Reversible heat-induced dissociation of β2-microglobulin amyloid fibrils

Biochemistry

Volumn 50, Issue 15, 2011, Pages 3211-3220

  Kardos, József ^a   Micsonai, András ^a   Pál Gábor, Henriett ^a,c   Petrik, Éva ^a   Gráf, László ^a   Kovács, János ^b   Lee, Young Ho ^d   Naiki, Hironobu ^e   Goto, Yuji ^d  

^a Department of Biochemistry ^*  (Hungary)

^b EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^c INSTITUTE OF ENZYMOLOGY   (Hungary)

^d OSAKA UNIVERSITY   (Japan)

^e UNIVERSITY OF FUKUI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE COMPOUNDS; AMYLOID FIBRIL; DIALYSIS-RELATED AMYLOIDOSIS; DYNAMIC PROCESS; ELEVATED TEMPERATURE; HIGHEST TEMPERATURE; IN-VIVO; INDUCED DISSOCIATION; PROTEOLYTIC DIGESTION; RECENT PROGRESS; REPOLYMERIZATION; REVERSIBLE HEAT; SIMPLE METHOD; STABLE STRUCTURES; SYNUCLEIN; THERMAL STABILITY; THIOFLAVIN;

CIRCULAR DICHROISM SPECTROSCOPY; DIALYSIS; DICHROISM; DIFFUSERS (OPTICAL); DISSOCIATION; MONOMERS; THERMODYNAMIC STABILITY;

GLYCOPROTEINS;

ALPHA SYNUCLEIN; AMYLOID; BETA 2 MICROGLOBULIN; K3 PEPTIDE; MONOMER; PEPTIDE; THIOFLAVINE; UNCLASSIFIED DRUG;

AGING; AMYLOIDOSIS; ARTICLE; CELL NUCLEUS; CIRCULAR DICHROISM; CONTROLLED STUDY; DEPOLYMERIZATION; DIALYSIS; DISSOCIATION; EQUILIBRIUM CONSTANT; FIBER; FLUORESCENCE SPECTROSCOPY; HEAT; HIGH TEMPERATURE; IN VIVO STUDY; INCUBATION TIME; MOLECULAR DYNAMICS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; REPOLYMERIZATION; THERMOSTABILITY;

AMMONIUM SULFATE; AMYLOID; BETA 2-MICROGLOBULIN; HOT TEMPERATURE; KINETICS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; SODIUM DODECYL SULFATE;

EID: 79953851306     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2000017     Document Type: Article

References (80)

1. Kelly, J. W. (1998) The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways Curr. Opin. Struct. Biol. 8, 101-106 (Pubitemid 28107921)
2. Rochet, J. C. and Lansbury, P. T., Jr. (2000) Amyloid fibrillogenesis: themes and variations Curr. Opin. Struct. Biol. 10, 60-68 (Pubitemid 30099328)
3. Stefani, M. and Dobson, C. M. (2003) Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution J. Mol. Med. 81, 678-699 (Pubitemid 37491594)
4. Makin, O. S. and Serpell, L. C. (2005) Structures for amyloid fibrils FEBS J. 272, 5950-5961 (Pubitemid 41713687)
5. Saiki, M., Honda, S., Kawasaki, K., Zhou, D., Kaito, A., Konakahara, T., and Morii, H. (2005) Higher-order molecular packing in amyloid-like fibrils constructed with linear arrangements of hydrophobic and hydrogen-bonding side-chains J. Mol. Biol. 348, 983-998 (Pubitemid 40544396)
6. Tycko, R. (2004) Progress towards a molecular-level structural understanding of amyloid fibrils Curr. Opin. Struct. Biol. 14, 96-103 (Pubitemid 38249598)
7. Chiti, F., Webster, P., Taddei, N., Clark, A., Stefani, M., Ramponi, G., and Dobson, C. M. (1999) Designing conditions for in vitro formation of amyloid protofilaments and fibrils Proc. Natl. Acad. Sci. U. S. A. 96, 3590-3594 (Pubitemid 29168954)
8. Dobson, C. M. (2003) Protein folding and misfolding Nature 426, 884-890 (Pubitemid 38056880)
9. Fandrich, M. and Dobson, C. M. (2002) The behaviour of polyamino acids reveals an inverse side chain effect in amyloid structure formation EMBO J. 21, 5682-5690 (Pubitemid 35315268)
10. Makin, O. S., Atkins, E., Sikorski, P., Johansson, J., and Serpell, L. C. (2005) Molecular basis for amyloid fibril formation and stability Proc. Natl. Acad. Sci. U. S. A. 102, 315-320 (Pubitemid 40116764)
11. Nelson, R. and Eisenberg, D. (2006) Recent atomic models of amyloid fibril structure Curr. Opin. Struct. Biol. 16, 260-265
12. Nelson, R., Sawaya, M. R., Balbirnie, M., Madsen, A. O., Riekel, C., Grothe, R., and Eisenberg, D. (2005) Structure of the cross-beta spine of amyloid-like fibrils Nature 435, 773-778 (Pubitemid 40839722)
13. Bader, R., Bamford, R., Zurdo, J., Luisi, B. F., and Dobson, C. M. (2006) Probing the mechanism of amyloidogenesis through a tandem repeat of the PI3-SH3 domain suggests a generic model for protein aggregation and fibril formation J. Mol. Biol. 356, 189-208 (Pubitemid 43069737)
14. Bhattacharyya, A. M., Thakur, A. K., and Wetzel, R. (2005) polyglutamine aggregation nucleation: thermodynamics of a highly unfavorable protein folding reaction Proc. Natl. Acad. Sci. U. S. A. 102, 15400-15405 (Pubitemid 41528069)
15. Carrotta, R., Manno, M., Bulone, D., Martorana, V., and San Biagio, P. L. (2005) Protofibril formation of amyloid beta-protein at low pH via a non-cooperative elongation mechanism J. Biol. Chem. 280, 30001-30008 (Pubitemid 41216175)
16. Harper, J. D. and Lansbury, P. T., Jr. (1997) Models of amyloid seeding in Alzheimers disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins Annu. Rev. Biochem. 66, 385-407 (Pubitemid 27274662)
17. Kad, N. M., Myers, S. L., Smith, D. P., Smith, D. A., Radford, S. E., and Thomson, N. H. (2003) Hierarchical assembly of beta2-microglobulin amyloid in vitro revealed by atomic force microscopy J. Mol. Biol. 330, 785-797
18. Kanno, T., Yamaguchi, K., Naiki, H., Goto, Y., and Kawai, T. (2005) Association of thin filaments into thick filaments revealing the structural hierarchy of amyloid fibrils J. Struct. Biol. 149, 213-218 (Pubitemid 40170103)
19. McParland, V. J., Kad, N. M., Kalverda, A. P., Brown, A., Kirwin-Jones, P., Hunter, M. G., Sunde, M., and Radford, S. E. (2000) Partially unfolded states of beta(2)-microglobulin and amyloid formation in vitro Biochemistry 39, 8735-8746 (Pubitemid 30602783)
20. Modler, A. J., Gast, K., Lutsch, G., and Damaschun, G. (2003) Assembly of amyloid protofibrils via critical oligomers - a novel pathway of amyloid formation J. Mol. Biol. 325, 135-148 (Pubitemid 36153003)
21. Naiki, H, H. N., Suzuki, S, Kimura, H, Nakakuki, K, and Gejyo, F. (1997) Establishment of a kinetic model of dialysis-related amyloid fibril extension in vitro Amyloid-Int. J. Exp. Clin. Invest. 4, 223-232 (Pubitemid 127716139)
22. Uversky, V. N. and Fink, A. L. (2004) Conformational constraints for amyloid fibrillation: the importance of being unfolded Biochim. Biophys. Acta 1698, 131-153 (Pubitemid 38591469)
23. Chiti, F., Stefani, M., Taddei, N., Ramponi, G., and Dobson, C. M. (2003) Rationalization of the effects of mutations on peptide and protein aggregation rates Nature 424, 805-808 (Pubitemid 37021713)
24. Taddei, N., Capanni, C., Chiti, F., Stefani, M., Dobson, C. M., and Ramponi, G. (2001) Folding and aggregation are selectively influenced by the conformational preferences of the alpha-helices of muscle acylphosphatase J. Biol. Chem. 276, 37149-37154
25. Pace, C. N., Shirley, B. A., and Thomson, J. A. (1990) Measuring the conformational stability of a protein, in Protein Structures: A Practical Approach (Creighton, T. E., Ed.) pp 311 - 330.
26. Brange, J., Andersen, L., Laursen, E. D., Meyn, G., and Rasmussen, E. (1997) Toward understanding insulin fibrillation J. Pharm. Sci. 86, 517-525 (Pubitemid 27203397)
27. Hamada, D. and Dobson, C. M. (2002) A kinetic study of beta-lactoglobulin amyloid fibril formation promoted by urea Protein Sci. 11, 2417-2426
28. Hirota-Nakaoka, N., Hasegawa, K., Naiki, H., and Goto, Y. (2003) Dissolution of beta2-microglobulin amyloid fibrils by dimethylsulfoxide J. Biochem. 134, 159-164 (Pubitemid 37071192)
29. Murali, J. and Jayakumar, R. (2005) Spectroscopic studies on native and protofibrillar insulin J. Struct. Biol. 150, 180-189 (Pubitemid 40615743)
30. Narimoto, T., Sakurai, K., Okamoto, A., Chatani, E., Hoshino, M., Hasegawa, K., Naiki, H., and Goto, Y. (2004) Conformational stability of amyloid fibrils of beta2-microglobulin probed by guanidine-hydrochloride-induced unfolding FEBS Lett. 576, 313-319 (Pubitemid 39388619)
31. Wille, H. and Prusiner, S. B. (1999) Ultrastructural studies on scrapie prion protein crystals obtained from reverse micellar solutions Biophys. J. 76, 1048-1062 (Pubitemid 29264586)
32. Dzwolak, W. (2006) Tuning amyloidogenic conformations through cosolvents and hydrostatic pressure: when the soft matter becomes even softer Biochim. Biophys. Acta 1764, 470-480
33. Foguel, D. and Silva, J. L. (2004) New insights into the mechanisms of protein misfolding and aggregation in amyloidogenic diseases derived from pressure studies Biochemistry 43, 11361-11370 (Pubitemid 39186958)
34. Meersman, F. and Dobson, C. M. (2006) Probing the pressure-temperature stability of amyloid fibrils provides new insights into their molecular properties Biochim. Biophys. Acta 1764, 452-460
35. Torrent, J., Balny, C., and Lange, R. (2006) High pressure modulates amyloid formation Protein Peptide Lett. 13, 271-277
36. Arora, A., Ha, C., and Park, C. B. (2004) Insulin amyloid fibrillation at above 100 degrees C: new insights into protein folding under extreme temperatures Protein Sci. 13, 2429-2436 (Pubitemid 39128863)
37. Baxa, U., Ross, P. D., Wickner, R. B., and Steven, A. C. (2004) The N-terminal prion domain of Ure2p converts from an unfolded to a thermally resistant conformation upon filament formation J. Mol. Biol. 339, 259-264 (Pubitemid 38596947)
38. Bousset, L., Briki, F., Doucet, J., and Melki, R. (2003) The native-like conformation of Ure2p in fibrils assembled under physiologically relevant conditions switches to an amyloid-like conformation upon heat-treatment of the fibrils J. Struct. Biol. 141, 132-142 (Pubitemid 36287126)
39. Dubois, J., Ismail, A. A., Chan, S. L., and Ali-Khan, Z. (1999) Fourier transform infrared spectroscopic investigation of temperature- and pressure-induced disaggregation of amyloid A Scand. J. Immunol. 49, 376-380 (Pubitemid 29185420)
40. Litvinovich, S. V., Brew, S. A., Aota, S., Akiyama, S. K., Haudenschild, C., and Ingham, K. C. (1998) Formation of amyloid-like fibrils by self-association of a partially unfolded fibronectin type III module J. Mol. Biol. 280, 245-258 (Pubitemid 28325517)
41. Morel, B., Varela, L., and Conejero-Lara, F. The thermodynamic stability of amyloid fibrils studied by differential scanning calorimetry. J. Phys. Chem. B 114, 4010 - 4019.
42. Sasahara, K., Naiki, H., and Goto, Y. (2005) Kinetically controlled thermal response of beta2-microglobulin amyloid fibrils J. Mol. Biol. 352, 700-711 (Pubitemid 41225479)
43. Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennett, W. S., Strominger, J. L., and Wiley, D. C. (1987) Structure of the human class I histocompatibility antigen, HLA-A2 Nature 329, 506-512 (Pubitemid 17131093)
44. Gejyo, F., Yamada, T., Odani, S., Nakagawa, Y., Arakawa, M., Kunitomo, T., Kataoka, H., Suzuki, M., Hirasawa, Y., and Shirahama, T. 1985, A new form of amyloid protein associated with chronic hemodialysis was identified as beta 2-microglobulin Biochem. Biophys. Res. Commun. 129, 701-706 (Pubitemid 15243930)
45. Ban, T., Hamada, D., Hasegawa, K., Naiki, H., and Goto, Y. (2003) Direct observation of amyloid fibril growth monitored by thioflavin T fluorescence J. Biol. Chem. 278, 16462-16465 (Pubitemid 36799502)
46. Kad, N. M., Thomson, N. H., Smith, D. P., Smith, D. A., and Radford, S. E. (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)
47. Ohhashi, Y., Kihara, M., Naiki, H., and Goto, Y. (2005) Ultrasonication-induced amyloid fibril formation of beta2-microglobulin J. Biol. Chem. 280, 32843-32848 (Pubitemid 41368332)
48. Chatani, E., Kato, M., Kawai, T., Naiki, H., and Goto, Y. (2005) Main-chain dominated amyloid structures demonstrated by the effect of high pressure J. Mol. Biol. 352, 941-951 (Pubitemid 41267079)
49. Chatani, E., Naiki, H., and Goto, Y. (2006) Seeding-dependent propagation and maturation of beta2-microglobulin amyloid fibrils under high pressure J. Mol. Biol. 359, 1086-1096 (Pubitemid 43842053)
50. Hoshino, M., Katou, H., Hagihara, Y., Hasegawa, K., Naiki, H., and Goto, Y. (2002) Mapping the core of the beta(2)-microglobulin amyloid fibril by H/D exchange Nat. Struct. Biol. 9, 332-336 (Pubitemid 34462549)
51. Kardos, J., Okuno, D., Kawai, T., Hagihara, Y., Yumoto, N., Kitagawa, T., Zavodszky, P., Naiki, H., and Goto, Y. (2005) Structural studies reveal that the diverse morphology of beta(2)-microglobulin aggregates is a reflection of different molecular architectures Biochim. Biophys. Acta 1753, 108-120 (Pubitemid 41597437)
52. Kardos, J., Yamamoto, K., Hasegawa, K., Naiki, H., and Goto, Y. (2004) Direct measurement of the thermodynamic parameters of amyloid formation by isothermal titration calorimetry J. Biol. Chem. 279, 55308-55314 (Pubitemid 40066528)
53. Yamaguchi, K., Katou, H., Hoshino, M., Hasegawa, K., Naiki, H., and Goto, Y. (2004) Core and heterogeneity of beta2-microglobulin amyloid fibrils as revealed by H/D exchange J. Mol. Biol. 338, 559-571 (Pubitemid 38479650)
54. Sasahara, K., Naiki, H., and Goto, Y. (2006) Exothermic effects observed upon heating of beta2-microglobulin monomers in the presence of amyloid seeds Biochemistry 45, 8760-8769 (Pubitemid 44100673)
55. Chiba, T., Hagihara, Y., Higurashi, T., Hasegawa, K., Naiki, H., and Goto, Y. (2003) Amyloid fibril formation in the context of full-length protein: effects of proline mutations on the amyloid fibril formation of beta2-microglobulin J. Biol. Chem. 278, 47016-47024 (Pubitemid 37452285)
56. Villanueva, J., Hoshino, M., Katou, H., Kardos, J., Hasegawa, K., Naiki, H., and Goto, Y. (2004) Increase in the conformational flexibility of beta 2-microglobulin upon copper binding: a possible role for copper in dialysis-related amyloidosis Protein Sci. 13, 797-809 (Pubitemid 38252576)
57. Naiki, H. and Gejyo, F. (1999) Kinetic analysis of amyloid fibril formation Methods Enzymol. 309, 305-318 (Pubitemid 29446457)
58. Naiki, H., Higuchi, K., Hosokawa, M., and Takeda, T. (1989) Fluorometric determination of amyloid fibrils in vitro using the fluorescent dye, thioflavin T1 Anal. Biochem. 177, 244-249 (Pubitemid 19088253)
59. Lee, Y. H., Chatani, E., Sasahara, K., Naiki, H., and Goto, Y. (2009) A comprehensive model for packing and hydration for amyloid fibrils of beta2-microglobulin J. Biol. Chem. 284, 2169-2175
60. Chatani, E., Lee, Y. H., Yagi, H., Yoshimura, Y., Naiki, H., and Goto, Y. (2009) Ultrasonication-dependent production and breakdown lead to minimum-sized amyloid fibrils Proc. Natl. Acad. Sci. U. S. A. 106, 11119-11124
61. Garcia, A. F., Heindl, P., Voigt, H., Buttner, M., Butz, P., Tauber, N., Tauscher, B., and Pfaff, E. (2005) Dual nature of the infectious prion protein revealed by high pressure J. Biol. Chem. 280, 9842-9847 (Pubitemid 40395830)
62. Hasegawa, K., Ono, K., Yamada, M., and Naiki, H. (2002) Kinetic modeling and determination of reaction constants of Alzheimers beta-amyloid fibril extension and dissociation using surface plasmon resonance Biochemistry 41, 13489-13498 (Pubitemid 35332684)
63. Naiki, H., Higuchi, K., Nakakuki, K., and Takeda, T. (1991) Kinetic analysis of amyloid fibril polymerization in vitro Lab Invest. 65, 104-110
64. ONuallain, B., Shivaprasad, S., Kheterpal, I., and Wetzel, R. (2005) Thermodynamics of A beta(1-40) amyloid fibril elongation Biochemistry 44, 12709-12718 (Pubitemid 41377310)
65. Cantor, C. R. and Schimmel, P. R. (1980) Biophysical Chemistry Part I, The Conformation of Biological Macromolecules, W. H. Freeman, New York.
66. Oosawa, F. and Kasai, M. (1962) A theory of linear and helical aggregations of macromolecules J. Mol. Biol. 4, 10-21
67. Hall, D. and Edskes, H. (2004) Silent prions lying in wait: a two-hit model of prion/amyloid formation and infection J. Mol. Biol. 336, 775-786 (Pubitemid 38183028)
68. Masel, J., Jansen, V. A., and Nowak, M. A. (1999) Quantifying the kinetic parameters of prion replication Biophys. Chem. 77, 139-152 (Pubitemid 29206647)
69. Tanaka, M., Collins, S. R., Toyama, B. H., and Weissman, J. S. (2006) The physical basis of how prion conformations determine strain phenotypes Nature 442, 585-589 (Pubitemid 44167919)
70. Xue, W. F., Homans, S. W., and Radford, S. E. (2008) Systematic analysis of nucleation-dependent polymerization reveals new insights into the mechanism of amyloid self-assembly Proc. Natl. Acad. Sci. U. S. A. 105, 8926-8931
71. Carulla, N., Caddy, G. L., Hall, D. R., Zurdo, J., Gairi, M., Feliz, M., Giralt, E., Robinson, C. V., and Dobson, C. M. (2005) Molecular recycling within amyloid fibrils Nature 436, 554-558 (Pubitemid 41112928)
72. Cordeiro, Y., Kraineva, J., Ravindra, R., Lima, L. M., Gomes, M. P., Foguel, D., Winter, R., and Silva, J. L. (2004) Hydration and packing effects on prion folding and beta-sheet conversion. High pressure spectroscopy and pressure perturbation calorimetry studies J. Biol. Chem. 279, 32354-32359 (Pubitemid 39014688)
73. Dirix, C., Meersman, F., MacPhee, C. E., Dobson, C. M., and Heremans, K. (2005) High hydrostatic pressure dissociates early aggregates of TTR105-115, but not the mature amyloid fibrils J. Mol. Biol. 347, 903-909 (Pubitemid 40387442)
74. Serio, T. R., Cashikar, A. G., Kowal, A. S., Sawicki, G. J., Moslehi, J. J., Serpell, L., Arnsdorf, M. F., and Lindquist, S. L. (2000) Nucleated conformational conversion and the replication of conformational information by a prion determinant Science 289, 1317-1321 (Pubitemid 30656041)
75. Myers, S. L., Jones, S., Jahn, T. R., Morten, I. J., Tennent, G. A., Hewitt, E. W., and Radford, S. E. (2006) A systematic study of the effect of physiological factors on beta2-microglobulin amyloid formation at neutral pH Biochemistry 45, 2311-2321 (Pubitemid 43271331)
76. Pal-Gabor, H., Gombos, L., Micsonai, A., Kovacs, E., Petrik, E., Kovacs, J., Graf, L., Fidy, J., Naiki, H., Goto, Y., Liliom, K., and Kardos, J. (2009) Mechanism of lysophosphatidic acid-induced amyloid fibril formation of beta(2)-microglobulin in vitro under physiological conditions Biochemistry 48, 5689-5699
77. Yamamoto, S., Hasegawa, K., Yamaguchi, I., Tsutsumi, S., Kardos, J., Goto, Y., Gejyo, F., and Naiki, H. (2004) Low concentrations of sodium dodecyl sulfate induce the extension of beta 2-microglobulin-related amyloid fibrils at a neutral pH Biochemistry 43, 11075-11082 (Pubitemid 39433696)
78. Yamamoto, S., Yamaguchi, I., Hasegawa, K., Tsutsumi, S., Goto, Y., Gejyo, F., and Naiki, H. (2004) Glycosaminoglycans enhance the trifluoroethanol- induced extension of beta 2-microglobulin-related amyloid fibrils at a neutral pH J. Am. Soc. Nephrol. 15, 126-133 (Pubitemid 38020704)
79. Relini, A., Canale, C., De Stefano, S., Rolandi, R., Giorgetti, S., Stoppini, M., Rossi, A., Fogolari, F., Corazza, A., Esposito, G., Gliozzi, A., and 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
80. White, H. E., Hodgkinson, J. L., Jahn, T. R., Cohen-Krausz, S., Gosal, W. S., Müller, S., Orlova, E. V., Radford, S. E., and Saibil, H. R. (2009) Globular tetramers of beta(2)-microglobulin assemble into elaborate amyloid fibrils J. Mol. Biol. 389, 48-57