The mechanism of membrane disruption by cytotoxic amyloid oligomers formed by prion protein(106-126) is dependent on bilayer composition

Journal of Biological Chemistry

Volumn 289, Issue 15, 2014, Pages 10419-10430

  Walsh, Patrick ^a,b   Vanderlee, Gillian ^c   Yau, Jason ^a,b   Campeau, Jody ^d   Sim, Valerie L ^d   Yip, Christopher M ^b,c   Sharpe, Simon ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ATOMIC FORCE MICROSCOPY; CELL DEATH; CYTOTOXICITY; GLYCOPROTEINS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OLIGOMERS; PEPTIDES; REFRACTIVE INDEX;

ANTI-MICROBIAL ACTIVITY; ANTIMICROBIAL PEPTIDE; BILAYER COMPOSITIONS; FIBRILLAR AGGREGATES; MEMBRANE DISRUPTION; NEURODEGENERATIVE DISORDERS; ORGANOTYPIC CULTURE; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY;

MEMBRANES;

OLIGOMER; PRION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE; CELL SEPARATION; CONTROLLED STUDY; CYTOTOXICITY; DEUTERON NUCLEAR MAGNETIC RESONANCE; MEMBRANE DAMAGE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL;

AMYLOID; AMYLOID OLIGOMERS; ATOMIC FORCE MICROSCOPY; CYTOTOXICITY; MEMBRANE BILAYER; MEMBRANE DISRUPTION; PEPTIDES; SOLID STATE NMR; TIRF;

AMYLOID; ANIMALS; ANTIMICROBIAL CATIONIC PEPTIDES; CELL MEMBRANE; CEREBELLUM; CHOLESTEROL; DETERGENTS; ESCHERICHIA COLI; LIPID BILAYERS; LIPIDS; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED C57BL; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; ORGAN CULTURE TECHNIQUES; PC12 CELLS; PEPTIDE FRAGMENTS; PHOSPHATIDYLCHOLINES; PRIONS; RATS;

EID: 84898638427     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.515866     Document Type: Article

References (82)

1. Glenner, G. G., and Wong, C. W. (1984) Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochem. Biophys. Res. Commun. 120, 885-890
2. Prusiner, S. B. (1982) Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144
3. Spillantini, M. G., Schmidt, M. L., Lee, V. M., Trojanowski, J. Q., Jakes, R., and Goedert, M. (1997) α-Synuclein in Lewy bodies. Nature 388, 839-840
4. Baglioni, S., Casamenti, F., Bucciantini, M., Luheshi, L. M., Taddei, N., Chiti, F., Dobson, C. M., and Stefani, M. (2006) Prefibrillar amyloid aggregates could be generic toxins in higher organisms. J. Neurosci. 26, 8160-8167
5. Kayed, R., Head, E., Thompson, J. L., McIntire, T. M., Milton, S. C., Cot- man, C. W., and Glabe, C. G. (2003) Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300, 486-489
6. 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. (1998) Diffusible, nonfibrillar ligands derived from A β1-42 are potent central nervous system neurotoxins. Proc. Natl. Acad. Sci. U.S.A. 95, 6448-6453
7. Walsh, D. M., and Selkoe, D. J. (2004) Oligomers on the brain: the emerging role of soluble protein aggregates in neurodegeneration. Protein Pept. Lett. 11, 213-228
8. 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 conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases. J. Biol. Chem. 279, 46363-46366
9. 2+-sensitive channel in reconstituted lipid vesicles. Biochemistry 38, 11189-11196
10. Pollard, H. B., Arispe, N., and Rojas, E. (1995) Ion channel hypothesis for Alzheimer amyloid peptide neurotoxicity. Cell. Mol. Neurobiol. 15, 513-526
11. Walsh, D. M., and Selkoe, D. J. (2007) Aβ oligomers-A decade of discovery. J. Neurochem. 101, 1172-1184
12. Quist, A., Doudevski, I., Lin, H., Azimova, R., Ng, D., Frangione, B., Kagan, B., Ghiso, J., and Lal, R. (2005) Amyloid ion channels: A common structural link for protein misfolding disease. Proc. Natl. Acad. Sci. U.S.A. 102, 10427-10432
13. Bemporad, F., and Chiti, F. (2012) Protein misfolded oligomers: experimental approaches, mechanism of formation, and structure-toxicity relationships. Chem. Biol. 19, 315-327
14. Fandrich, M. (2012) Oligomeric intermediates in amyloid formation: Structure determination and mechanisms of toxicity. J. Mol. Biol. 421, 427-440
15. Kayed, R., Pensalfini, A., Margol, L., Sokolov, Y., Sarsoza, F., Head, E., Hall, J., and Glabe, C. (2009) Annular protofibrils are a structurally and functionally distinct type of amyloid oligomer. J. Biol. Chem. 284, 4230-4237
16. Brender, J. R., Salamekh, S., and Ramamoorthy, A. (2012) Membrane disruption and early events in the aggregation of the diabetes related peptide IAPP from a molecular perspective. Acc. Chem. Res. 45, 454-462
17. Shai, Y. (1999) Mechanism of the binding, insertion, and destabilization of phospholipid bilayer membranes by β-helical antimicrobial and cell nonselective membrane-lytic peptides. Biochim. Biophys. Acta 1462, 55-70
18. Yeaman, M. R., and Yount, N. Y. (2003) Mechanisms of antimicrobial peptide action and resistance. Pharmacol. Rev. 55, 27-55
19. Yip, C. M., Darabie, A. A., and McLaurin, J. (2002)Aβ42-peptide assembly on lipid bilayers. J. Mol. Biol. 318, 97-107
20. Yip, C. M., Elton, E. A., Darabie, A. A., Morrison, M. R., and McLaurin, J. (2001) Cholesterol, a modulator of membrane-associated Aβ- fibrillogenesis and neurotoxicity. J. Mol. Biol. 311, 723-734
21. Williamson, R., and Sutherland, C. (2011) Neuronal membranes are key to the pathogenesis of Alzheimers disease: the role of both raft and non-raft membrane domains. Curr. Alzheimer Res. 8, 213-221
22. Castro, B. M., de Almeida, R. F., Goormaghtigh, E., Fedorov, A., and Prieto, M. (2011) Organization and dynamics of Fas transmembrane domain in raft membranes and modulation by ceramide. Biophys. J. 101, 1632-1641
23. Gajate, C., Gonzalez-Camacho, F., and Mollinedo, F. (2009) Lipid raft connection between extrinsic and intrinsic apoptotic pathways. Biochem. Biophys. Res. Commun. 380, 780-784
24. Forloni, G., Angeretti, N., Chiesa, R., Monzani, E., Salmona, M., Bugiani, O., and Tagliavini, F. (1993) Neurotoxicity of a prion protein fragment. Nature 362, 543-546
25. Salmona, M., Malesani, P., De Gioia, L., Gorla, S., Bruschi, M., Molinari, A., Della Vedova, F., Pedrotti, B., Marrari, M. A., Awan, T., Bugiani, O., Forloni, G., and Tagliavini, F. (1999) Molecular determinants of the physicochemical properties of a critical prion protein region comprising residues 106-126. Biochem. J. 342, 207-214
26. Selvaggini, C., De Gioia, L., Cantu, L., Ghibaudi, E., Diomede, L., Passerini, F., Forloni, G., Bugiani, O., Tagliavini, F., and Salmona, M. (1993) Molecular characteristics of a protease-resistant, amyloidogenic and neurotoxic peptide homologous to residues 106-126 of the prion protein. Biochem. Biophys. Res. Commun. 194, 1380-1386
27. Brown, D. R. (1998) Prion protein-overexpressing cells show altered response to a neurotoxic prion protein peptide. J. Neurosci. Res. 54, 331-340
28. Deli, M. A., Sakaguchi, S., Nakaoke, R., Abraham, C. S., Takahata, H., Kopacek, J., Shigematsu, K., Katamine, S., and Niwa, M. (2000) PrP fragment 106-126 is toxic to cerebral endothelial cells expressing PrP(C). Neuroreport 11, 3931-3936
29. Fioriti, L., Quaglio, E., Massignan, T., Colombo, L., Stewart, R. S., Salmona, M., Harris, D. A., Forloni, G., and Chiesa, R. (2005) The neurotoxicity of prion protein (PrP) peptide 106-126 is independent of the expression level of PrP and is not mediated by abnormal PrP species. Mol. Cell. Neurosci. 28, 165-176
30. Kurganov, B., Doh, M., and Arispe, N. (2004) Aggregation of liposomes induced by the toxic peptides Alzheimer's Aβs, human amylin and prion(106-126): facilitation by membrane-bound GM1 ganglioside. Peptides 25, 217-232
31. Thellung, S., Florio, T., Villa, V., Corsaro, A., Arena, S., Amico, C., Robello, M., Salmona, M., Forloni, G., Bugiani, O., Tagliavini, F., and Schettini, G. (2000) Apoptotic cell death and impairment of L-type voltage-sensitive calcium channel activity in rat cerebellar granule cells treated with the prion protein fragment 106-126. Neurobiol. Dis. 7, 299-309
32. Salmona, M., Forloni, G., Diomede, L., Algeri, M., De Gioia, L., Angeretti, N., Giaccone, G., Tagliavini, F., and Bugiani, O. (1997) A neurotoxic and gliotrophic fragment of the prion protein increases plasma membrane microviscosity. Neurobiol. Dis. 4, 47-57
33. Carimalo, J., Cronier, S., Petit, G., Peyrin, J. M., Boukhtouche, F., Arbez, N., Lemaigre-Dubreuil, Y., Brugg, B., and Miquel, M. C. (2005) Activation of the JNK-c-Jun pathway during the early phase of neuronal apoptosis induced by PrP106-126 and prion infection. Eur. J. Neurosci. 21, 2311-2319
34. Kourie, J. I., Farrelly, P. V., and Henry, C. L. (2001) Channel activity of deamidated isoforms of prion protein fragment 106-126 in planar lipid bilayers. J. Neurosci. Res. 66, 214-220
35. Lin, M. C., Mirzabekov, T., and Kagan, B. (1997) Channel formation by a neurotoxic prion protein fragment. J. Biol. Chem. 272, 44-47
36. Ettaiche, M., Pichot, R., Vincent, J. P., and Chabry, J. (2000) In vivo cytotoxicity of the prion protein fragment 106-126. J. Biol. Chem. 275, 36487-36490
37. Walsh, P., Neudecker, P., and Sharpe, S. (2010) Structural properties and dynamic behaviour of non-fibrillar oligomers formed by PrP(106-126). J. Am. Chem. Soc. 132, 7684-7695
38. Walsh, P., Simonetti, K., and Sharpe, S. (2009) Core structure of amyloid fibrils formed by residues 106-126 of the human prion protein. Structure 17, 417-426
39. Walsh, P., Yau, J., Simonetti, K., and Sharpe, S. (2009) Morphology and secondary structure of stable β-oligomers formed by the amyloid peptide PrP(106-126). Biochemistry 48, 5779-5781
40. Oreopoulos, J., and Yip, C. M. (2009) Probing membrane order and topography in supported lipid bilayers by combined polarized total internal reflection fluorescence atomic force microscopy. Biophys. J. 96, 1970-1984
41. Falsig, J., and Aguzzi, A. (2008) The prion organotypic slice culture assay-POSCA. Nat. Protoc. 3, 555-562
42. Miret, S., De Groene, E. M., and Klaffke, W. (2006) Comparison of in vitro assays of cellular toxicity in the human hepatic cell line HepG2. J. Biomol. Screen. 11, 184-193
43. Bertrand, R., Solary, E., O'Connor, P., Kohn, K. W., and Pommier, Y. (1994) Induction of a common pathway of apoptosis by staurosporine. Exp. Cell Res. 211, 314-321
44. Moore, A., Donahue, C. J., Bauer, K. D., and Mather, J. P. (1998) Simultaneous measurement of cell cycle and apoptotic cell death. Methods Cell Biol. 57, 265-278
45. Mor, A., Nguyen, V. H., Delfour, A., Migliore-Samour, D., and Nicolas, P. (1991) Isolation, amino acid sequence, and synthesis of dermaseptin, a novel antimicrobial peptide of amphibian skin. Biochemistry 30, 8824-8830
46. Domingues, T. M., Riske, K. A., and Miranda, A. (2010) Revealing the lytic mechanism of the antimicrobial peptide gomesin by observing giant unilamellar vesicles. Langmuir 26, 11077-11084
47. Russell, A. L., Kennedy, A. M., Spuches, A. M., Venugopal, D., Bhonsle, J. B., and Hicks, R. P. (2010) Spectroscopic and thermodynamic evidence for antimicrobial peptide membrane selectivity. Chem. Phys. Lipids 163, 488-497
48. Kendall, D. A., and MacDonald, R. C. (1982) A fluorescence assay to monitor vesicle fusion and lysis. J. Biol. Chem. 257, 13892-13895
49. Yip, C. M., and McLaurin, J. (2001) Amyloid-β peptide assembly: a critical step in fibrillogenesis and membrane disruption. Biophys. J. 80, 1359-1371
50. Nagle, J. F., and Tristram-Nagle, S. (2000) Structure of lipid bilayers. Biochim. Biophys. Acta 1469, 159-195
51. Kučerka, N., Nieh, M.-P., and Katsaras, J. (2011) Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature. Biochim. Biophys. Acta 1808, 2761-2771
52. Seelig, J. (1978) 31P nuclear magnetic resonance and the head group structure of phospholipids in membranes. Biochim. Biophys. Acta 515, 105-140
53. Ramamoorthy, A., Thennarasu, S., Lee, D. K., Tan, A., and Maloy, L. (2006) Solid-state NMR investigation of the membrane-disrupting mechanism of antimicrobial peptides MSI-78 and MSI-594 derived from magainin 2 and melittin. Biophys. J. 91, 206-216
54. Baumgart, T., Hunt, G., Farkas, E. R., Webb, W. W., and Feigenson, G. W. (2007) Fluorescence probe partitioning between Lo/Ld phases in lipid membranes. Biochim. Biophys. Acta 1768, 2182-2194
55. Feigenson, G. W. (2006) Phase behavior of lipid mixtures. Nat. Chem. Biol. 2, 560-563
56. Hicks, D. A., Nalivaeva, N. N., and Turner, A. J. (2012) Lipid rafts and Alzheimer's disease: protein-lipid interactions and perturbation of signaling. Front. Physiol. 3, 189
57. Malchiodi-Albedi, F., Paradisi, S., Matteucci, A., Frank, C., and Diociaiuti, M. (2011) Amyloid oligomer neurotoxicity, calcium dysregulation, and lipid rafts. Int. J. Alzheimers Dis. 10.4061/2011/906964
58. Wood, W. G., Schroeder, F., Igbavboa, U., Avdulov, N. A., and Chochina, S. V. (2002) Brain membrane cholesterol domains, aging and amyloid peptides. Neurobiol. Aging 23, 685-694
59. Korlach, J., Schwille, P., Webb, W. W., and Feigenson, G. W. (1999) Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 96, 8461-8466
60. Axelrod, D. (1989) in Fluorescence Polarization Microscopy (Langsing, T., and Wang, Y., eds) Vol. 30, pp. 333-352, Academic Press, San Diego
61. Timbs, M. M., and Thompson, N. L. (1990) Slow rotational mobilities of antibodies and lipids associated with substrate-supported phospholipid monolayers as measured by polarized fluorescence photobleaching recovery. Biophys. J. 58, 413-428
62. Spink, C. H., Yeager, M. D., and Feigenson, G. W. (1990) Partitioning behavior of indocarbocyanine probes between coexisting gel and fluid phases in model membranes. Biochim. Biophys. Acta 1023, 25-33
63. Oreopoulos, J., and Yip, C. M. (2009) Combinatorial microscopy for the study of protein-membrane interactions in supported lipid bilayers: Order parameter measurements by combined polarized TIRFM/AFM. J. Struct. Biol. 168, 21-36
64. Taylor, M. G., Akiyama, T., Saito, H., and Smith, I. C. (1982) Direct observation of the properties of cholesterol in membranes by deuterium NMR. Chem. Phys. Lipids. 31, 359-379
65. Glabe, C. G. (2006) Common mechanisms of amyloid oligomer pathogenesis in degenerative disease. Neurobiol. Aging 27, 570-575
66. Florio, T., Thellung, S., Amico, C., Robello, M., Salmona, M., Bugiani, O., Tagliavini, F., Forloni, G., and Schettini, G. (1998) Prion protein fragment 106-126 induces apoptotic cell death and impairment of L-type voltagesensitive calcium channel activity in the GH3 cell line. J. Neurosci. Res. 54, 341-352
67. Silei, V., Fabrizi, C., Venturini, G., Salmona, M., Bugiani, O., Tagliavini, F., and Lauro, G. M. (1999) Activation of microglial cells by PrP and β-amyloid fragments raises intracellular calcium through L-type voltage sensitive calcium channels. Brain Res. 818, 168-170
68. Zhong, J., Zheng, W., Huang, L., Hong, Y., Wang, L., Qiu, Y., and Sha, Y. (2007) PrP106-126 amide causes the semi-penetrated poration in the supported lipid bilayers. Biochim. Biophys. Acta 1768, 1420-1429
69. Brown, D. R., Schmidt, B., and Kretzschmar, H. A. (1996) Role of microglia and host prion protein in neurotoxicity of a prion protein fragment. Nature 380, 345-347
70. Gu, Y., Fujioka, H., Mishra, R. S., Li, R., and Singh, N. (2002) Prion peptide 106-126 modulates the aggregation of cellular prion protein and induces the synthesis of potentially neurotoxic transmembrane PrP. J. Biol. Chem. 277, 2275-2286
71. Pietri, M., Caprini, A., Mouillet-Richard, S., Pradines, E., Ermonval, M., Grassi, J., Kellermann, O., and Schneider, B. (2006) Overstimulation of PrPC signaling pathways by prion peptide 106-126 causes oxidative injury of bioaminergic neuronal cells. J. Biol. Chem. 281, 28470-28479
72. Brender, J. R., Durr, U. H., Heyl, D., Budarapu, M. B., and Ramamoorthy, A. (2007) Membrane fragmentation by an amyloidogenic fragment of human islet amyloid polypeptide detected by solid-state NMR spectroscopy of membrane nanotubes. Biochim. Biophys. Acta 1768, 2026-2029
73. Kagan, B. L., Jang, H., Capone, R., Teran Arce, F., Ramachandran, S., Lal, R., and Nussinov, R. (2012) Antimicrobial activities of amyloid peptides. Mol. Pharm. 9, 708-717
74. McMullen, T. P., Lewis, R. N., and McElhaney, R. N. (2004) Cholesterolphospholipid interactions, the liquid-ordered phase and lipid rafts in model and biological membranes. Curr. Opin. Colloid Interface Sci. 8, 459-468
75. Owen, D. M., Williamson, D. J., Magenau, A., and Gaus, K. (2012) Subresolution lipid domains exist in the plasma membrane and regulate protein diffusion and distribution. Nat. Commun. 3, 1256
76. Kaiser, H.-J., Lingwood, D., Levental, I., Sampaio, J. L., Kalvodova, L., Rajendran, L., and Simons, K. (2009) Order of lipid phases in model and plasma membranes. Proc. Natl. Acad. Sci. U.S.A. 106, 16645-16650
77. George, K. S., and Wu, S. (2012) Lipid raft: A floating island of death or survival. Toxicol. Appl. Pharmacol. 259, 311-319
78. 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
79. Bucciantini, M., Nosi, D., Forzan, M., Russo, E., Calamai, M., Pieri, L., Formigli, L., Quercioli, F., Soria, S., Pavone, F., Savistchenko, J., Melki, R., and Stefani, M. (2012) Toxic effects of amyloid fibrils on cell membranes: the importance of ganglioside GM1. FASEB J. 26, 818-831
80. Comellas, G., Lemkau, L. R., Zhou, D. H., George, J. M., and Rienstra, C. M. (2012) Structural intermediates during α-synuclein fibrillogenesis on phospholipid vesicles. J. Am. Chem. Soc. 134, 5090-5099
81. Lu, J. X., Yau, W. M., and Tycko, R. (2011) Evidence from solid-stateNMR for nonhelical conformations in the transmembrane domain of the amyloid precursor protein. Biophys. J. 100, 711-719
82. Smith, P. E., Brender, J. R., and Ramamoorthy, A. (2009) Induction of negative curvature as a mechanism of cell toxicity by amyloidogenic peptides: the case of islet amyloid polypeptide. J. Am. Chem. Soc. 131, 4470-4478