Membrane integrity and amyloid cytotoxicity: A model study involving mitochondria and lysozyme fibrillation products

Journal of Molecular Biology

Volumn 409, Issue 5, 2011, Pages 826-838

  Meratan, Ali Akbar ^a   Ghasemi, Atiyeh ^a   Nemat Gorgani, Mohsen ^a  

^a UNIVERSITY OF TEHRAN   (Iran)

Author keywords

cytotoxicity; hen egg white lysozyme; membrane permeabilization; mitochondria; protofibrils

Indexed keywords

AMYLOID; CYTOCHROME C; HEN EGG WHITE LYSOZYME; LYSOZYME; MITOCHONDRIAL ENZYME; MONOMER; OLIGOMER; SODIUM CHLORIDE; SPERMINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CIRCULAR DICHROISM; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DOT HYBRIDIZATION; DYNAMIC LIGHT SCATTERING; ENZYME RELEASE; FIBER; FLUORESCENCE; FLUOROMETRY; GEL PERMEATION CHROMATOGRAPHY; HYDROPHOBICITY; IN VITRO STUDY; LIGHT SCATTERING; MALE; MEMBRANE PERMEABILITY; MEMBRANE STRUCTURE; MITOCHONDRIAL MEMBRANE; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSMISSION ELECTRON MICROSCOPY;

EID: 79958032375     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.04.045     Document Type: Article

References (74)

1. Dobson C.M. The structural basis of protein folding and its links with human disease Philos. Trans. R. Soc. London, Ser. B 356 2001 133 145 (Pubitemid 32241461)
2. Stefani M., and Dobson C.M. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution J. Mol. Med. 81 2003 678 699 (Pubitemid 37491594)
3. Bucciantini M., Calloni G., Chiti F., Formigli L., Nosi D., Dobson C.M., and Stefani M. Prefibrillar amyloid protein aggregates share common features of cytotoxicity J. Biol. Chem. 279 2004 31374 31382 (Pubitemid 39037804)
4. Chiti F., Webster P., Taddei N., Clark A., Stefani M., Ramponi G., and Dobson C.M. Designing conditions for in vitro formation of amyloid protofilaments and fibrils Proc. Natl Acad. Sci. USA 96 1999 3590 3594 (Pubitemid 29168954)
5. Guijarro J.I., Sunde M., Jones J.A., Campbell I.D., and Dobson C.M. Amyloid fibril formation by an SH3 domain Proc. Natl Acad. Sci. USA 95 1998 4224 4228 (Pubitemid 28207893)
6. Harper J.D., Wong S.S., Lieber C.M., and Lansbury Jr.P.T. Observation of metastable Aβ amyloid protofibrils by atomic force microscopy Chem. Biol. 4 1997 119 125 (Pubitemid 27161750)
7. Poirier M.A., Li H., Macosko J., Cail S., Amzel M., and Ross C.A. Huntingtin spheroids and protofibrils as precursors in polyglutamine fibrillization J. Biol. Chem. 277 2002 41032 41037 (Pubitemid 35215693)
8. Conway K.A., Harper J.D., and Lansbury Jr.P.T. Fibrils formed in vitro from α-synuclein and two mutant forms linked to Parkinson's disease are typical amyloid Biochemistry 39 2000 2552 2563 (Pubitemid 30148907)
9. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., and Zurdo J. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases Nature 416 2002 507 511 (Pubitemid 34288846)
10. Klein W.L., Stine Jr.W.B., and Teplow D.B. Small assemblies of unmodified amyloid β-protein are the proximate neurotoxin in Alzheimer's disease Neurobiol. Aging 25 2004 569 580 (Pubitemid 38686476)
11. Caughey B., and Lansbury Jr.P.T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders Annu. Rev. Neurosci. 26 2003 267 298 (Pubitemid 37064935)
12. Walsh D.M., and Selkoe D.J. Oligomers on the brain: the emerging role of soluble protein aggregates in neurodegeneration Protein Pept. Lett. 11 2004 213 228 (Pubitemid 38689025)
13. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., and Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis Science 300 2003 486 489 (Pubitemid 36444329)
14. Demuro A., Mina E., Kayed R., Milton S.C., Parker I., and Glabe C.G. Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers J. Biol. Chem. 280 2005 17294 17300 (Pubitemid 41389198)
15. Kayed R., Sokolov Y., Edmonds B., McIntire T.M., Milton S.C., Hall J.E., and Glabe C.G. Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases J. Biol. Chem. 279 2004 46363 46366 (Pubitemid 39518276)
16. Green J.D., Kreplak L., Goldsbury C., Li Blatter X., Stolz M., and Cooper G.S. Atomic force microscopy reveals defects within mica supported lipid bilayers induced by the amyloidogenic human amylin peptide J. Mol. Biol. 342 2004 877 887 (Pubitemid 39165656)
17. Weise K., Radovan D., Gohlke A., Opitz N., and Winter R. Interaction of hIAPP with model raft membranes and pancreatic β-cells: cytotoxicity of hIAPP oligomers ChemBioChem 11 2010 1280 1290
18. Lin H., Bhatia R., and Lal R. Amyloid β protein forms ion channels: implications for Alzheimer's disease pathophysiology FASEB J. 15 2001 2433 2444 (Pubitemid 33063171)
19. Lashuel H.A., Hartley D., Petre B.M., Walz T., and Lansbury Jr.P.T. Neurodegenerative disease: amyloid pores from pathogenic mutations Nature 418 2002 291 (Pubitemid 34790672)
20. Lin M.C., Mirzabekov T., and Kagan B.L. Channel formation by a neurotoxic prion protein fragment J. Biol. Chem. 272 1997 44 47 (Pubitemid 27021122)
21. Kagan B.L., Hirakura Y., Azimov R., Azimova R., and Lin M.C. The channel hypothesis of Alzheimer's disease: current status Peptides 23 2002 1311 1315 (Pubitemid 34786709)
22. Beal M.F. Energetics in the pathogenesis of neurodegenerative diseases Trends Neurosci. 23 2000 298 304 (Pubitemid 30387044)
23. Lin M.T., and Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases Nature 443 2006 787 795 (Pubitemid 44622683)
24. Petersen C.A.H., Alikhani N., Behbahani H., Wiehager B., Pavlov P.F., and Alafuzoff I. The amyloid β-peptide is imported into mitochondria via the TOM import machinery and localized to mitochondrial cristae Proc. Natl Acad. Sci. USA 105 2008 13145 13150
25. Devi L., Raghavendran V., Prabhu B.M., Avadhani N.G., and Anandatheerthavarada H.K. Mitochondrial import and accumulation of α-synuclein impair complex I in human dopaminergic neuronal cultures and Parkinson disease brain J. Biol. Chem. 283 2008 9089 9100
26. Kroemer G., Zamzami N., and Susin S.A. Mitochondrial control of apoptosis Immunol. Today 18 1997 44 51 (Pubitemid 27072433)
27. Green D.R., and Reed J.C. Mitochondria and apoptosis Science 281 1998 1309 1312 (Pubitemid 28406816)
28. Radford S.E., Dobson C.M., and Evans P.A. The folding of hen lysozyme involves partially structured intermediates and multiple pathways Nature 358 1992 302 307
29. Gorbenko G.P., Ioffe V.M., and Kinnunen P.K.J. Binding of lysozyme to phospholipid bilayers: evidence for protein aggregation upon membrane association Biophys. J. 93 2007 140 153 (Pubitemid 47041658)
30. Posse E., De Arcuri B.F., and Morero R.D. Lysozyme interactions with phospholipid vesicles: relationships with fusion and release of aqueous content Biochim. Biophys. Acta 1193 1994 101 106 (Pubitemid 24234184)
31. Kimelberg H.K. Protein-liposome interactions and their relevance to the structure and function of cell membranes Mol. Cell. Biochem. 10 1976 171 190
32. Krebs M.R.H., Wilkins D.K., Chung E.W., Pitkeathly M.C., Chamberlain A.K., and Zurdo J. Formation and seeding of amyloid fibrils from wild-type hen lysozyme and a peptide fragment from the β-domain J. Mol. Biol. 300 2000 541 549
33. Pepys M.B., Hawkins P.N., Booth D.R., Vigushin D.M., Tennent G.A., and Soutar A.K. Human lysozyme gene mutations cause hereditary systemic amyloidosis Nature 362 1993 553 557 (Pubitemid 23113032)
34. Lashuel H.A., and Lansbury Jr.P.T. Are amyloid diseases caused by protein aggregates that mimic bacterial pore-forming toxins? Q. Rev. Biophys. 39 2006 167 201 (Pubitemid 44711851)
35. Frare E., Mossuto M.F., de Laureto P.P., Tolin S., Menzer L., and Dumoulin M. Characterization of oligomeric species on the aggregation pathway of human lysozyme J. Mol. Biol. 387 2009 17 27
36. Simoneau S., Rezaei H., Sales N., Kaiser-Schulz G., Lefebvre-Roque M., and Vidal C. In vitro and in vivo neurotoxicity of prion protein oligomers PLoS Pathog. 3 2007 e125
37. Bolognesi B., Kumita J.R., Barros T.P., Esbjorner E.K., Luheshi L.M., and Crowther D.C. ANS binding reveals common features of cytotoxic amyloid species ACS Chem. Biol. 5 2010 735 740
38. Stefani M. Biochemical and biophysical features of both oligomer/fibril and cell membrane in amyloid cytotoxicity FEBS J. 277 2010 4602 4613
39. Kourie J.I., and Henry C.L. Ion channel formation and membrane-linked pathologies of misfolded hydrophobic proteins: the role of dangerous unchaperoned molecules Clin. Exp. Pharmacol. Physiol. 29 2002 741 753
40. Van Rooijen B.D., Claessens M., and Subramaniam V. Lipid bilayer disruption by oligomeric α-synuclein depends on bilayer charge and accessibility of the hydrophobic core Biochim. Biophys. Acta 1788 2009 1271 1278
41. Fujiwara S., Matsumoto F., and Yonezawa Y. Effects of salt concentration on association of the amyloid protofilaments of hen egg white lysozyme studied by time-resolved neutron scattering J. Mol. Biol. 331 2003 21 28 (Pubitemid 36870773)
42. Frare E., De Laureto P.P., Zurdo J., Dobson C.M., and Fontana A. A highly amyloidogenic region of hen lysozyme J. Mol. Biol. 340 2004 1153 1165 (Pubitemid 38968708)
43. Vernaglia B.A., Huang J., and Clark E.D. Guanidine hydrochloride can induce amyloid fibril formation from hen egg-white lysozyme Biomacromolecules 5 2004 1362 1370 (Pubitemid 39089737)
44. Lashuel H.A., Petre B.M., Wall J., Simon M., Nowak R.J., Walz T., and Lansbury Jr.P.T. α-Synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils J. Mol. Biol. 322 2002 1089 1102 (Pubitemid 35266514)
45. 2-microglobulin amyloid assembly revealed by ion mobility spectrometry-mass spectrometry Proc. Natl Acad. Sci. USA 107 2010 6794 6798
46. Huang R.H., and Faulkne R. The role of phospholipid in the multiple functional forms of brain monoamine oxidase J. Biol. Chem. 256 1981 9211 9215 (Pubitemid 12208313)
47. Picone P., Carrotta R., Montana G., Nobile M.R., Biagio P.L.S., and Di Carlo M. Aβ oligomers and fibrillar aggregates induce different apoptotic pathways in LAN5 neuroblastoma cell cultures Biophys. J. 96 2009 1 12
48. Vekrellis K., Xilouri M., Emmanouilidou E., and Stefanis L. Inducible over-expression of wild type α-synuclein in human neuronal cells leads to caspase-dependent non-apoptotic death J. Neurochem. 109 2009 1348 1362
49. Campioni S., Mannini B., Zampagni M., Pensalfini A., Parrini C., and Evangelisti E. A causative link between the structure of aberrant protein oligomers and their toxicity Nat. Chem. Biol. 6 2010 140 147
50. Khurana R., Ionescu-Zanetti C., Pope M., Li J., Nielson L., and Ramirez-Alvarado M. A general model for amyloid fibril assembly based on morphological studies using atomic force microscopy Biophys. J. 85 2003 1135 1144 (Pubitemid 36909675)
51. Kremer J.J., Pallitto M.M., Sklansky D.J., and Murphy R.M. Correlation of β-amyloid aggregate size and hydrophobicity with decreased bilayer fluidity of model membranes Biochemistry 39 2000 10309 10318 (Pubitemid 30663053)
52. Ohno-Shosaku T., and Okada Y. Electric pulse-induced fusion of mouse lymphoma cells: roles of divalent cations and membrane liquid domains J. Membr. Biol. 85 1985 269 280 (Pubitemid 15069819)
53. Ha B.Y. Stabilization and destabilization of cell membranes by multivalent ions Phys. Rev. E: Stat. Phys., Plasmas, Fluids, Relat. Interdiscip. Top. 64 2001 051902
54. Tomov T.C., Tsoneva I.C., and Doncheva J.C. Electrical stability of erythrocytes in the presence of divalent cations Biosci. Rep. 8 1988 421 426
55. 2+ Biosci. Rep. 4 1984 797 805 (Pubitemid 15220186)
56. Volles M.J., and Lansbury Jr.P.T. Vesicle permeabilization by protofibrillar α-synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism Biochemistry 41 2002 4595 4602 (Pubitemid 34275660)
57. Daum G. Lipids of mitochondria Biochim. Biophys. Acta 822 1985 1 42 (Pubitemid 15042024)
58. Schuber F. Influence of polyamines on membrane functions Biochem. J. 260 1989 1 10 (Pubitemid 19139892)
59. Quist A., Doudevski I., Lin H., Azimova R., Ng D., and Frangione B. Amyloid ion channels: a common structural link for protein-misfolding disease Proc Natl Acad. Sci. USA 102 2005 10427 10432 (Pubitemid 41061570)
60. Van Rooijen B.D., Claessens M., and Subramaniam V. Membrane permeabilization by oligomeric α-synuclein: in search of the mechanism PLoS ONE 5 2010 e14292
61. Kristian T., Gertsch J., Bates T.E., and Siesjo B.K. Characteristics of the calcium triggered mitochondrial permeability transition in nonsynaptic brain mitochondria: effect of cyclosporin A and ubiquinone O J. Neurochem. 74 2000 1999 2009 (Pubitemid 30217655)
62. Berman S.B., Watkins S.C., and Hastings T.G. Quantitative biochemical and ultrastructural comparison of mitochondrial permeability transition in isolated brain and liver mitochondria: evidence for reduced sensitivity of brain mitochondria Exp. Neurol. 164 2000 415 425 (Pubitemid 32008986)
63. Hristova K., Selsted M.E., and White S.H. Critical role of lipid composition in membrane permeabilization by rabbit neutrophil defensins J. Biol. Chem. 272 1997 24224 24233 (Pubitemid 27418623)
64. Chee P.Y., Dahl J.L., and Fahien L.A. The purification and properties of rat brain glutamate dehydrogenase J. Neurochem. 33 1979 53 60 (Pubitemid 9233911)
65. Goldberg M.E., Rudolph R., and Jaenicke R. A kinetic study of the competition between renaturation and aggregation during the refolding of denatured-reduced egg white lysozyme Biochemistry 30 1991 2790 2797
66. Tyson P.A., and Steinberg M. Accessibility of tryptophan residues in Na, K-ATPase J. Biol. Chem. 262 1987 4644 4648
67. Kabir F., and Wilson J.E. Mitochondrial hexokinase in brain of various species: differences in sensitivity to solubilization by glucose 6-phosphate Arch. Biochem. Biophys. 300 1993 641 650 (Pubitemid 23232923)
68. Golestani A., Ramshini H., and Nemat-Gorgani M. A study on the two binding sites of hexokinase on brain mitochondria BMC Biochem. 8 2007 20
69. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the folin phenol reagent J. Biol. Chem. 193 1951 265 275
70. D'Souza S.F., and Srere P.A. Binding of citrate synthase to mitochondrial inner membrane J. Biol. Chem. 258 1983 4706 4709
71. Pour-Rahimi F., and Nemat-Gorgani M. Reversible association of ox liver glutamate dehydrogenase with the inner mitochondrial membrane Int. J. Biochem. 19 1987 53 61 (Pubitemid 17012807)
72. Wu Y., Brovko L., and Griffiths M.W. Influence of phage population on the phage-mediated bioluminescent adenylate kinase (AK) assay for detection of bacteria Lett. Appl. Microbiol. 33 2001 311 315 (Pubitemid 32955633)
73. Hassett R.P., and Crockett E.L. Endpoint fluorometric assays for determining activities of carnitine palmitoyltransferase and citrate synthase Anal. Biochem. 287 2000 176 179
74. Lemeshko V.V., Solano S., Lopez L.F., Rendon D.A., Ghafourifar P., and Gomez L.A. Dextran causes aggregation of mitochondria and influences their oxidoreductase activities and light scattering Arch. Biochem. Biophys. 412 2003 176 185 (Pubitemid 36344141)