Insights into the mechanism of aggregation and fibril formation from bovine serum albumin

Journal of Physical Chemistry B

Volumn 115, Issue 14, 2011, Pages 4195-4205

  Bhattacharya, Mily ^a   Jain, Neha ^a   Mukhopadhyay, Samrat ^a  

^a INDIAN INSTITUTE OF SCIENCE EDUCATION AND RESEARCH MOHALI   (India)

Author keywords

[No Author keywords available]

Indexed keywords

AGGLOMERATION; AMINO ACIDS; BODY FLUIDS; DICHROISM; FLUOROPHORES; GLYCOPROTEINS; IONIC STRENGTH; ISOMERS; OLIGOMERS; PROTEINS;

AGGREGATION PROCESS; AMYLOID FIBRIL; AMYLOID-LIKE FIBRIL; BOVINE SERUM ALBUMINS; CD SPECTROSCOPY; CIRCULAR DICHROISM; CONFORMATIONAL CONVERSION; CONFORMATIONAL ISOMERS; ELEVATED TEMPERATURE; FIBRIL FORMATION; FLUORESCENCE INTENSITIES; HELICAL PROTEINS; INTRINSIC TRYPTOPHANS; PH CONDITION; PROTEIN CONCENTRATIONS; STRUCTURAL CHANGE; STRUCTURAL CONTENT; STRUCTURAL PROBES; TEMPORAL EVOLUTION; TIME DEPENDENCE;

CIRCULAR DICHROISM SPECTROSCOPY;

EID: 79953805289     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp111528c     Document Type: Article

References (75)

1. Luheshi, L. M.; Crowther, D. C.; Dobson, C. M. Protein misfolding and disease: From the test tube to the organism Curr. Opin. Chem. Biol. 2008, 12, 25-31
2. Jahn, T. R.; Radford, S. E. Folding versus aggregation: Polypeptide conformations on competing pathways Arch. Biochem. Biophys. 2008, 469, 100-117 (Pubitemid 350214559)
3. Wetzel, R. Kinetics and thermodynamics of amyloid fibril assembly Acc. Chem. Res. 2006, 39, 671-679
4. Pepys, M. B. Amyloidosis Annu. Rev. Med. 2006, 57, 223-241 (Pubitemid 43261989)
5. Miranker, A. D. Unzipping the mysteries of amyloid fiber formation Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 4335-4336 (Pubitemid 38437410)
6. Tycko, R. Progress towards a molecular level structural understanding of amyloid fibrils Curr. Opin. Struct. Biol. 2004, 14, 96-103 (Pubitemid 38249598)
7. Rochet, J. C.; Lansbury, P. T., Jr. Amyloid fibrillogenesis: Themes and variations Curr. Opin. Struct. Biol. 2000, 10, 60-68 (Pubitemid 30099328)
8. Gazit, E. Mechanisms of amyloid fibril self-assembly and inhibition: Model short peptides as a key research tool FEBS J. 2005, 272, 5971-5978 (Pubitemid 41713689)
9. Guijarro, J. I.; Sunde, M.; Jones, J. A.; Campbell, I. D.; Dobson, C. M. Amyloid fibril formation by an SH3 domain Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 4224-4228 (Pubitemid 28207893)
10. Chiti, F.; Webster, P.; Taddei, N.; Clark, A.; Stefani, M.; Ramponi, G.; Dobson, C. M. Designing conditions for in vitro formation of amyloid protofilaments and fibrils Proc. Natl. Acad. Sci. U.S.A. 1999, 96, 3590-3594 (Pubitemid 29168954)
11. Fandrich, M.; Fletcher, M. A.; Dobson, C. M. Amyloid fibrils from muscle myoglobin Nature 2001, 410, 165-166
12. Uversky, V. N.; Fink, A. L. Conformational constraints for amyloid fibrillation: The importance of being unfolded Biochim. Biophys. Acta 2004, 1698, 131-153 (Pubitemid 38591469)
13. Kelly, J. W. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways Curr. Opin. Struct. Biol. 1998, 8, 101-106 (Pubitemid 28107921)
14. Zerovnik, E. Amyloid-fibril formation, proposed mechanisms and relevance to conformational disease Eur. J. Biochem. 2002, 269, 3362-3371 (Pubitemid 34988978)
15. Morel, B.; Casares, S.; Conejero-Lara, F. A. Single mutation induces amyloid aggregation in the α-spectrin SH3 domain: Analysis of the early stages of fibril formation J. Mol. Biol. 2006, 356, 453-468 (Pubitemid 43099983)
16. Chiti, F.; Taddei, N.; Baroni, F.; Capanni, C.; Stefani, M.; Ramponi, G.; Dobson, C. M. Kinetic partitioning of protein folding and aggregation Nat. Struct. Biol. 2002, 9, 137-143 (Pubitemid 34132417)
17. Chiti, F.; Stefani, M.; Taddei, N.; Ramponi, G.; Dobson, C. M. Rationalization of the effects of mutations on peptide and protein aggregation rates Nature 2003, 424, 805-808 (Pubitemid 37021713)
18. Volles, M. J.; Lee, S.-J.; Rochet, J.-C.; Shtilerman, M. D.; Ding, T. T.; Kessler, J. C.; Lansbury, P. T. Vesicle permeabilization by protofibrillar α-synuclein: Implications for the pathogenesis and treatment of Parkinsonb s disease Biochemistry 2001, 40, 7812-7819 (Pubitemid 32622972)
19. Kayed, R.; Sokolov, Y.; Edmonds, B.; McIntire, T. M.; Milton, S. C.; Hall, J. E.; Glabe, C. G. Permeabilization of lipid bilayers is a common conformation-dependent activity of soluble amyloid oligomers in protein misfolding diseases J. Biol. Chem. 2004, 279, 46363-46366 (Pubitemid 39518276)
20. Bucciantini, M.; Giannoni, E.; Chiti, F.; Baroni, F.; Formigli, L.; Zurdo, J.; Taddei, N.; Ramponi, G.; Dobson, C. M.; Stefani, M. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases Nature 2002, 416, 507-511 (Pubitemid 34288846)
21. Herczenik, E.; Gebbink, M. F. B. G. Molecular and cellular aspects of protein misfolding and disease FASEB J. 2008, 22, 2115-2133 (Pubitemid 351948631)
22. Davis, T. J.; Soto-Ortega, D. D.; Kotarek, J. A.; Gonzalez-Velasquez, F. J.; Sivakumar, K.; Wu, L.; Wang, Q.; Moss, M. A. Comparative study of inhibition at multiple stages of amyloid-β self-assembly provides mechanistic insight Mol. Pharmacol. 2009, 76, 405-413
23. Carter, D. C.; Ho, J. X. Structure of serum albumin Adv. Protein Chem. 1994, 45, 153-203 (Pubitemid 24139888)
24. Peters, T., Jr. Serum albumin Adv. Protein Chem. 1985, 37, 161-245
25. Rossing, T. H.; Maffaeo, N.; Fencl, V. Acid-base effects of altering plasma protein concentration in human blood in vitro J. Appl. Physiol. 1986, 61, 2260-2265 (Pubitemid 17233698)
26. He, X. M.; Carter, D. C. Atomic structure and chemistry of human serum albumin Nature 1992, 358, 209-215
27. Sugio, S.; Kashima, A.; Mochizuki, S.; Noda, M.; Kobayashi, K. Crystal structure of human serum albumin at 2.5Å resolution Protein Eng. 1999, 12, 439-446 (Pubitemid 29322441)
28. Luetscher, J. A. Serum albumin. II. Identification of more than one albumin in horse and human serum by electrophoretic mobility in acid solution J. Am. Chem. Soc. 1939, 61, 2888-2890
29. Williams, E. J.; Foster, J. F. The aggregation of bovine plasma albumin at low pH J. Am. Chem. Soc. 1960, 82, 3741-3745
30. Foster, J. F. Some aspects of the structure and the conformational properties of serum albumin. In Albumin structure, function and uses; Rosenoer, V. M.; Oratz, M.; Rothschild, M. A., Eds.; Pergamon: Oxford, U.K., 1977; pp 53 - 84.
31. Wilting, J.; Kremer, J. M. H.; Ijzerman, A. P.; Schulman, S. G. The kinetics of the binding of warfarin to human serum albumin as studied by stopped-flow spectrophotometry Biochim. Biophys. Acta 1982, 706, 96-104 (Pubitemid 13235259)
32. Militello, V.; Vetri, V.; Leone, M. Conformational changes involved in thermal aggregation processes of bovine serum albumin Biophys. Chem. 2003, 105, 133-141 (Pubitemid 36970268)
33. Militello, V.; Casarino, C.; Emanuele, A.; Giostra, A.; Pullara, F.; Leone, M. Aggregation kinetics of bovine serum albumin studied by FTIR spectroscopy and light scattering Biophys. Chem. 2004, 107, 175-187 (Pubitemid 38220958)
34. Taboada, P.; Barbosa, S.; Castro, E.; Mosquera, V. Amyloid fibril formation and other aggregate species formed by human serum albumin association J. Phys. Chem. B 2006, 110, 20733-20736 (Pubitemid 44797322)
35. Holm, N. K.; Jespersen, S. K.; Thomassen, L. V.; Wolff, T. Y.; Sehgal, P.; Thomsen, L. A.; Christiansen, G.; Andersen, C. B.; Knudsen, A. D.; Otzen, D. E. Aggregation and fibrillation of bovine serum albumin Biochim. Biophys. Acta 2007, 1774, 1128-1138 (Pubitemid 47333256)
36. Vetri, V.; Librizzi, F.; Leone, M.; Militello, V. Thermal aggregation of bovine serum albumin at different pH: Comparison with human serum albumin Eur. Biophys. J. 2007, 36, 717-725 (Pubitemid 350092526)
37. Juarez, J.; Taboada, P.; Mosquera, V. Existence of different structural intermediates on the fibrillation pathway of human serum albumin Biophys. J. 2009, 96, 2353-2370
38. Juarez, J.; Lopez, S. G.; Cambon, A.; Taboada, P.; Mosquera, V. Influence of electrostatic interactions on the fibrillation process of human serum albumin J. Phys. Chem. B 2009, 113, 10521-10529
39. 2+ ions on the fibrillar aggregates formed by the amyloid peptide and other peptides at the organic-aqueous interface Chem. Phys. Lett. 2010, 496, 104-108
40. Wei, Y.; Chen, L.; Chen, J.; Ge, L.; He, R. Q. Rapid glycation with D-ribose induces globular amyloid-like aggregations of BSA with high cytotoxicity to SH-SY5Y cells. BMC Cell Biol. 2009, 10, doi: 10.1186/1471-2121-10-10.
41. Lindgren, M.; Sörgjerd, K.; Hammarström, P. Detection and characterization of aggregates, prefibrillar amyloidogenic oligomers and protofibrils using fluorescence spectroscopy Biophys. J. 2005, 88, 4200-4212 (Pubitemid 40991131)
42. Allsop, D.; Swanson, L.; Moore, S.; Davies, Y.; York, A.; El-Agnaf, O. M. A.; Soutar, I. Fluorescence anisotropy: A method for early detection of Alzheimer β-peptide (A-β) aggregation Biochem. Biophys. Res. Commun. 2001, 285, 58-63 (Pubitemid 32912510)
43. Mukhopadhyay, S.; Nayak, P. K.; Udgaonkar, J. B.; Krishnamoorthy, G. Characterization of the formation of amyloid protofibrils from barstar by mapping residue-specific fluorescence dynamics J. Mol. Biol. 2006, 358, 935-942 (Pubitemid 44382447)
44. Dusa, A.; Kaylor, J.; Edridge, S.; Bodner, N.; Hong, D.-P.; Fink, A. L. Characterization of oligomers during α-Synuclein aggregation using intrinsic tryptophan fluorescence Biochemistry 2006, 45, 2752-2760
45. Padrick, S. B.; Miranker, A. D. Islet amyloid: Phase partitioning and secondary nucleation are central to the mechanism of fibrillogenesis Biochemistry 2002, 41, 4694-4703 (Pubitemid 34275671)
46. Atanasiu, C.; Su, T.-J.; Sturrock, S. S.; Dryden, D. T. F. Interaction of the ocr gene 0.3 protein of bacteriophage T7 with EcoKI restriction/ modification enzyme Nucleic Acids Res. 2002, 30, 3936-3944
47. Hudson, E. N.; Weber, G. Synthesis and characterization of two fluorescence sulfhydryl reagents Biochemistry 1973, 12, 4154-4161
48. Bhattacharya, M.; Jain, N.; Bhasne, K.; Kumari, V.; Mukhopadhyay, S. pH-induced conformational isomerization of bovine serum albumin studied by extrinsic and intrinsic protein fluorescence. J. Fluoresc. (Published online Dec. 3, 2010; DOI: 10.1007/s10895-010-0781-3).
49. Lakowicz, J. R. Principles of fluorescence spectroscopy, 3 rd ed.; Springer: New York, 2006.
50. Levine, H., III. Quantification of β-sheet amyloid fibril structures with thioflavin T Methods Enzymol. 1999, 309, 274-284
51. The sample incubated at 300 N
52. Aggregation at pH 3.5 and 5 under identical incubation conditions could not be monitored since, in the former, the protein became increasingly turbid with time upon heating that resulted in an inconsistent, oscillating pattern in the ThT fluorescence intensity. For the sample incubated at pH 5, the protein coagulated within 4 min of heating, which could be accounted for the fact that pH 5 is very close to the isoelectric point (pI = 4.5-4.8) of BSA, implying that the aggregation mechanism is b more disorderedb wherein larger aggregates add onto the smaller ones (see ref 36).
53. Mishra, R.; Sörgjerd, K.; Nyström, S.; Nordigalrden, A.; Yu, Y.-C.; Hammarström, P. Lysozyme amyloidogenesis is accelerated by specific nicking and fragmentation but decelerated by intact protein binding and conversion J. Mol. Biol. 2007, 366, 1029-1044 (Pubitemid 46175878)
54. Jain, S.; Udgaonkar, J. B. Evidence for stepwise formation of amyloid fibrils by the mouse prion protein J. Mol. Biol. 2008, 382, 1228-1241
55. Although the steady-state fluorescence anisotropy does not allow us to determine the exact oligomeric size and the aggregation number, it is likely that the initial oligomers are not very large since none of the fluorescent reporters exhibited a large increase in the anisotropy upon oligomer formation. Subsequently, these small oligomers grew in size during fibril formation as indicated by a large increase in the anisotropy.
56. Daniel, E.; Weber, G. Cooperative effects in binding by bovine serum albumin I: The binding of 1-anilino-8-naphthalenesulfonate fluorimetric titrations Biochemistry 1966, 5, 1893-1900
57. Bolognesi, B.; Kumita, J. R.; Barros, T. P.; Esbjorner, E. K.; Luheshi, L. M.; Crowther, D. C.; Wilson, M. R.; Dobson, C. M.; Favrin, G.; Yerbury, J. J. ANS binding reveals common features of cytotoxic amyloid species ACS Chem. Biol. 2010, 5, 735-740
58. Pepys, M. B.; Hawkins, P. H.; Booth, D. R.; Vigushin, D. M.; Tennent, G. A.; Soutar, A. K.; Totty, N.; Bguyen, O.; Blake, C. C.; Terry, C. J.; Feest, T. G.; Zalin, A. M.; Hsuan, J. J. Human lysozyme gene mutations cause hereditary systemic amyloidosis Nature 1993, 362, 553-557 (Pubitemid 23113032)
59. Harper, J. D.; Lansbury, P. T., Jr. Models of amyloid seeding in Alzheimerb s disease and scrapie: Mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins Annu. Rev. Biochem. 1997, 66, 385-407 (Pubitemid 27274662)
60. Oosawa, F.; Asakura, S.; Hotta, K.; Nobuhisa, I.; Ooi, T. G-F transformation of actin as a fibrous condensation J. Polym. Sci. 1959, 37, 323-336
61. Knowles, T. P. J.; Waudby, C. A.; Devlin, G. L.; Cohen, S. I. A.; Aguzzi, A.; Vendruscolo, M.; Terentjev, E. M.; Welland, M. E.; Dobson, C. M. An analytical solution to the kinetics of breakable filament assembly Science 2009, 326, 1533-1537
62. Radford, S. E.; Gosal, W. S.; Platt, G. W. Towards an understanding of the structural and molecular mechanism of β2-microglobulin amyloid formation in vitro Biochim. Biophys. Acta 2005, 1753, 51-63 (Pubitemid 41597431)
63. Sasahara, K.; Yagi, H.; Sakai, M.; Naiki, H.; Goto, Y. Amyloid nucleation triggered by agitation of β2-microglobulin under acidic and neutral pH conditions Biochemistry 2008, 47, 2650-2660 (Pubitemid 351304570)
64. Hurshman, A. R.; White, J. T.; Powers, E. T.; Kelly, J. W. Transthyretin aggregation under partially denaturing conditions is a downhill polymerization Biochemistry 2004, 43, 7365-7381 (Pubitemid 38745754)
65. Kumar, S.; Mohanty, S. K.; Udgaonkar, J. B. Mechanism of formation of amyloid protofibrils of barstar from soluble oligomers: Evidence for multiple steps and lateral association coupled to conformational conversion J. Mol. Biol. 2007, 367, 1186-1204 (Pubitemid 46389623)
66. Thusius, D.; Dessen, P.; Jallon, J.-M. Mechanism of bovine liver glutamate dehydrogenase self-association I. Kinetic evidence for a random association of polymer chains J. Mol. Biol. 1975, 92, 413-432
67. Powers, E. T.; Powers, D. L. The kinetics of nucleated polymerizations at high concentrations: Amyloid fibril formation near and above the b supercritical concentrationbBiophys. J. 2006, 91, 122-132 (Pubitemid 44015313)
68. Pappu, R. V.; Wang, X.; Vitalis, A.; Crick, S. L. A polymer physics perspective on driving forces and mechanisms for protein aggregation Arch. Biochem. Biophys. 2008, 469, 132-141 (Pubitemid 350212851)
69. Morris, A. M.; Watzky, M. A.; Finke, R. G. Protein aggregation kinetics, mechanism and curve-fitting: A review of the literature Biochim. Biophys. Acta 2009, 1794, 375-397
70. Uratani, Y.; Asakura, S.; Imahori, K. A circular dichroism study of Salmonella flagellin: Evidence for conformational change on polymerization J. Mol. Biol. 1972, 67, 85-98
71. Prusiner, S. B. Novel proteinaceous infectious particles cause scrapie Science 1982, 216, 136-144 (Pubitemid 12089840)
72. Beaven, G. H.; Gratzer, W. B.; Davies, H. G. Formation and structure of gels and fibrils from glucagon Eur. J. Biochem. 1969, 11, 37-42
73. Hofrichter, J.; Ross, P. D.; Eaton, W. A. Kinetics and mechanism of deoxyhemoglobin S gelation: A new approach to understanding sickle cell disease Proc. Natl. Acad. Sci. U.S.A. 1974, 71, 4864-4868
74. Jarrett, J. T.; Lansbury, P. T., Jr. Seeding one-dimensional crystallization of amyloid: A pathogenic mechanism in Alzheimerb s disease and scrapie Cell 1993, 73, 1055-1058 (Pubitemid 23180480)
75. Serio, T. R.; Cashikar, A. G.; Kowal, A. S.; Sawicki, G. J.; Moslehi, J. J.; Serpell, L.; Arnsdorf, M. F.; Lindquist, S. L. Nucleated conformational conversion and the replication of conformational information by a prion determinant Science 2000, 289, 1317-1321 (Pubitemid 30656041)