In vivo and in vitro analyses of toxic mutants of HET-s: FTIR antiparallel signature correlates with amyloid toxicity

Journal of Molecular Biology

Volumn 412, Issue 1, 2011, Pages 137-152

  Berthelot, Karine ^a   Ta, Ha Phuong ^b,c   Géan, Julie ^b   Lecomte, Sophie ^b   Cullin, Christophe ^a  

^a Institut de Biochimie et Genetique Cellulaires   (France)

^b CNRS   (France)

^c INSTITUT DES SCIENCES MOLÉCULAIRES   (France)

Author keywords

aggregation; folding; FTIR; HET s; toxicity

Indexed keywords

AMYLOID PROTEIN;

ARTICLE; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; INFRARED SPECTROSCOPY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE;

PODOSPORA ANSERINA;

EID: 84860390157     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.07.009     Document Type: Article

References (60)

1. Chiti F., and Dobson C.M. Protein misfolding, functional amyloid, and human disease Annu. Rev. Biochem. 75 2006 333 366 (Pubitemid 44118036)
2. Hammer N.D., Schmidt J.C., and Chapman M.R. The curli nucleator protein, CsgB, contains an amyloidogenic domain that directs CsgA polymerization Proc. Natl Acad. Sci. USA 104 2007 12494 12499 (Pubitemid 47206166)
3. Romero D., Aguilar C., Losick R., and Kolter R. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms Proc. Natl Acad. Sci. USA 107 2010 2230 2234
4. Kenney J.M., Knight D., Wise M.J., and Vollrath F. Amyloidogenic nature of spider silk Eur. J. Biochem. 269 2002 4159 4163 (Pubitemid 34994911)
5. Kwan A.H., Winefield R.D., Sunde M., Matthews J.M., Haverkamp R.G., Templeton M.D., and Mackay J.P. Structural basis for rodlet assembly in fungal hydrophobins Proc. Natl Acad. Sci. USA 103 2006 3621 3626 (Pubitemid 43376605)
6. Ramsook C.B., Tan C., Garcia M.C., Fung R., Soybelman G., and Henry R. Yeast cell adhesion molecules have functional amyloid-forming sequences Eukaryot. Cell 9 2010 393 404
7. Iconomidou V.A., Vriend G., and Hamodrakas S.J. Amyloids protect the silkmoth oocyte and embryo FEBS Lett. 479 2000 141 145 (Pubitemid 30616422)
8. Podrabsky J.E., Carpenter J.F., and Hand S.C. Survival of water stress in annual fish embryos: dehydration avoidance and egg envelope amyloid fibers Am. J. Physiol.: Regul., Integr. Comp. Physiol. 280 2001 R123 R131
9. McGlinchey R.P., Shewmaker F., McPhie P., Monterroso B., Thurber K., and Wickner R.B. The repeat domain of the melanosome fibril protein Pmel17 forms the amyloid core promoting melanin synthesis Proc. Natl Acad. Sci. USA 106 2009 13731 13736
10. Kranenburg O., Bouma B., Kroon-Batenburg L.M., Reijerkerk A., Wu Y.P., Voest E.E., and Gebbink M.F. Tissue-type plasminogen activator is a multiligand cross-beta structure receptor Curr. Biol. 12 2002 1833 1839 (Pubitemid 35273903)
11. Gebbink M.F., Voest E.E., and Reijerkerk A. Do antiangiogenic protein fragments have amyloid properties? Blood 104 2004 1601 1605 (Pubitemid 39202263)
12. Münch J., Rücker E., Ständker L., Adermann K., Goffinet C., and Schindler M. Semen-derived amyloid fibrils drastically enhance HIV infection Cell 131 2007 1059 1071 (Pubitemid 350235017)
13. Soscia S.J., Kirby J.E., Washicosky K.J., Tucker S.M., Ingelsson M., and Hyman B. The Alzheimer's disease-associated amyloid beta-protein is an antimicrobial peptide PLoS One 5 2010 e9505
14. Maji S.K., Perrin M.H., Sawaya M.R., Jessberger S., Vadodaria K., and Rissman R.A. Functional amyloids as natural storage of peptide hormones in pituitary secretory granules Science 325 2009 328 332
15. Fändrich M., Fletcher M.A., and Dobson C.M. Amyloid fibrils from muscle myoglobin Nature 410 2001 165 166
16. Holm N.K., Jespersen S.K., Thomassen L.V., Wolff T.Y., Sehgal P., and Thomsen L.A. Aggregation and fibrillation of bovine serum albumin Biochim. Biophys. Acta 1774 2007 1128 1138 (Pubitemid 47333256)
17. 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)
18. Zhao H., Tuominen E.K., and Kinnunen P.K. Formation of amyloid fibers triggered by phosphatidylserine-containing membranes Biochemistry 43 2004 10302 10307 (Pubitemid 39079303)
19. 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)
20. Maji S.K., Wang L., Greenwald J., and Riek R. Structure-activity relationship of amyloid fibrils FEBS Lett. 583 2009 2610 2617
21. Nelson R., Sawaya M.R., Balbirnie M., Madsen A.∅., Riekel C., Grothe R., and Eisenberg D. Structure of the cross-beta spine of amyloid-like fibrils Nature 435 2005 773 778 (Pubitemid 40839722)
22. Sawaya M.R., Sambashivan S., Nelson R., Ivanova M.I., Sievers S.A., and Apostol M.I. Atomic structures of amyloid cross-beta spines reveal varied steric zippers Nature 447 2007 453 457 (Pubitemid 46816731)
23. Cerf E., Sarroukh R., Tamamizu-Kato S., Breydo L., Derclaye S., and Dufrêne Y.F. Antiparallel beta-sheet: a signature structure of the oligomeric amyloid beta-peptide Biochem. J. 421 2009 415 423
24. Antzutkin O.N., Balbach J.J., Leapman R.D., Rizzo N.W., Reed J., and Tycko R. Multiple quantum solid-state NMR indicates a parallel, not antiparallel, organization of beta-sheets in Alzheimer's beta-amyloid fibrils Proc. Natl Acad. Sci. USA 97 2000 13045 13050
25. 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)
26. Cleary J.P., Walsh D.M., Hofmeister J.J., Shankar G.M., Kuskowski M.A., Selkoe D.J., and Ashe K.H. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function Nat. Neurosci. 8 2005 79 84 (Pubitemid 41236735)
27. Kayed R., Pensalfini A., Margol L., Sokolov Y., Sarsoza F., and Head E. Annular protofibrils are a structurally and functionally distinct type of amyloid oligomer J. Biol. Chem. 284 2009 4230 4237
28. Petkova A.T., Leapman R.D., Guo Z., Yau W.M., Mattson M.P., and Tycko R. Self-propagating, molecular-level polymorphism in Alzheimer's beta-amyloid fibrils Science 307 2005 262 265 (Pubitemid 40116242)
29. Xue W.F., Hellewell A.L., Gosal W.S., Homans S.W., Hewitt E.W., and Radford S.E. Fibril fragmentation enhances amyloid cytotoxicity J. Biol. Chem. 284 2009 34272 34282
30. Lashuel H.A., Hartley D., Petre B.M., Walz T., and Lansbury P.T. Neurodegenerative disease: amyloid pores from pathogenic mutations Nature 418 2002 291 (Pubitemid 34790672)
31. 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)
32. Gharibyan A.L., Zamotin V., Yanamandra K., Moskaleva O.S., Margulis B.A., Kostanyan I.A., and Morozova-Roche L.A. Lysozyme amyloid oligomers and fibrils induce cellular death via different apoptotic/necrotic pathways J. Mol. Biol. 365 2007 1337 1349 (Pubitemid 46048842)
33. Meyer-Luehmann M., Spires-Jones T.L., Prada C., Garcia-Alloza M., de Calignon A., and Rozkalne A. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease Nature 451 2008 720 724 (Pubitemid 351220570)
34. Mossuto M.F., Dhulesia A., Devlin G., Frare E., Kumita J.R., and de Laureto P.P. The non-core regions of human lysozyme amyloid fibrils give rise to cytotoxicity J. Mol. Biol. 402 2010 783 796
35. Engel M.F., Khemtémourian L., Kleijer C.C., Meeldijk H.J., Jacobs J., and Verkleij A.J. Membrane damage by human islet amyloid polypeptide through fibril growth at the membrane Proc. Natl Acad. Sci. USA 105 2008 6033 6038 (Pubitemid 351758394)
36. 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)
37. Martins I.C., Kuperstein I., Wilkinson H., Maes E., Vanbrabant M., and Jonckheere W. Lipids revert inert Abeta amyloid fibrils to neurotoxic protofibrils that affect learning in mice EMBO J. 27 2008 224 233
38. Couthouis J., Rébora K., Immel F., Berthelot K., Castroviejo M., and Cullin C. Screening for toxic amyloid in yeast exemplifies the role of alternative pathway responsible for cytotoxicity PLoS One 4 2009 e4539
39. Coustou V., Deleu C., Saupe S., and Begueret J. The protein product of the het-s heterokaryon incompatibility gene of the fungus Podospora anserina behaves as a prion analog Proc. Natl Acad. Sci. USA 94 1997 9773 9778 (Pubitemid 27408139)
40. Wasmer C., Lange A., Van Melckebeke H., Siemer A.B., Riek R., and Meier B.H. Amyloid fibrils of the HET-s(218-289) prion form a beta solenoid with a triangular hydrophobic core Science 319 2008 1523 1526 (Pubitemid 351398180)
41. Berthelot K., Immel F., Géan J., Lecomte S., Oda R., Kauffmann B., and Cullin C. Driving amyloid toxicity in a yeast model by structural changes: a molecular approach FASEB J. 23 2009 2254 2263
42. Berthelot K., Lecomte S., Géan J., Immel F., and Cullin C. A yeast toxic mutant of HET-s(218-289) prion displays alternative intermediates of amyloidogenesis Biophys. J. 99 2010 1239 1246
43. Goormaghtigh E., Cabiaux V., and Ruysschaert J.M. Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. I. Assignments and model compounds Subcell. Biochem. 23 1994 329 362
44. Chirgadze Y.N., and Nevskaya N.A. Infrared spectra and resonance interaction of amide-I vibration of the antiparallel-chain pleated sheet Biopolymers 15 1976 607 625
45. Chirgadze Y.N., and Nevskaya N.A. Infrared spectra and resonance interaction of amide-I vibration of the parallel-chain pleated sheet Biopolymers 15 1976 627 636
46. Howie A.J., and Brewer D.B. Optical properties of amyloid stained by Congo red: history and mechanisms Micron 40 2009 285 301
47. Couthouis J., Marchal C., D'Angelo F., Berthelot K., and Cullin C. The toxicity of an "artificial" amyloid is related to how it interacts with membranes Prion 4 2010 283 291
48. van der Rest M.E., Kamminga A.H., Nakano A., Anraku Y., Poolman B., and Konings W.N. The plasma membrane of Saccharomyces cerevisiae: structure, function, and biogenesis Microbiol. Rev. 59 1995 304 322
49. Perutz M.F., Pope B.J., Owen D., Wanker E.E., and Scherzinger E. Aggregation of proteins with expanded glutamine and alanine repeats of the glutamine-rich and asparagine-rich domains of Sup35 and of the amyloid beta-peptide of amyloid plaques Proc. Natl Acad. Sci. USA 99 2002 5596 5600 (Pubitemid 34411594)
50. Perutz M.F., Johnson T., Suzuki M., and Finch J.T. Glutamine repeats as polar zippers: their possible role in inherited neurodegenerative diseases Proc. Natl Acad. Sci. USA 91 1994 5355 5358 (Pubitemid 24174325)
51. Wiltzius J.J., Sievers S.A., Sawaya M.R., Cascio D., Popov D., Riekel C., and Eisenberg D. Atomic structure of the cross-beta spine of islet amyloid polypeptide (amylin) Protein Sci. 17 2008 1467 1474
52. Fernandez-Flores A. A review of amyloid staining: methods and artifacts Biotech. Histochem. 2010 10.3109/10520291003784493
53. Lorenzo A., and Yankner B.A. Beta-amyloid neurotoxicity requires fibril formation and is inhibited by Congo red Proc. Natl Acad. Sci. USA 91 1994 12243 12247 (Pubitemid 24368641)
54. Lendel C., Bolognesi B., Wahlström A., Dobson C.M., and Gräslund A. Detergent-like interaction of Congo red with the amyloid beta peptide Biochemistry 49 2010 1358 1360
55. Bose P.P., Chatterjee U., Xie L., Johansson J., Göthelid E., and Arvidsson P.I. Effects of Congo red on Abeta1-40 fibril formation process and morphology ACS Chem. Neurosci. 1 2010 315 324
56. Habicht G., Haupt C., Friedrich R.P., Hortschansky P., Sachse C., and Meinhardt J. Directed selection of a conformational antibody domain that prevents mature amyloid fibril formation by stabilizing Abeta protofibrils Proc. Natl Acad. Sci. USA 104 2007 19232 19237
57. Sarroukh R., Cerf E., Derclaye S., Dufrêne Y.F., Goormaghtigh E., Ruysschaert J.M., and Raussens V. Transformation of amyloid β(1-40) oligomers into fibrils is characterized by a major change in secondary structure Cell. Mol. Life Sci. 68 2011 1429 1438
58. Chou K.C., Pottle M., Némethy G., Ueda Y., and Scheraga H.A. Structure of beta-sheets. Origin of the right-handed twist and of the increased stability of antiparallel over parallel sheets J. Mol. Biol. 162 1982 89 112
59. Gietz R.D., Schiestl R.H., Willems A.R., and Woods R.A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure Yeast 11 1995 355 360
60. Cullin C., and Minvielle-Sebastia L. Multipurpose vectors designed for the fast generation of N- or C-terminal epitope-tagged proteins Yeast 10 1994 105 112 (Pubitemid 24052953)