Structure and assembly-disassembly properties of wild-type transthyretin amyloid protofibrils observed with atomic force microscopy

Journal of Molecular Recognition

Volumn 24, Issue 3, 2011, Pages 467-476

  Pires, Ricardo H ^a   Saraiva, Maria J ^b,c   Damas, Ana M ^b,c   Kellermayer, Miklõs S Z ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIVERSITY OF PORTO   (Portugal)

Author keywords

amyloid; atomic force microscopy; cytotoxic oligomers; fibrillogenesis; periodicity; protofibril; transthyretin

Indexed keywords

AMYLOID; PREALBUMIN;

ARTICLE; ATOMIC FORCE MICROSCOPY; CHEMISTRY; METHODOLOGY;

AMYLOID; MICROSCOPY, ATOMIC FORCE; PREALBUMIN;

EID: 79955124353     PISSN: 09523499     EISSN: 10991352     Source Type: Journal    
DOI: 10.1002/jmr.1112     Document Type: Article

References (50)

1. Almeida MR, Damas AM, Lans MC, Brouwer A, Saraiva MJ., 1997. Thyroxine binding to transthyretin Met 119. Comparative studies of different heterozygotic carriers and structural analysis. Endocrine 6: 309-315. (Pubitemid 27431403)
2. Arimon M, Diez-Perez I, Kogan MJ, Durany N, Giralt E, Sanz F, Fernandez-Busquets X., 2005. Fine structure study of Abeta 1-42 fibrillogenesis with atomic force microscopy. Faseb J. 19: 1344-1346. (Pubitemid 41113744)
3. Benditt EP, Eriksen N, Berglund C., 1970. Congo red dichroism with dispersed amyloid fibrils, an extrinsic cotton effect. Proc. Natl Acad. Sci. USA 66: 1044-1051.
4. Bergstrom J, Gustavsson A, Hellman U, Sletten K, Murphy CL, Weiss DT, Solomon A, Olofsson BO, Westermark P., 2005. Amyloid deposits in transthyretin-derived amyloidosis: cleaved transthyretin is associated with distinct amyloid morphology. J. Pathol. 206: 224-232. (Pubitemid 40754027)
5. 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. (Pubitemid 26324709)
6. Blake CC, Geisow MJ, Oatley SJ, Rerat B, Rerat C., 1978. Structure of prealbumin: secondary, tertiary and quaternary interactions determined by Fourier refinement at 1.8 A. J. Mol. Biol. 121: 339-356. (Pubitemid 8361803)
7. Blake CC, Serpell LC, Sunde M, Sandgren O, Lundgren E., 1996. A molecular model of the amyloid fibril. Ciba Found Symp. 199 (6-15): discussion 15-21, 16-40.
8. Bonifacio MJ, Sakaki Y, Saraiva MJ., 1996. 'In vitro' amyloid fibril formation from transthyretin: the influence of ions and the amyloidogenicity of TTR variants. Biochim. Biophys. Acta 1316: 35-42. (Pubitemid 26173904)
9. Cardoso I, Goldsbury CS, Muller SA, Olivieri V, Wirtz S, Damas AM, Aebi U, Saraiva MJ., 2002. Transthyretin fibrillogenesis entails the assembly of monomers: a molecular model for in vitro assembled transthyretin amyloid-like fibrils. J. Mol. Biol. 317: 683-695. (Pubitemid 34722157)
10. Carnally SM, Dev HS, Stewart AP, Barrera NP, Van Bemmelen MX, Schild L, Henderson RM, Edwardson JM., 2008. Direct visualization of the trimeric structure of the ASIC1a channel, using AFM imaging. Biochem. Biophys. Res. Commun. 372: 752-755.
11. Carrotta R, Manno M, Bulone D, Martorana V, San Biagio PL., 2005. Protofibril formation of amyloid beta-protein at low pH via a non-cooperative elongation mechanism. J. Biol. Chem. 280: 30001-30008. (Pubitemid 41216175)
12. Caughey B, Lansbury PT., 2003. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26: 267-298. (Pubitemid 37064935)
13. Chiti F, Dobson CM., 2006. Protein misfolding, functional amyloid, and human disease. Annu. Rev. Biochem. 75: 333-366. (Pubitemid 44118036)
14. Colon W, Kelly JW., 1992. Partial denaturation of transthyretin is sufficient for amyloid fibril formation in vitro. Biochemistry 31: 8654-8660.
15. Connors LH, Ericsson T, Skare J, Jones LA, Lewis WD, Skinner M., 1998. A simple screening test for variant transthyretins associated with familial transthyretin amyloidosis using isoelectric focusing. Biochim. Biophys. Acta 1407: 185-192. (Pubitemid 29067435)
16. Correia BE, Loureiro-Ferreira N, Rodrigues JR, Brito RM., 2006. A structural model of an amyloid protofilament of transthyretin. Protein Sci. 15: 28-32. (Pubitemid 43004230)
17. Fleming CE, Nunes AF, Sousa MM., 2009. Transthyretin: more than meets the eye. Prog. Neurobiol. 89: 266-276.
18. Foss TR, Wiseman RL, Kelly JW., 2005. The pathway by which the tetrameric protein transthyretin dissociates. Biochemistry 44: 15525-15533. (Pubitemid 41706136)
19. Gosal WS, Morten IJ, Hewitt EW, Smith DA, Thomson NH, Radford SE., 2005. Competing pathways determine fibril morphology in the self-assembly of beta2-microglobulin into amyloid. J. Mol. Biol. 351: 850-864. (Pubitemid 41111901)
20. Gregoire C, Marco S, Thimonier J, Duplan L, Laurine E, Chauvin JP, Michel B, Peyrot V, Verdier JM., 2001. Three-dimensional structure of the lithostathine protofibril, a protein involved in Alzheimer's disease. Embo J. 20: 3313-3321. (Pubitemid 32634339)
21. Habicht G, Haupt C, Friedrich RP, Hortschansky P, Sachse C, Meinhardt J, Wieligmann K, Gellermann GP, Brodhun M, Gotz J, Halbhuber KJ, Rocken C, Horn U, Fandrich M., 2007. Directed selection of a conformational antibody domain that prevents mature amyloid fibril formation by stabilizing Abeta protofibrils. Proc. Natl Acad. Sci. USA 104: 19232-19237.
22. Hill SE, Robinson J, Matthews G, Muschol M., 2009. Amyloid protofibrils of lysozyme nucleate and grow via oligomer fusion. Biophys. J. 96: 3781-3790.
23. Hou X, Parkington HC, Coleman HA, Mechler A, Martin LL, Aguilar MI, Small DH., 2007. Transthyretin oligomers induce calcium influx via voltage-gated calcium channels. J. Neurochem. 100: 446-457. (Pubitemid 46011005)
24. Inouye H, Domingues FS, Damas AM, Saraiva MJ, Lundgren E, Sandgren O, Kirschner DA., 1998. Analysis of x-ray diffraction patterns from amyloid of biopsied vitreous humor and kidney of transthyretin (TTR) Met30 familial amyloidotic polyneuropathy (FAP) patients: axially arrayed TTR monomers constitute the protofilament. Amyloid 5: 163-174. (Pubitemid 128699444)
25. Kad NM, Thomson NH, Smith DP, Smith DA, Radford SE., 2001. Beta(2)-microglobulin and its deamidated variant, N17D form amyloid fibrils with a range of morphologies in vitro. J. Mol. Biol. 313: 559-571. (Pubitemid 33052287)
26. Karsai Á, Grama L, Murvai Ü, Soós K, Penke B, Kellermayer MSZ., 2007. Potassium-dependent oriented growth of amyloid à 25-35 fibrils on mica. Nanotechnology 18: 345102.
27. Karsai Á, Mártonfalvi Z, Nagy A, Grama L, Penke B, Kellermayer MSZ., 2006. Mechanical manipulation of Alzheimer's amyloid à 1-42 fibrils. J. Struct. Biol. 155: 316-326. (Pubitemid 44278642)
28. 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.
29. Karsai Á, Nagy A, Kengyel A, Mártonfalvi Z, Grama L, Penke B, Kellermayer MSZ., 2005. Effect of lysine-28 side chain acetylation on the nanomechanical behavior of Alzheimer amyloid Ã25-3 fibrils. J. Chem. Info. Mod. 45: 1641-1646. (Pubitemid 41784734)
30. Kellermayer MS, Grama L, Karsai A, Nagy A, Kahn A, Datki ZL, Penke B., 2005. Reversible mechanical unzipping of amyloid beta-fibrils. J. Biol. Chem. 280: 8464-8470. (Pubitemid 40349751)
31. Kellermayer MS, Karsai A, Benke M, Soos K, Penke B., 2008. Stepwise dynamics of epitaxially growing single amyloid fibrils. Proc. Natl Acad. Sci. USA 105: 141-144.
32. Khurana R, Ionescu-Zanetti C, Pope M, Li J, Nielson L, Ramirez-Alvarado M, Regan L, Fink AL, Carter SA., 2003. A general model for amyloid fibril assembly based on morphological studies using atomic force microscopy. Biophys. J. 85: 1135-1144. (Pubitemid 36909675)
33. Kodali R, Wetzel R., 2007. Polymorphism in the intermediates and products of amyloid assembly. Curr. Opin. Struct. Biol. 17: 48-57. (Pubitemid 46242190)
34. Lai Z, Colon W, Kelly JW., 1996. The acid-mediated denaturation pathway of transthyretin yields a conformational intermediate that can self-assemble into amyloid. Biochemistry 35: 6470-6482. (Pubitemid 26164080)
35. Modler AJ, Fabian H, Sokolowski F, Lutsch G, Gast K, Damaschun G., 2004. Polymerization of proteins into amyloid protofibrils shares common critical oligomeric states but differs in the mechanisms of their formation. Amyloid 11: 215-231. (Pubitemid 40115921)
36. Modler AJ, Gast K, Lutsch G, Damaschun G., 2003. Assembly of amyloid protofibrils via critical oligomers-a novel pathway of amyloid formation. J. Mol. Biol. 325: 135-148. (Pubitemid 36153003)
37. Muller DJ, Engel A., 1997. The height of biomolecules measured with the atomic force microscope depends on electrostatic interactions. Biophys. J. 73: 1633-1644. (Pubitemid 27360752)
38. Naiki H, Nagai Y., 2009. Molecular pathogenesis of protein misfolding diseases: pathological molecular environments versus quality control systems against misfolded proteins. J. Biochem. 146: 751-756.
39. Nixon RA., 2007. Autophagy, amyloidogenesis and Alzheimer disease. J. Cell Sci. 120: 4081-4091.
40. Relini A, Canale C, De Stefano S, Rolandi R, Giorgetti S, Stoppini M, Rossi A, Fogolari F, Corazza A, Esposito G, Gliozzi A, Bellotti V., 2006. Collagen plays an active role in the aggregation of beta2-microglobulin under physiopathological conditions of dialysis-related amyloidosis. J. Biol. Chem. 281: 16521-16529.
41. Relini A, De Stefano S, Torrassa S, Cavalleri O, Rolandi R, Gliozzi A, Giorgetti S, Raimondi S, Marchese L, Verga L, Rossi A, Stoppini M, Bellotti V., 2008. Heparin strongly enhances the formation of beta2-microglobulin amyloid fibrils in the presence of type I collagen. J. Biol. Chem. 283: 4912-4920.
42. Serpell LC, Sunde M, Benson MD, Tennent GA, Pepys MB, Fraser PE., 2000. The protofilament substructure of amyloid fibrils. J. Mol. Biol. 300: 1033-1039.
43. Serpell LC, Sunde M, Fraser PE, Luther PK, Morris EP, Sangren O, Lundgren E, Blake CC., 1995. Examination of the structure of the transthyretin amyloid fibril by image reconstruction from electron micrographs. J. Mol. Biol. 254: 113-118.
44. Sousa MM, Cardoso I, Fernandes R, Guimaraes A, Saraiva MJ., 2001. Deposition of transthyretin in early stages of familial amyloidotic polyneuropathy: evidence for toxicity of nonfibrillar aggregates. Am. J. Pathol. 159: 1993-2000. (Pubitemid 33104254)
45. Sousa MM, Fernandes R, Palha JA, Taboada A, Vieira P, Saraiva MJ., 2002. Evidence for early cytotoxic aggregates in transgenic mice for human transthyretin Leu55Pro. Am. J. Pathol. 161: 1935-1948. (Pubitemid 35265550)
46. Sousa MM, Saraiva MJ., 2003. Neurodegeneration in familial amyloid polyneuropathy: from pathology to molecular signaling. Prog. Neurobiol. 71: 385-400. (Pubitemid 38125193)
47. Sunde M, Serpell LC, Bartlam M, Fraser PE, Pepys MB, Blake CC., 1997. Common core structure of amyloid fibrils by synchrotron X-ray diffraction. J. Mol. Biol. 273: 729-739. (Pubitemid 27488813)
48. Westermark P, Sletten K, Johansson B, Cornwell GG 3rd., 1990. Fibril in senile systemic amyloidosis is derived from normal transthyretin. Proc. Natl Acad. Sci. USA 87: 2843-2845.
49. Yamaguchi I, Hasegawa K, Takahashi N, Gejyo F, Naiki H., 2001. Apolipoprotein E inhibits the depolymerization of beta 2-microglobulin-related amyloid fibrils at a neutral pH. Biochemistry 40: 8499-8507. (Pubitemid 32667254)
50. Yamamoto S, Hasegawa K, Yamaguchi I, Goto Y, Gejyo F, Naiki H., 2005. Kinetic analysis of the polymerization and depolymerization of beta(2)-microglobulin-related amyloid fibrils in vitro. Biochim. Biophys. Acta 1753: 34-43. (Pubitemid 41597429)