Deciphering the structure, growth and assembly of amyloid-like fibrils using high-speed atomic force microscopy

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Milhiet, Pierre Emmanuel ^a,b   Yamamoto, Daisuke ^c   Berthoumieu, Olivia ^a,b   Dosset, Patrice ^a,b   le Grimellec, Christian ^a,b   Verdier, Jean Michel ^b,d,e   Marchal, Stéphane ^b,d,e   Ando, Toshio ^c  

^a INSERM   (France)

^b UNIV MONTPELLIER   (France)

^c KANAZAWA UNIVERSITY   (Japan)

^d University of Montpellier   (France)

^e PSL RESEARCH UNIVERSITY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; LITHOSTATHINE; MICA; TRYPSIN; AMYLOID;

ARTICLE; ATOMIC FORCE MICROSCOPY; GROWTH RATE; MOLECULAR DYNAMICS; MOLECULAR IMAGING; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN LATERAL ASSOCIATION; PROTEIN PURIFICATION; PROTEIN STACKING; PROTEIN STRUCTURE; RNA TRANSLATION; STRUCTURE ANALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; METHODOLOGY;

AMYLOID; LITHOSTATHINE; MICROSCOPY, ATOMIC FORCE; MOLECULAR STRUCTURE;

EID: 78149452358     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013240     Document Type: Article

References (50)

1. Kopito RR, Ron D (2000) Conformational disease. Nat Cell Biol 2: E207-209.
2. Walker LC, LeVine H (2000) The cerebral proteopathies. Neurobiol Aging 21: 559-561.
3. Nelson R, Eisenberg D (2006) Recent atomic models of amyloid fibril structure. Curr Opin Struct Biol 16: 260-265.
4. Sawaya MR, Sambashivan S, Nelson R, Ivanova MI, Sievers SA, et al. (2007) Atomic structures of amyloid cross-beta spines reveal varied steric zippers. Nature 447: 453-457.
5. Jimenez JL, Nettleton EJ, Bouchard M, Robinson CV, Dobson CM, et al. (2002) The protofilament structure of insulin amyloid fibrils. Proc Natl Acad Sci U S A 99: 9196-9201.
6. Jimenez JL, Guijarro JI, Orlova E, Zurdo J, Dobson CM, et al. (1999) Cryoelectron microscopy structure of an SH3 amyloid fibril and model of the molecular packing. EMBO J 18: 815-821.
7. Fandrich M, Fletcher MA, Dobson CM (2001) Amyloid fibrils from muscle myoglobin. Nature 410: 165-166.
8. Govaerts C, Wille H, Prusiner SB, Cohen FE (2004) Evidence for assembly of prions with left-handed beta-helices into trimers. Proc Natl Acad Sci U S A 101: 8342-8347.
9. Paulson HL (2000) Toward an understanding of polyglutamine neurodegeneration. Brain Pathol 10: 293-299.
10. Scherzinger E, Lurz R, Turmaine M, Mangiarini L, Hollenbach B, et al. (1997) Huntingtin-encoded polyglutamine expansions form amyloid-like protein aggregates in vitro and in vivo. Cell 90: 549-558.
11. Perutz MF, Finch JT, Berriman J, Lesk A (2002) Amyloid fibers are water-filled nanotubes. Proc Natl Acad Sci U S A 99: 5591-5595.
12. Perutz MF, Pope BJ, Owen D, Wanker EE, Scherzinger E (2002) 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 U S A 99: 5596-5600.
13. Blake C, Serpell L (1996) Synchrotron X-ray studies suggest that the core of the transthyretin amyloid fibril is a continuous beta-sheet helix. Structure 4: 989-998.
14. Janowski R, Kozak M, Jankowska E, Grzonka Z, Grubb A, et al. (2001) Human cystatin C, an amyloidogenic protein, dimerizes through three-dimensional domain swapping. Nat Struct Biol 8: 316-320.
15. Knaus KJ, Morillas M, Swietnicki W, Malone M, Surewicz WK, et al. (2001) Crystal structure of the human prion protein reveals a mechanism for oligomerization. Nat Struct Biol 8: 770-774.
16. Bernard JP, Adrich Z, Montalto G, De Caro A, De Reggi M, et al. (1992) Inhibition of nucleation and crystal growth of calcium carbonate by human lithostathine. Gastroenterology 103: 1277-1284.
17. Geider S, Dussol B, Nitsche S, Veesler S, Berthezene P, et al. (1996) Calcium carbonate crystals promote calcium oxalate crystallization by heterogeneous or epitaxial nucleation: possible involvement in the control of urinary lithogenesis. Calcif Tissue Int 59: 33-37.
18. Gerbaud V, Pignol D, Loret E, Bertrand JA, Berland Y, et al. (2000) Mechanism of calcite crystal growth inhibition by the N-terminal undecapeptide of lithostathine. J Biol Chem 275: 1057-1064.
19. Lee BI, Mustafi D, Cho W, Nakagawa Y (2003) Characterization of calcium binding properties of lithostathine. J Biol Inorg Chem 8: 341-347.
20. De Caro A, Lohse J, Sarles H (1979) Characterization of a protein isolated from pancreatic calculi of men suffering from chronic calcifying pancreatitis. Biochem Biophys Res Commun 87: 1176-1182.
21. Perfetti R, Egan JM, Zenilman ME, Shuldiner AR (1994) Expression of the regenerating gene in the pancreas of aging mice. Transplant Proc 26: 733.
22. Sekikawa A, Fukui H, Fujii S, Nanakin A, Kanda N, et al. (2005) Possible role of REG I alpha protein in ulcerative colitis and colitic cancer. Gut 54: 1437-1444.
23. Mauro V, Carette D, Chevallier D, Michiels JF, Segretain D, et al. (2008) Reg I protein in healthy and seminoma human testis. Histol Histopathol 23: 1195-1203.
24. Cerini C, Peyrot V, Garnier C, Duplan L, Veesler S, et al. (1999) Biophysical characterization of lithostathine. Evidences for a polymeric structure at physiological pH and a proteolysis mechanism leading to the formation of fibrils. J Biol Chem 274: 22266-22274.
25. Laurine E, Gregoire C, Fandrich M, Engemann S, Marchal S, et al. (2003) Lithostathine quadruple-helical filaments form proteinase K-resistant deposits in Creutzfeldt-Jakob disease. J Biol Chem 278: 51770-51778.
26. Gregoire C, Marco S, Thimonier J, Duplan L, Laurine E, et al. (2001) Threedimensional structure of the lithostathine protofibril, a protein involved in Alzheimer's disease. EMBO J 20: 3313-3321.
27. Pignol D, Bertrand JA, Bernard JP, Verdier JM, Dagorn JC, et al. (1995) Crystallization and preliminary crystallographic study of human lithostathine. Proteins 23: 604-606.
28. Bertrand JA, Pignol D, Bernard JP, Verdier JM, Dagorn JC, et al. (1996) Crystal structure of human lithostathine, the pancreatic inhibitor of stone formation. EMBO J 15: 2678-2684.
29. Ando T, Uchihashi T, Kodera N, Yamamoto D, Miyagi A, et al. (2008) Highspeed AFM and nano-visualization of biomolecular processes. Pflugers Arch 456: 211-225.
30. Harper JD, Lieber CM, Lansbury PT, Jr. (1997) Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer's disease amyloid-beta protein. Chem Biol 4: 951-959.
31. Bauer HH, Aebi U, Haner M, Hermann R, Muller M, et al. (1995) Architecture and polymorphism of fibrillar supramolecular assemblies produced by in vitro aggregation of human calcitonin. J Struct Biol 115: 1-15.
32. Mesquida P, Riener C, Macphee C, Mckendry R (2007) Morphology and mechanical stability of amyloid-like peptide fibrils. J Mater Sci: Mater Med 18: 1325-1331.
33. Sunde M, Blake CC (1998) From the globular to the fibrous state: protein structure and structural conversion in amyloid formation. Q Rev Biophys 31: 1-39.
34. Green JD, Goldsbury C, Kistler J, Cooper GJ, Aebi U (2004) Human amylin oligomer growth and fibril elongation define two distinct phases in amyloid formation. J Biol Chem 279: 12206-12212.
35. Goldsbury C, Frey P, Olivieri V, Aebi U, Müller SA (2005) Multiple assembly pathways underlie amyloid-beta fibril polymorphisms. J Mol Biol 352: 282-298.
36. Kellermayer MS, Karsai A, Benke M, Soos K, Penke B (2008) Stepwise dynamics of epitaxially growing single amyloid fibrils. Proc Natl Acad Sci U S A 105: 141-144.
37. Fay N (2005) Structure of the Prion Ure2p in Protein Fibrils Assembled in Vitro. J Biol Chem 280: 37149-37158.
38. Yagi H, Ban T, Morigaki K, Naiki H, Goto Y (2007) Visualization and classification of amyloid beta supramolecular assemblies. Biochemistry 46: 15009-15017.
39. Ranson N, Stromer T, Bousset L, Melki R, Serpell L (2006) Insights into the architecture of the Ure2p yeast protein assemblies from helical twisted fibrils. Protein Science 15: 2481-2487.
40. Lashuel HA, Petre BM, Wall J, Simon M, Nowak RJ, et al. (2002) Alphasynuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J Mol Biol 322: 1089-1102.
41. Meinhardt J, Sachse C, Hortschansky P, Grigorieff N, Fandrich M (2009) Abeta(1-40) fibril polymorphism implies diverse interaction patterns in amyloid fibrils. J Mol Biol 386: 869-877.
42. Kidd M (1963) Paired helical filaments in electron microscopy of Alzheimer's disease. Nature 197: 192-193.
43. Moreno-Herrero F, Perez M, Baro AM, Avila J (2004) Characterization by atomic force microscopy of Alzheimer paired helical filaments under physiological conditions. Biophys J 86: 517-525.
44. Roher AE, Chaney MO, Kuo YM, Webster SD, Stine WB, et al. (1996) Morphology and toxicity of Abeta-(1-42) dimer derived from neuritic and vascular amyloid deposits of Alzheimer's disease. J Biol Chem 271: 20631-20635.
45. Andersen CB, Yagi H, Manno M, Martorana V, Ban T, et al. (2009) Branching in amyloid fibril growth. Biophys J 96: 1529-1536.
46. Hoyer W, Cherny D, Subramaniam V, Jovin TM (2004) Rapid self-assembly of alpha-synuclein observed by in situ atomic force microscopy. J Mol Biol 340: 127-139.
47. Karsai A, Murvai U, Soos K, Penke B, Kellermayer MS (2008) Oriented epitaxial growth of amyloid fibrils of the N27C mutant beta 25-35 peptide. Eur Biophys J 37: 1133-1137.
48. Soto C, Estrada L, Castilla J (2006) Amyloids, prions and the inherent infectious nature of misfolded protein aggregates. Trends Biochem Sci 31: 150-155.
49. Fay N (2003) Assembly of the Yeast Prion Ure2p into Protein Fibrils: Thermodynamic and kinetic characterization. J Biol Chem 278: 30199-30205.
50. Ando T, Uchihashi T, Kodera N, Yamamoto D, Taniguchi M, et al. (2007) High-speed atomic force microscopy for observing dynamic biomolecular processes. J Mol Recognit 20: 448-458.