A yeast toxic mutant of HET-s amyloid disrupts membrane integrity

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 9, 2012, Pages 2325-2334

  Ta, Ha Phuong ^a   Berthelot, Karine ^b,c   Coulary Salin, Bénédicte ^b   Castano, Sabine ^a   Desbat, Bernard ^a   Bonnafous, Pierre ^a   Lambert, Olivier ^a   Alves, Isabel ^a   Cullin, Christophe ^b   Lecomte, Sophie ^a  

^a CNRS   (France)

^b Institut de Biochimie et Genetique Cellulaires   (France)

^c UNIVERSITÉ BORDEAUX 1   (France)

Author keywords

Amyloid toxicity; ATR FTIR; HET s; Leakage; Membrane; PWR

Indexed keywords

AMYLOID PROTEIN; LIPOSOME; NON TOXIC AMYLOID; TOXIC AMYLOID; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; BINDING AFFINITY; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE BINDING; MEMBRANE PERMEABILITY; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN LIPID INTERACTION; PROTEIN SECONDARY STRUCTURE; TRANSMISSION ELECTRON MICROSCOPY;

AMINO ACID SEQUENCE; AMINO ACIDS; AMYLOID; CELL MEMBRANE; CRYOELECTRON MICROSCOPY; FUNGAL PROTEINS; KINETICS; LECTINS; LIPID BILAYERS; LIPIDS; LIPOSOMES; MEMBRANE MICRODOMAINS; MICROSCOPY, ELECTRON, TRANSMISSION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROSCOPY, FOURIER TRANSFORM INFRARED;

EID: 84861865678     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.04.013     Document Type: Article

References (61)

1. F. Chiti, C.M. Dobson, Protein misfolding, functional amyloid, and human disease, Annu. Rev. Biochem. 75 (2006) 333-366. (Pubitemid 44118036)
2. M. Fändrich, M. Fletcher, C. Dobson, Amyloid fibrils from muscle myoglobin, Nature 410 (2001) 165-166.
3. N.K. Holm, S.K. Jespersen, L.V. Thomassen, T.Y. Wolff, P. Sehgal, L.A. Thomsen, G. Christiansen, C.B. Andersen, A.D. Knudsen, D.E. Otzen, Aggregation and fibrillation of bovine serum albumin, Biochim. Biophys. Acta 1774 (2007) 1128-1138. (Pubitemid 47333256)
4. F. Chiti, P. Webster, N. Taddei, A. Clark, M. Stefani, G. Ramponi, C.M. Dobson, Designing conditions for in vitro formation of amyloid protofilaments and fibrils, Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 3342-3344.
5. H. Zhao, E.K. Tuominen, P.K. Kinnunen, Formation of amyloid fibers triggered by phosphatidylserine-containing membranes, Biochemistry 43 (2004) 10302-10307. (Pubitemid 39079303)
6. T. Kowalewski, D. Holtzman, In situ atomic force microscopy study of Alzheimer's beta-amyloid peptide on different substrates: new insights into mechanism of beta-sheet formation, Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 3688-3693. (Pubitemid 29168971)
7. F. Shewmaker, R. McGlinchey, R. Wickner, Structural insights into functional and pathological amyloid, J. Biol. Chem. 286 (2011) 16533-16540.
8. R. Kayed, E. Head, J.L. Thompson, T.M. McIntire, S.C. Milton, C.W. Cotman, C. Glabe, Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis, Science 300 (2003) 486-489. (Pubitemid 36444329)
9. Y. Nagai, T. Inui, H.A. Popiel, N. Fujikake, K. Hasegawa, Y. Urade, Y. Goto, H. Naiki, T. Toda, A toxic monomeric conformer of the polyglutamine protein, Nat. Struct. Mol. Biol. 14 (2007) 332-340. (Pubitemid 46608340)
10. M. Bucciantini, E. Giannoni, F. Chiti, F. Baroni, L. Formigli, J. Zurdo, N. Taddei, G. Ramponi, C.M. Dobson, M. Stefani, Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases, Nature 416 (2002) 507-511. (Pubitemid 34288846)
11. J.P. Cleary, D.M. Walsh, J.J. Hofmeister, G.M. Shankar, M.A. Kuskowski, D.J. Selkoe, K.H. Ashe, Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function, Nat. Neurosci. 8 (2005) 79-84. (Pubitemid 41236735)
12. R. Kayed, A. Pensalfini, L. Margol, Y. Sokolov, F. Sarsoza, E. Head, J. Hall, C. Glabe, Annular protofibrils are a structurally and functionally distinct type of amyloid oligomer, J. Biol. Chem. 284 (2009) 4230-4237.
13. A.T. Petkova, R.D. Leapman, Z. Guo, W.M. Yau, M.P. Mattson, R. Tycko, Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils, Science 307 (2005) 262-265. (Pubitemid 40116242)
14. W.F. Xue, A.L. Hellewell, W.S. Gosal, S.W. Homans, E.W. Hewitt, S.E. Radford, Fibril fragmentation enhances amyloid cytotoxicity, J. Biol. Chem. 284 (2009) 34272-34282.
15. H.A. Lashuel, D. Hartley, B.M. Petre, T. Walz, P.T. Lansbury, Neurodegenerative disease: amyloid pores from pathogenic mutations, Nature 418 (2002) 291. (Pubitemid 34790672)
16. A. Quist, I. Doudevski, H. Lin, R. Azimova, D. Ng, B. Frangione, B. Kagan, J. Ghiso, R. Lal, Amyloid ion channels: a common structural link for protein-misfolding disease, Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 10427-10432. (Pubitemid 41061570)
17. A.L. Gharibyan, V. Zamotin, K. Yanamandra, O.S. Moskaleva, B.A. Margulis, I.A. Kostanyan, L.A. Morozova-Roche, Lysozyme amyloid oligomers and fibrils induce cellular death via different apoptotic/necrotic pathways, J. Mol. Biol. 365 (2007) 1337-1349. (Pubitemid 46048842)
18. M. Meyer-Luehmann, T. Spires-Jones, C. Prada, M. Garcia-Alloza, A. de Calignon, A. Rozkalne, J. Koenigsknecht-Talboo, D. Holtzman, B. Bacskai, B. Hyman, Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease, Nature 451 (2008) 638-639.
19. M.F. Mossuto, A. Dhulesia, G. Devlin, E. Frare, J.R. Kumita, P. Polverino de Laureto, M. Dumoulin, A. Fontana, C.M. Dobson, X. Salvatella, The non-core regions of human lysozyme amyloid fibrils influence cytotoxicity, J. Mol. Biol. 402 (2010) 783-796.
20. C. Aisenbrey, T. Borowik, R. Byström, M. Bokvist, F. Lindström, H. Misiak, M.-A. Sani, G. Gröbner, How is protein aggregation in amyloidogenic diseases modulated by biological membranes? Eur. Biophys. J. 37 (2008) 247-255.
21. T.L. Williams, L.C. Serpell, Membrane and surface interactions of the Alzheimer's Aβ peptide: insights into the mechanism of cytotoxicity, FEBS J. 278 (2011) 3905-3917.
22. C. Hertel, E. Terzi, N. Hauser, R. Jakob-Rotne, J. Seelig, J.A. Kemp, Inhibition of the electrostatic interaction between beta-amyloid peptide and membranes prevents beta-amyloid-induced toxicity, Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 9412-9416. (Pubitemid 27357843)
23. M.F. Engel, H. Yigittop, R.C. Elgersma, D.T. Rijkers, R.M. Liskamp, B. de Kruijff, J.W. Höppener, J.A. Killian, Islet amyloid polypeptide inserts into phospholipid mono-layers as monomer, J. Mol. Biol. 356 (2006) 783-789. (Pubitemid 43139337)
24. G.S. Baron, Conversion of raft associated prion protein to the protease-resistant requires insertion of PrP-res (PrPSc) into contiguous membranes, EMBO J. 21 (2002) 1031-1040. (Pubitemid 34206176)
25. R.P. Mason, R.F. Jacob, M.F. Walter, P.E. Mason, N.A. Avdulov, S.V. Chochina, U. Igbavboa, W.G. Wood, Distribution and fluidizing action of soluble and aggregated amyloid β-peptide in rat synaptic plasma membranes, J. Biol. Chem. 274 (1999) 18801-18807.
26. M.F. Engel, L. Khemtémourian, C.C. Kleijer, H.J. Meeldijk, J. Jacobs, A.J. Verkleij, B. de Kruijff, J.A. Killian, J.W.M. Höppener, Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane, Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 6033-6038. (Pubitemid 351758394)
27. R. Kayed, Y. Sokolov, B. Edmond, M.-T. McIntire, S.C. Milton, J.E. Hall, C.G. Glabe, 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)
28. E.E. Ambroggio, D.H. Kim, F. Separovic, C.J. Barrow, K.J. Barnham, L.A. Bagatolli, G.D. Fidelio, Surface behavior and lipid interaction of Alzheimer β-amyloid peptide1-42: a membrane-disrupting peptide, Biophys. J. 88 (2005) 2706-2713. (Pubitemid 40976137)
29. L.P. Choo-Smith, W. Garzon-Rodriguez, C.G. Glabe, W.K. Surewicz, Acceleration of amyloid fibril formation by specific binding of Abeta-(1-40) peptide to ganglioside-containing membrane vesicles, J. Biol. Chem. 272 (1997) 22987-22990. (Pubitemid 27392420)
30. M. Necula, C.N. Chirita, J. Kuret, Rapid anionic micelle-mediated α-synuclein fibrillization in vitro, J. Biol. Chem. 278 (2003) 46674-46680. (Pubitemid 37452245)
31. X. Yu, J. Zheng, Cholesterol promotes the interaction of Alzheimer 2 β-amyloid monomer with lipid bilayer, J. Mol. Biol. (2011), http://dx.doi.org/10.1016/ j.jmb.2011.1011.1006.
32. F. Malchiodi-Albedi, S. Paradisi, A. Matteucci, C. Frank, M. Diociaiuti, Amyloid oligomer neurotoxicity, calcium dysregulation, and lipid rafts, Int. J. Alzheimers Dis. (2011) 906964.
33. T. Okada, M. Wakabayashi, K. Ikeda, K. Matsuzaki, Formation of toxic fibrils of Alzheimer's amyloid beta-protein-(1-40) by monosialoganglioside GM1, a neuronal membrane component, J. Mol. Biol. (2007) 481-489. (Pubitemid 47048280)
34. E. Terzi, G. Holzemann, J. Seelig, Interaction of Alzheimer beta-amyloid peptide(1-40) with lipid membranes, Biochemistry 36 (1997) 14845-14852. (Pubitemid 27524407)
35. M. Zhu, A.L. Fink, Lipid binding inhibits α-synuclein fibril formation, J. Biol. Chem. 278 (2003) 16873-16877. (Pubitemid 36799558)
36. I.C. Martins, I. Kuperstein, H. Wilkinson, E. Maes, M. Vanbraban, W. Jonckheere, P. Van Gelder, D. Hartmann, R. D'Hooge, B. De Strooper, J. Schymkowitz, F. Rousseau, Lipids revert inert Aβ amyloid fibrils to neurotoxic protofibrils that affect learning in mice, EMBO J. 27 (2008) 224-233.
37. Y. Zhang, J.M. Shi, C.J. Cai-Juan Bai, H. Wang, H.Y. Li, Y. Wu, S.R. Ji, Intra-membrane oligomerization and extra-membrane oligomerization of amyloid-beta peptide are competing processes as a result of distinct patterns of motif interplay, J. Biol. Chem. 287 (2012) 748-756.
38. J. Couthouis, K. Rébora, F. Immel, K. Berthelot, M. Castroviejo, C. Cullin, Screening for toxic amyloid in yeast exemplifies the role of alternative pathway responsible for cytotoxicity, PLoS One 4 (2009) e4539.
39. K. Berthelot, H.P. Ta, J. Géan, S. Lecomte, C. Cullin, In vivo and In vitro analyses of toxic mutants of HET-s: FTIR antiparallel signature correlates with amyloid toxicity, J. Mol. Biol. 412 (2011) 137-152.
40. V. Coustou, C. Deleu, S. Saupe, J. Begueret, The protein product of the het-s hetero-karyon incompatibility gene of the fungus Podospora anserina behaves as a prion analog, Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 9773-9778. (Pubitemid 27408139)
41. C. Wasmer, A. Lange, H. Van Melckebeke, A.B. Siemer, B. Riek, H. Meier, Amyloid fibrils of the HET-s(218-289) prion form a β solenoid with a triangle hydrophobic core, Science 319 (2008) 1523-1526. (Pubitemid 351398180)
42. K. Berthelot, F. Immel, J. Géan, S. Lecomte, R. Oda, B. Kauffmann, C. Cullin, Driving amyloid toxicity in a yeast model by structural changes: a molecular approach, FASEB J. 23 (2009) 2254-2263.
43. K. Berthelot, S. Lecomte, J. Géan, F. Immel, C. Cullin, A yeast toxic mutant of HET-s (218-289) prion displays alternative intermediate of amyloidogenesis, Biophys. J. 99 (2010) 1239-1246.
44. J. Couthouis, C.Marchal, F.D'Angelo, K. Berthelot, C. Cullin, The toxicity of an "artificial"amyloid is related to how it interacts with membranes, Prion 4 (4) (2010) 283-291.
45. H.P. Ta, K. Berthelot, B. Coulary-Salin, B. Desbat, J. Géan, L. Servant, C. Cullin, S. Lecomte, Comparative studies of nontoxic and toxic amyloids interacting with membrane models at the air-water interface, Langmuir 27 (2011) 4797-4807.
46. G. Rouser, S. Fkeischer, A. Yamamoto, Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots, Lipids 5 (1970) 494-496.
47. Z. Salamon, H.A. Macleod, G. Tollin, Coupled plasmon-waveguide resonators: a new spectroscopic tool for probing proteolipid film structure and properties, Biophys. J. 73 (1997) 2791-2797. (Pubitemid 27471488)
48. I.D. Alves, S. Cowell, Z. Salamon, S. Devanathan, G. Tollin, V.J. Hruby, Different structural states of the proteolipid membrane are produced by ligand binding to the human delta-opioid receptor as shown by plasmon waveguide resonance spectroscopy, Mol. Pharmacol. 65 (2004) 1248-1257. (Pubitemid 38543495)
49. Z. Salamon, S. Devanathan, I.D. Alves, G. Tollin, Plasmon-waveguide resonance studies of lateral segregation of lipids and proteins into microdomains (rafts) in solid-supported bilayers, J. Biol. Chem. 280 (2005) 11175-11184. (Pubitemid 40418424)
50. I.D. Alves, Z. Salamon, V.J. Hruby, G. Tollin, Ligand modulation of lateral segregation of a G-protein-coupled receptor into lipid microdomains in sphingomyelin/ phosphatidylcholine solid-supported bilayers, Biochemistry 44 (2005) 9168-9178. (Pubitemid 40943231)
51. Y.N. Chirgadze, O.V. Fedorov, N.P. Trushina, Estimation of amino acid residue side-chain absorption in the infrared spectra of protein solutions in heavy water, Biopolymers 14 (1975) 679-694.
52. M.E. Van der Rest, A.H. Kamminga, A. Nakano, Y. Anraku, B. Poolman, W.N. Konings, The plasma membrane of Saccharomyces cerevisiae: structure, function, and biogenesis, Microbiol. Rev. 59 (1995) 304-322.
53. S. Jha, D. Sellin, R. Seidel, R. Winter, Amyloidogenic propensities and conformational properties of ProIAPP and IAPP in the presence of lipid bilayer membranes, J. Mol. Biol. 389 (2009) 907-920.
54. A. Relini, O. Cavalleri, R. Rolandia, A. Gliozzi, The two-fold aspect of the interplay of amyloidogenic proteins with lipid membranes, Chem. Phys. Lipids 158 (2009) 1-9.
55. M.J. Volles, S.J. Lee, J.C. Rochet, M.D. Shtilerman, T.T. Ding, J.C. Kessler, P.T. Lansbury, Vesicle permeabilization by protobrillar alpha-synuclein: implications for the pathogenesis and treatment of Parkinson's disease, Biochemistry 40 (2001) 7812-7819. (Pubitemid 32622972)
56. G. Valincius, F. Heinrich, R. Budvytyte, D.J. Vanderah, D.J. McGillivray, Y. Sokolov, J.E. Hall, M. Losche, Soluble amyloid beta-oligomers affect dielectric membrane properties by bilayer insertion and domain formation: implications for cell toxicity, Biophys. J. 95 (2008) 4845-4861.
57. F. Haque, A.P. Pandey, L.R. Cambrea, J.C. Rochet, J.S. Hovis, Adsorption of alpha-synuclein on lipid bilayers: modulating the structure and stability of protein assemblies, J. Phys. Chem. B 114 (2010) 4070-4081.
58. J.D. Knight, A.D. Miranker, Phospholipid catalysis of diabetic amyloid assembly, J. Mol. Biol. 341 (2004) 1175-1187. (Pubitemid 39099208)
59. E. Cerf, R. Sarroukh, S. Tamamizu-Kato, L. Breydo, S. Derclaye, Y.F. Dufrêne, V. Narayanaswami, E. Goormaghtigh, J.-M. Ruysschaert, V. Raussens, Antiparallel beta-sheet: a signature of the oligomeric amyloid beta-peptide, Biochem. J. 421 (2009) 415-423.
60. R. Sarroukh, E. Cerf, S. Derclaye, Y.F. Dufrene, E. Goormaghtigh, J.M. Ruysschaert, V. Raussens, Transformation of amyloid beta(1-40) oligomers into fibrils is characterized by a major change in secondary structure, Cell. Mol. Life Sci. 68 (2011) 1429-1438.
61. M.S. Celej, R. Sarroukh, E. Goormaghtigh, G. Fidelio, J.M. Ruysschaert, V. Raussens, Toxic prefibrillar α-synuclein amyloid oligomers adopt a distinctive antiparallel β-sheet structure, Biochem. J. 443 (2012) 719-726.