706)
107. M. Stefani Protein folding and misfolding on surfaces Int. J. Mol. Sci. 9 2008 2515 2542
108. M. Stefani, and C. Dobson Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution J. Mol. Med. 81 2003 678 699 (Pubitemid 37491594)
109. B.J. Tabner, O.M.A. El-Agnaf, M.J. German, N.J. Fullwood, and D. Allso Protein aggregation, metals and oxidative stress in neurodegenerative diseases Biochem. Soc. Trans. 33 2005 1082 1086 (Pubitemid 41659118)
110. S.A. Tatulian, R.L. Biltonen, and L.K. Tamm Structural changes in a secretory phospholipase A2 induced by membrane binding: a clue to interfacial activation? J. Mol. Biol. 268 1997 809 815 (Pubitemid 27229165)
111. E. Terzi, G. Holzemann, and J. Seelig Self-association of beta-amyloid peptide (1-40) in solution and binding to lipid membranes J. Mol. Biol. 252 1995 633 642
112. V.M. Trusova Intrinsic fluorescence of lysozyme in model protein-lipid systems Biophys. Bull. 22 2009 62 67
113. V.N. Uversky, and A.L. Fink Conformational constraints for amyloid fibrillation: the importance of being unfolded Biochim. Biophys. Acta 1698 2004 131 153 (Pubitemid 38591469)
114. V.N. Uversky, J. Li, and A.L. Fink Evidence for a partially folded intermediate in alpha-synuclein fibril formation J. Biol. Chem. 276 2001 10737 10744 (Pubitemid 38089246)
115. F.G. van der Goot, J.M. González-Mañas, J.H. Lakey, and F. Pattus A 'molten-globule' membrane-insertion intermediate of the pore-forming domain of colicin A Nature 354 1991 408 410 (Pubitemid 21896852)
116. W. van Klompenburg, I. Nilsson, G. von Heijne, and B. de Kruijff Anionic phospholipids are determinants of membrane protein topology EMBO J. 16 1997 4261 4266 (Pubitemid 27298178)
117. S. Ventura, J. Zurdo, S. Narayanan, M. Parreno, R. Mangues, and B. Reif Short amino acid stretches can mediate amyloid formation in globular proteins: the Src homology 3 (SH3) case Proc. Natl. Acad. Sci. USA 101 2004 77258 77263
118. W.C. Wimley, and S.H. White Experimentally determined hydrophobicity scale for proteins at membrane interfaces Nat. Struct. Biol. 3 1996 842 848 (Pubitemid 26330634)
119. A. Woehler, J. Wlodarczyk, and E.G. Ponimaskin Specific oligomerization of the 5-HT1A receptor in the plasma membrane Glycoconj. J. 26 2009 749 756
120. H. Wojtasek, and W.S. Leal Conformational change in the pheromone-binding protein from Bombyx mori induced by pH and by interaction with membranes J. Biol. Chem. 274 1999 30950 30956
121. E.K.L. Yeow, and H.A. Clayton Enumeration of oligomerization states of membrane proteins in living cells by homo-FRET spectroscopy and microscopy: theory and application Biophys. J. 92 2007 3098 3104 (Pubitemid 46684571)
122. C.M. Yip, A.A. Darabie, and J. McLaurin Aβ42-peptide assembly on lipid bilayers J. Mol. Biol. 318 2002 97 107
123. J.P. Zbilut, A. Colosimo, F. Conti, M. Colafranceschi, C. Manetti, and M. Valerio Protein aggregation/folding: the role of deterministic singularities of sequence hydrophobicity as determined by nonlinear signal analysis of acylphosphatase and Aβ (1-40) Biophys. J. 85 2003 3544 3557 (Pubitemid 37490270)
124. A. Zemel, A. Ben-Shaul, and S. May Membrane perturbation induced by interfacially absorbed peptides Biophys. J. 86 2004 3607 3619 (Pubitemid 38780240)
125. H. Zhao, E.K.J. Tuominen, and P.K.J. Kinnunen Formation of amyloid fibers triggered by phosphatidylserine-containing membranes Biochemistry 43 2004 10302 10307 (Pubitemid 39079303)
126. V.P. Zhdanov, and B. Kasemo Protein adsorption and desorption on lipid bilayers Biophys. Chem. 146 2010 60 64
127. M. Zhu, J. Li, and A.L. Fink The association of α-synuclein with membranes affects bilayer structure, stability and fibril formation J. Biol. Chem. 278 2003 40186 40197 (Pubitemid 37248587)