Early stages of β2-microglobulin aggregation and the inhibiting action of αB-crystallin

Proteins: Structure, Function and Genetics

Volumn 73, Issue 4, 2008, Pages 1037-1046

  Pullara, Filippo ^a   Emanuele, Antonio ^a,b  

^a UNIVERSITY OF PALERMO   (Italy)

^b NONE   (Italy)

Author keywords

Amyloid formation; Chaperon; Free energy landscapes; Light scattering; Pre fibrillar aggregates; Self assembly; Solvent induced forces

Indexed keywords

ALPHA CRYSTALLIN; AMYLOID PROTEIN; BETA 2 MICROGLOBULIN; CHAPERONE; MONOMER; OLIGOMER; SOLVENT;

ARTICLE; ENERGY TRANSFER; INHIBITION KINETICS; LIGHT SCATTERING; NANOFILTRATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN MODIFICATION; SOLUTE; STOICHIOMETRY; THERMODYNAMICS; CHEMISTRY; COMPUTER PROGRAM; HUMAN; LIGHT; PROTEIN QUATERNARY STRUCTURE; RADIATION SCATTERING; TIME;

ALPHA-CRYSTALLIN B CHAIN; BETA 2-MICROGLOBULIN; HUMANS; LIGHT; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; SCATTERING, RADIATION; SOFTWARE; TIME FACTORS;

EID: 58149316598     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22122     Document Type: Article

References (74)

1. Jahn TR, Parker M, Homans SW, Radford SE. Amyloid formation under physiological conditions proceeds via a native-like folding intermediate. Nat Struct Mol Biol 2006;13:195-201. (Pubitemid 43348504)
2. Lansbury PT, Lashuel HA. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 2006;443: 774-779. (Pubitemid 44622681)
3. Dobson CM. Prying into prions. Nature 2005;435:747-749.
4. Collinge J. Prion diseases of humans and animals: their causes and molecular basis. Annu Rev Neurosci 2001;24:519-550. (Pubitemid 32695238)
5. Rochet JC, Lansbury PT, Jr. Amyloid fibrillogenesis: themes and variations. Curr Opin Struct Biol 2000;10:60-68.
6. Jackson GS, Clarke AR. Mammalian prion protein. Curr Opin Struct Biol 2000;10:69-74.
7. Kelly JW. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr Opin Struc Biol 1998; 8:101-106. (Pubitemid 28107921)
8. BenNaim A, Ting KL, Jernigan RL. Solvent effect on binding thermodynamics of biopolymers. Biopolymers 1990;29:901-919. (Pubitemid 20145686)
9. Kerbs MRH, Bromley EHC, Rogers SS, Donald AM. The mechanism of amyloid spherulite formation by bovin insulin. Biophys J 2005;88:2013-2021. (Pubitemid 40976211)
10. Fishwick CWG, Aggeli A, Boden N, Davies RP, Beevers AJ, Carrick L, McLeish TCB, Nyrkova IA, Semenov AN. Self-assembling β-sheet tape forming peptides. Supramol Chem 2006;18:435-443. (Pubitemid 44174389)
11. San Biagio PL, Palma MU. Spinodal lines and Flory-Huggins freeenergies for solutions of human hemoglobins HbS and HbA. Biophys J 1991;60:508-512.
12. Vaiana SM, Palma-Vittorelli MB, Palma MU. Time scale of protein aggregation dictated by liquid-liquid demixing. Proteins 2003;51: 147-153. (Pubitemid 36293040)
13. Manno M, Emanuele A, Martorana V, San Biagio PL, Bulone D, Palma-Vittorelli MB, McPerson DT, Xu J, Parker TM, Urry DW. Interaction of processes on different length scales in a bioelastomer capable of performing energy conversion. Biopolymers 2001;59:51-64. (Pubitemid 32531786)
14. Manno M, San Biagio PL, Palma MU. The role of pH on instability and aggregation of sickle hemoglobin solutions. Proteins 2004;55: 169-176. (Pubitemid 38292844)
15. San Biagio PL, Martorana V, Emanuele A, Vaiana SM, Manno M, Bulone D, Palma-Vittorelli MB, Palma MU. Interacting processes in protein coagulation. Proteins 1999;37:116-120.
16. Pullara F, Emanuele A, Palma-Vittorelli MB, Palma MU. Lysozyme crystallization rates controlled by anomalous fluctuations. J Cryst Growth 2005;274:536-544. (Pubitemid 40114401)
17. Corazza A, Pettirossi F, Viglino P, Verdone G, Garcia J, Dumy P, Giorgetti S, Mangione P, Raimondi S, Stoppini M, Bellotti V, Esposito G. Properties of some variants of human β2-microglobulin and amyloidogenesis. J Biol Chem 2004;279:9176-9189. (Pubitemid 38295981)
18. Hartl FU, Hayer-Hartl M. Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 2002;295:1852-1858. (Pubitemid 34214115)
19. Ben-Zvi AP, Goloubinoff P. Review: mechanisms of disaggregation and refolding of stable protein aggregates by molecular chaperones. J Struct Biol 2001;135:84-93. (Pubitemid 33733497)
20. Saper MA, Bjorkman PJ, Wiley DC. Refined structure of the human histocompatibility antigen HLA-A2 at 2.6 Å resolution. J Mol Biol 1991;219:277-319.
21. Gejyo F, Yamada T, Odani S, Nakagawa Y, Arakawa M, Kunitomo T, Kataoka H, Suzuki M, Hirasawa Y, Shirahama T, Cohen A. S, Schmid K.. A new form of amyloid protein associated with chronic hemodialysis was identified as b2-microglobulin. Biochem Biophys Res Commun 1985;129:701-706. (Pubitemid 15243930)
22. Verdone G, Corazza A, Viglino P, Pettirossi F, Giorgetti S, Mangione P, Andreola A, Stoppini M, Bellotti V, Esposito G. The solution structure of human β2-microglobulin reveals the prodromes of its amyloid transition. Protein Sci 2002;11:487-499. (Pubitemid 34171254)
23. Esposito G, Michelutti R, Verdone G, Viglino P, Hernández H, Robinson CV, Amoresano A, Dal Piaz F, Monti M, Pucci P, Mangione P, Asti L, Stoppini M, Merlini G, Ferri G, Bellotti V. Removal of the Nterminal hexapeptide from human β2-microglobulin facilitates protein aggregation and fibril formation. Protein Sci 2000;9:831-845. (Pubitemid 30353325)
24. 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. Collagen plays an active role in the aggregation of β2-microglobulin under physiopathological conditions of dialysis-related amyloidosis. J Biol Chem 2006;281:16521-16529. (Pubitemid 43909603)
25. Hoshino M, Katou H, Hagihara Y, Hasegawa K, Naiki H, Goto Y. Mapping the core of the β(2)-microglobulin amyloid fibril by H/D exchange. Nat Struct Biol 2002;9:332-336.
26. McParland VJ, Kalverda AP, Homans SW, Radford SE. Structural properties of an amyloid precursor of β(2)-microglobulin. Nat Struct Biol 2002;9:326-331.
27. Eakin CM, Knight JD, Morgan CJ, Gelfand MA, Miranker AD. Formation of a copper specific binding site in non-native states of β- 2-microglobulin. Biochemistry 2002;41:10646-11065 (Pubitemid 34913324)
28. Villanueva J, Hoshino M, Katou H, Kardos J, Hasegawa K, Naiki H, Goto Y. Increase in the conformational flexibility of β2-microglobulin upon copper binding: a possible role for copper in dialysisrelated amyloidosis. Protein Sci 2004;13:797-809. (Pubitemid 38252576)
29. Linse S, Cabaleiro-Lago C, Xue WF, Lynch I, Lindman S, Thulin E, Radford SE, Dawson KA. Nucleation of protein fibrillation by nanoparticles. PNAS 2007;104:8691-8696.
30. Fink AL. Natively unfolded proteins. Curr Opin Struct Biol 2005; 15:35-41.
31. Uversky VN. Neuropathology, biochemistry, and biophysics of asynuclein aggregation. J Neurochem 2007;103:17-37. (Pubitemid 47407730)
32. Naiki H, Hashimoto N, Suzuki S, Kimura H, Nakakuki K, Gejyo F. Establishment of a kinetic model of dialysis-related amyloid fibril extension in vitro. Amyloid Int J Exp Clin Invest 1997;4:223-232. (Pubitemid 127716139)
33. Gosal WS, Morton IJ, Hewitt EW, Smith DAM, Thomson NH, Radford SE. Competing pathways determine fibril morphology in the self-assembly of β(2)-microglobulin into amyloid. J Mol Biol 2005;351:850-864.
34. Raman B, Ban T, Sakai M, Pasta SY, Ramakrishna T, Naiki H, Goto Y, Rao CM. αB-crystallin, a small heat-shock protein, prevents the amyloid fibril growth of an amyloid β-peptide and β2-microglobulin. Biochem J 2005;392:573-581. (Pubitemid 43022737)
35. Kad NM, Myers SL, Smith DP, Alistair Smith D, Radford SE, Thomson NH. Hierarchical assembly of β2-microglobulin amyloid in vitro revealed by atomic force microscopy. J Mol Biol 2003; 330:785-797.
36. Morgan CJ, Gelfand M, Atreya C, Miranker AD. Kidney dialysisassociated amyloidosis: a molecular role for copper in fiber formation. J Mol Biol 2001;309:339-345. (Pubitemid 32553492)
37. Yamamoto S, Hasegawa K, Yamaguchi I, Tsutsumi S, Kardos J, Goto Y, Gejyo F, Naiki H. Low concentrations of sodium dodecyl sulfate induce the extension of β2-microglobulin-related amyloid fibrils at a neutral pH. Biochemistry 2004;43:11075-11082. (Pubitemid 39433696)
38. Yamamoto S, Yamaguchi I, Hasegawa K, Tsutsumi S, Goto Y, Gejyo F, Naiki H. Glycosaminoglycans enhance the trifluoroethanolinduced extension of β2-microglobulin-related amyloid fibrils at a neutral pH. J Am Soc Nephrol 2004;15:126-133. (Pubitemid 38020704)
39. Horwitz J, Huang QL, Ding L, Bova MP. Lens α-crystallin: chaperone- like properties. Meth Enzymol 1998;290:365-383. (Pubitemid 28157764)
40. Sun TX, Liang JJN. Intermolecular exchange and stabilization of recombinant human αA- and αB-crystallin. J Biol Chem 1998;273: 286-290. (Pubitemid 28042206)
41. Andleya UP. Crystallins in the eye: Function and pathology. Prog Retinal Eye Res 2007;26:78-98.
42. Bhat SP, Nagineni CN. α-B subunit of lens-specific protein α-crystallin is present in other ocular and non-ocular tissues. Biochem Biophys Res Commun 1989;158:319-325. (Pubitemid 19045081)
43. Derham BK, Harding JJ. a-crystallin as a molecular chaperone. Prog Retin Eye Res 1999;18:463-509.
44. Clark JI, Muchowski PJ. Small heat-shock proteins and their potential role in human disease. Curr Opin Struct Biol 2000;10:52-59. (Pubitemid 30099327)
45. Horwitz J. The function of α-crystallin in vision. Semin Cell Dev Biol 2000;11:53-60.
46. Török Z, Goloubinoff P, Horvath I, Tsvetkova NM, Glatz A, Balogh G, Varvasovszki V, Los DA, Vierling E, Crowe JH, Vigh L. Synechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone- mediated refolding. PNAS 2001;98:3098-3103. (Pubitemid 32220805)
47. Rekas A, Adda CG, Aquilina JA, Barnham KJ, Sunde M, Galatis D, Williamson NA, Masters CL, Anders RF, Robinson CV, Cappai R, Carver JA. Interaction of the molecular chaperone αB-crystallin with α-synuclein: effects on amyloid fibril formation and chaperone activity. J Mol Biol 2004;340:1167-1183. (Pubitemid 38968709)
48. Berne A, Pecora R. Dynamic light scattering. New York: Wiley; 1976.
49. Braginskaya TG, Dobitchin PD, Ivanova MA, Klyubin VV, Lomakin AV, Noskin VA, Shmele GE, Tolpina SP. Analysis of the polydispersity by photon correlation spectroscopy. Regularization procedure. Physica Scripta 1983;28:73-79.
50. Carver JA, Lindner RA, Lyon C, Canet D, Hernandez H, Dobson CM, Redfield C. The interaction of the molecular chaperone acrystallin with unfolding α-lactalbumin: a structural and kinetic spectroscopic study. J Mol Biol 2002;318:815-827. (Pubitemid 34729371)
51. Martin JE, Wilcoxon J, Odinek J. Decay of density fluctuations in gels. Phys Rev A 1991;43:858-872.
52. Lee S, Carson K, Rice-Ficht A, Good T. Hsp20, a novel α-crystallin, prevents Aβ fibril formation and toxicity. Protein Sci 2005;14:593-601. (Pubitemid 40283897)
53. Cao X, Bansil R, Bhaskar KR, Turner BS, LaMont JT, Niu N, Afdhal NH. pH-Dependent conformational change of gastric mucin leads to sol-gel transition. Biophys J 1999;76:1250-1258. (Pubitemid 29262607)
54. Kita R, Takahashi A, Kaibara M. Formation of fibrin gel in fibrinogen- thrombin system: static and dynamic light scattering study. Biomacromolecules 2002;3:1013-1020.
55. Okamoto M, Norisuye T. Time-resolved dynamic light scattering study on gelation and gel-melting processes of gelatin gels. Macromolecules 2001;34:8496-8502. (Pubitemid 33093156)
56. Zhu PW, Napper DH. The effect of polymer concentration on the dynamics of adsorbed poly(N-isopropylacrylamide) at particle surfaces in water. J Coll Interface Sci 1999;214:389-394. (Pubitemid 29394757)
57. Krall AH, Weitz DA. Internal dynamics and elasticity of fractal colloidal gels. PRL 1998;80:778-781. (Pubitemid 128623859)
58. Cipelletti L, Manley S, Ball RC, Weitz DA. Universal aging features in the restructuring of fractal colloidal gels. PRL 2000;84:2275-2278.
59. Sandkühler P, Sefcik J, Morbidelli M. Kinetics of gel formation in dilute dispersions with strong attractive particle interactions. Adv Coll Interface Sci. 2004;108-109:133-143.
60. Carrick L, Tassieri M, Waigh TA, Aggeli A, Boden N, Bell C, Fisher J, Ingham E, Evans RML. The internal dynamic modes of charged self-assembled peptide fibrils. Langmuir 2005;21:3733-3737.
61. Kroy K, Frey E. Dynamic scattering from solutions of semiflexible polymers. Phys Rev E 1997;55:3092-3101. (Pubitemid 127619368)
62. Zimm BH. Dynamics of polymer molecules in dilute solutions: viscoelasticity, flow birefringence and dielectric loss. J Chem Phys 1956;24:269-278.
63. Outeiro TF, Klucken J, Strathearn KE, Liu F, Nguyen P, Rochet JC, Hyman BT, McLean PJ. Small heat shock proteins protect against asynuclein- induced toxicity and aggregation. Biochem Biophys Res Commun 2006;351:631-638. (Pubitemid 44780855)
64. Goloubinoff P, De Los Rios P. The mechanism of Hsp70 chaperones: (entropic) pulling the models together. TRENDS Biochem Sci 2007;32:372-380. (Pubitemid 47126861)
65. Carver JA, Rekas A, Thorn DC, Wilson MR. Small heat-shock proteins and clusterin: intra- and extracellular molecular chaperones with a common mechanism of action and function? IUBMB Life 2003;55:661-668.
66. Vaiana SM, Manno M, Emanuele A, Palma-Vittorelli MB, Palma MU. The role of solvent in protein folding and in aggregation. J Biol Phys 2001;27:133-145. (Pubitemid 34062479)
67. San Biagio PL, Madonia F, Newman J, Palma MU. Sol-sol structural transition of aqueous agarose systems. Biopolymers 1986;25: 2255-2269.
68. San Biagio PL, Bulone D, Emanuele A, Palma MU. Self-assembly of biopolymeric structures below the threshold of random cross-link percolation. Biophys J 1996;70:494-499. (Pubitemid 26021489)
69. Vaiana SM, Rotter MA, Emanuele A, Ferrone FA, Palma-Vittorelli MB. Effect of T-R conformational change on sickle-cell hemoglobin interactions and aggregation. Proteins 2005;58:426-438. (Pubitemid 40076056)
70. Vaiana SM, Emanuele A, Palma-Vittorelli MB, Palma MU. Irreversible formation of intermediate BSA oligomers requires and induces conformational changes. Proteins 2004;55:1053-1062. (Pubitemid 38702962)
71. Corti M, Degiorgio V. Critical behavior of a micellar solution. Phys Rev Lett 1980;45:1045-1048.
72. Lomakin A, Teplow DB, Kirschner DA, Benedek GB. Kinetic theory of fibrillogenesis of amyloid b-protein. Proc Natl Acad Sci USA 1997;94:7942-7947. (Pubitemid 27343754)
73. Bulone D, San Biagio PL. Mesoscopic gel at low agarose concentration in water: a dynamic light scattering study. Biophys J 1995;68: 1569-1573.
74. Ghosh K, Ozkan SB, Dill KA. The ultimate speed limit to protein folding is conformational searching. J Am Chem Soc 2007;129: 11920-11927. (Pubitemid 47515346)