Characterization of the Heterogeneity and Specificity of Interpolypeptide Interactions in Amyloid Protofibrils by Measurement of Site-Specific Fluorescence Anisotropy Decay Kinetics

Journal of Molecular Biology

Volumn 393, Issue 3, 2009, Pages 735-752

  Jha, Anjali ^a   Udgaonkar, Jayant B ^b   Krishnamoorthy, G ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

^b TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

amyloid protofibrils; barstar; interpeptide interactions; time resolved fluorescence anisotropy decay; two population anisotropy decay

Indexed keywords

AMYLOID; BARSTAR;

AMINO ACID SEQUENCE; ANISOTROPY; ARTICLE; CHEMICAL LABELING; CONTROLLED STUDY; FLUORESCENCE ANALYSIS; MOLECULAR MECHANICS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN POLYMORPHISM; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

EID: 70350134740     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.08.053     Document Type: Article

References (73)

1. Zerovnik E. Amyloid-fibril formation. Proposed mechanisms and relevance to conformational disease. Eur. J. Biochem. 269 (2002) 3362-3371
2. Cohen F.E., and Kelly J.W. Therapeutic approaches to protein-misfolding diseases. Nature 426 (2003) 905-909
3. Selkoe D.J. Folding proteins in fatal ways. Nature 426 (2003) 900-904
4. Masliah E. Alzheimer's in real time. Nature 451 (2008) 638-639
5. Chiti F., and Dobson C.M. Amyloid formation by globular proteins under native conditions. Nat. Chem. Biol. 5 (2009) 15-22
6. Makin O.S., and Serpell L.C. Structural characterization of islet amyloid polypeptide fibrils. J. Mol. Biol. 335 (2004) 1279-1288
7. 1-42 are potent central nervous system neurotoxins. Proc. Natl Acad. Sci. USA 95 (1998) 6448-6453
8. Bucciantini M., Giannoni E., Chiti F., Baroni F., Formigli L., Zurdo J., et al. Inherent toxicity of aggregates implies a common mechanism for protein misfolding diseases. Nature 416 (2002) 507-511
9. Kayed R., Head E., Thompson J.L., McIntire T.M., Milton S.C., Cotman C.W., and Glabe C.G. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 300 (2003) 486-489
10. Caughey B., and Lansbury P.T. Protofibrils, pores, fibrils, and neurodegeneration: separating the responsible protein aggregates from the innocent bystanders. Annu. Rev. Neurosci. 26 (2003) 267-298
11. Balbirnie M., Grothe R., and Eisenberg D.S. An amyloid-forming peptide from the yeast prion Sup35 reveals a dehydrated β-sheet structure for amyloid. Proc. Natl Acad. Sci. USA 98 (2001) 2375-2380
12. Petkova A.T., Ishii Y., Balbach J.J., Antzutkin O.N., Leapman R.D., Delaglio F., and Tycko R. A structural model for Alzheimer's β-amyloid fibrils based on experimental constraints from solid state NMR. Proc. Natl Acad. Sci. USA 99 (2002) 16742-16747
13. Torok M., Milton S., Kayed R., Wu P., McIntire T., Glabe C.G., and Langen R. Structural and dynamic features of Alzheimer's Aβ peptide in amyloid fibrils studied by site-directed spin labeling. J. Biol. Chem. 277 (2002) 40810-40815
14. Sawaya M.R., Sambashivan S., Nelson R., Ivanova M.I., Sievers S.A., Apostol M.I., et al. Atomic structures of amyloid cross-β spines reveal varied steric zippers. Nature 447 (2007) 453-457
15. Vilar M., Chou H., Luhrs T., Maji S.K., Riek-Loher D., and Verel R. The fold of α-synuclein fibrils. Proc. Natl Acad. Sci. USA 105 (2008) 8637-8642
16. Allsop D., Swanson L., Moore S., Davies Y., York A., El-Agnaf O.M.A., and Soutar I. Fluorescence anisotropy: a method for early detection of Alzheimer β-peptide (Aβ) aggregation. Biochem. Biophys. Res. Commun. 285 (2001) 58-63
17. Padrick S.B., and Miranker A.D. Islet amyloid: phase partitioning and secondary nucleation are central to the mechanism of fibrillogenesis. Biochemistry 41 (2002) 4694-4703
18. Krishnan R., and Lindquist S.L. Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435 (2005) 765-772
19. Koo B.W., and Miranker A.D. Contribution of the intrinsic disulfide to the assembly mechanism of islet amyloid. Protein Sci. 14 (2005) 231-239
20. Mukhopadhyay S., Nayak P.K., Udgaonkar J.B., and Krishnamoorthy G. Characterization of the formation of amyloid protofibrils from barstar by mapping residue-specific fluorescence dynamics. J. Mol. Biol. 358 (2006) 935-942
21. Dobson C.M. Getting out of shape. Nature 418 (2002) 729-730
22. Stefani M., and Dobson C.M. Protein aggregation and aggregate toxicity: new insights into protein folding, misfolding diseases and biological evolution. J. Mol. Med. 81 (2003) 678-699
23. Uversky V.N., and Fink A.L. Conformational constraints for amyloid fibrillation: the importance of being unfolded. Biochim. Biophys. Acta 1698 (2004) 131-153
24. Saxena A.M., Udgaonkar J.B., and Krishnamoorthy G. Characterization of intra-molecular distances and site-specific dynamics in chemically unfolded barstar: evidence for denaturant-dependent non-random structure. J. Mol. Biol. 359 (2006) 174-189
25. Jha S.K., and Udgaonkar J.B. Exploring the cooperativity of the fast folding reaction of a small protein using pulsed thiol labeling and mass spectrometry. J. Biol. Chem. 282 (2007) 37479-37491
26. Pradeep L., and Udgaonkar J.B. Diffusional barrier in the unfolding of a small protein. J. Mol. Biol. 366 (2007) 1016-1028
27. Sinha K.K., and Udgaonkar J.B. Dissecting the non-specific and specific components of the initial folding reaction of barstar by multi-site FRET measurements. J. Mol. Biol. 370 (2007) 385-405
28. 13C assignments of barstar using nuclear magnetic resonance spectroscopy. Biochemistry 33 (1994) 8866-8877
29. Juneja J., Bhavesh N.S., Udgaonkar J.B., and Hosur R.V. NMR identification and characterization of the flexible regions in the 160 kDa molten globule-like aggregate of barstar at low pH. Biochemistry 41 (2002) 9885-9899
30. Swaminathan R., Periasamy N., Udgaonkar J.B., and Krishnamoorthy G. Molten globule-like conformation of barstar: a study by fluorescence dynamics. J. Phys. Chem. 98 (1994) 9270-9278
31. Khurana R., Hate A.T., Nath U., and Udgaonkar J.B. pH dependence of the stability of barstar to chemical and thermal denaturation. Protein Sci. 4 (1995) 1133-1144
32. Kumar S., Mohanty S.K., and 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. 367 (2007) 1186-1204
33. Gast K., Modler A.J., Damaschun H., Krober R., Lutsch G., Zirwer D., et al. Effect of environmental conditions on aggregation and fibril formation of barstar. Eur. Biophys. J. 32 (2003) 710-723
34. Kumar S., and Udgaonkar J.B. Conformational conversion may precede or follow aggregate elongation on alternative pathways of amyloid protofibril formation. J. Mol. Biol. 385 (2009) 1266-1276
35. Jha A., Udgaonkar J.B., and Krishnamoorthy G. Towards elucidating the internal structure of protein protofibrils: site-specific fluorescence anisotropy decay kinetics. Proceedings of Trombay Symposium on Radiation and Photochemistry-2008 (TSRP), Pune, India (2008) 307-308
36. Goldsbury C., Kistler J., Aebi U., Arvinte T., and Cooper G.J. Watching amyloid fibrils grow by time-lapse atomic force microscopy. J. Mol. Biol. 285 (1999) 33-39
37. Bauer H., Aebi U., Haener M., Hermann R., Mueller M., Arvinte T., and Merkle H.P. Architecture and polymorphism of fibrillar supramolecular assemblies produced by in vitro aggregation of human calcitonin. J. Struct. Biol. 115 (1995) 1-15
38. Goldsbury C.S., Cooper G.J.S., Goldie K.N., Muller S.A., Engel A., Aebi U., and Kistler J. Polymorphic fibrillar assembly of human amylin. J. Struct. Biol. 119 (1997) 17-27
39. Thirunavukkuarasu S., Jares-Erijman E.A., and Jovin T.M. Multiparametric fluorescence detection of early stages in the amyloid protein aggregation of pyrene-labeled α-synuclein. J. Mol. Biol. 378 (2008) 1064-1073
40. Carver Jr. T.E., Hochstrasser R.A., and Millar D.P. Proofreading DNA: recognition of aberrant DNA termini by the Klenow fragment of DNA polymerase I. Proc. Natl Acad. Sci. USA 91 (1994) 10670-10674
41. Srivastava A., and Krishnamoorthy G. Cell type and spatial location dependence of cytoplasmic viscosity measured by time-resolved fluorescence microscopy. Arch. Biochem. Biophys. 340 (1997) 159-167
42. Lakowicz J.R. Principles of Fluorescence Spectroscopy. 3rd edit. (2006), Kluwer Academic/Plenum Publishers, New York, NY
43. Bailey M.F., Thompson E.H., and Millar D.P. Probing DNA polymerase fidelity mechanisms using time-resolved fluorescence anisotropy. Methods 25 (2001) 62-77
44. Rami B.R., Krishnamoorthy G., and Udgaonkar J.B. Dynamics of the core tryptophan during the formation of a productive molten globule intermediate of barstar. Biochemistry 42 (2003) 7986-8000
45. Ludescher R.D., Peting L., Hudson S., and Hudson B. Time-resolved fluorescence anisotropy for systems with lifetime and dynamic heterogeneity. Biophys. Chem. 28 (1987) 59-75
46. Diaz-Avalos R., Long C., Fontano E., Balbirnie M., Grothe R., Eisenberg D., and Caspar D.L. Cross-β order and diversity in nanocrystals of an amyloid-forming peptide. J. Mol. Biol. 330 (2003) 1165-1175
47. Makin O.S., Atkins E., Sikorski P., Johansson J., and Serpell L.C. Molecular basis for amyloid fibril formation and stability. Proc. Natl Acad. Sci. USA 102 (2005) 315-320
48. 2-microglobulin fragment probed by solid-state NMR. Proc. Natl Acad. Sci. USA 103 (2006) 18119-18124
49. Tycko R. Solid-state NMR as a probe of amyloid structure. Protein Pept. Lett. 13 (2006) 229-234
50. Chen M., Margittai M., Chen J., and Langen R. Investigation of α-synuclein fibril structure by site-directed spin labeling. J. Biol. Chem. 282 (2007) 24970-24979
51. Van der Wel P.C.A., Lewandowski J.R., and Griffin R.G. Solid-state NMR study of amyloid nanocrystals and fibrils formed by the peptide GNNQQNY from yeast prion protein Sup35p. J. Am. Chem. Soc. 129 (2007) 5117-5130
52. Harper J.D., Wong S.S., Lieber C.M., and Lansbury Jr. P.T. Assembly of Aβ amyloid protofibrils: an in vitro model for a possible early event in Alzheimer's disease. Biochemistry 38 (1999) 8972-8980
53. Conway K.A., Lee S.J., Rochet J.C., Ding T.T., Williamson R.E., and Lansbury Jr. P.T. Acceleration of oligomerization, not fibrillization, is a shared property of both α-synuclein mutations linked to early-onset Parkinson's disease: implications for pathogenesis and therapy. Proc. Natl Acad. Sci. USA 97 (2000) 571-576
54. Fowler W.E., Hantgan R.R., Hermans J., and Erickson H.P. Structure of the fibrin protofibril. Proc. Natl Acad. Sci. USA 78 (1981) 4872-4876
55. Harper J.D., Lieber C.M., and Lansbury Jr. P.T. Atomic force microscopic imaging of seeded fibril formation and fibril branching by the Alzheimer's disease amyloid-beta protein. Chem. Biol. 4 (1997) 951-959
56. Jarrett J.T., and Lansbury Jr. P.T. Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein OsmB. Biochemistry 31 (1992) 12345-12352
57. Grueninger D., Treiber N., Ziegler M.O., Koetter J.W., Schulze M.S., and Schulz G.E. Designed protein-protein association. Science 319 (2008) 206-209
58. Hasegawa K., Yamaguchi I., Omata S., Gejyo F., and Naiki H. Interaction between Aβ(1-42) and Aβ(1-40) in Alzheimer's β-amyloid fibril formation in vitro. Biochemistry 38 (1999) 15514-15521
59. Nelson R., Sawaya M.R., Balbirnie M., Madsen A.Ø., Riekel C., Grothe R., and Eisenberg D. Structure of the cross-β spine of amyloid-like fibrils. Nature 435 (2005) 773-778
60. Chothia C. Structural invariants in protein folding. Nature 254 (1975) 304-308
61. Richards F.M. Areas, volumes, packing and protein structure. Annu. Rev. Biophys. Bioeng. 6 (1977) 151-176
62. Lim W.A., and Sauer R.T. Alternative packing arrangements in the hydrophobic core of lambda repressor. Nature 339 (1989) 31-36
63. Eriksson A.E., Baase W.A., Zhang X.J., Heinz D.W., Blaber M., Baldwin E.P., and Matthews B.W. Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect. Science 255 (1992) 178-183
64. Lee B. Estimation of the maximum change in stability of globular proteins upon mutation of a hydrophobic residue to another of smaller size. Protein Sci. 2 (1993) 733-738
65. Jimenez J.L., Guijarro J.I., Orlova E., Zurdo J., Dobson C.M., Sunde M., and Saibil H.R. Cryo-electron microscopy structure of an SH3 amyloid fibril and model of the molecular packing. EMBO J. 18 (1999) 815-821
66. Kheterpal I., Williams A., Murphy C., Bledsoe B., and Wetzel R. Structural features of the Aβ amyloid fibril elucidated by limited proteolysis. Biochemistry 40 (2001) 11757-11767
67. Jimenez J.L., Nettleton E.J., Bouchard M., Robinson C.V., Dobson C.M., and Saibil H.R. The protofilament structure of insulin amyloid fibrils. Proc. Natl Acad. Sci. USA 99 (2002) 9196-9201
68. Miake H., Mizusawa H., Iwatsubo T., and Hasegawa M. Biochemical characterization of the core structure of α-synuclein filaments. J. Biol. Chem. 277 (2002) 19213-19219
69. 2-microglobulin suggests a molecular model for the fibril. Proc. Natl Acad. Sci. USA 101 (2004) 10584-10589
70. Kajava A.V., Baxa U., Wickner R.B., and Steven A.C. A model for Ure2p prion filaments and other amyloids: the parallel superplated β-structure. Proc. Natl Acad. Sci. USA 101 (2004) 7885-7890
71. Tycko R. Progress towards a molecular-level structural understanding of amyloid fibrils. Curr. Opin. Struct. Biol. 14 (2004) 96-103
72. Sackewitz M., Scheidt H.A., Lodderstedt G., Schierhorn A., Schwarz E., and Huster D. Structural and dynamical characterization of fibrils from a disease-associated alanine expansion domain using proteolysis and solid-state NMR spectroscopy. J. Am. Chem. Soc. 130 (2008) 7172-7173
73. Sridevi K., and Udgaonkar J.B. Surface expansion is independent of and occurs faster than core solvation during the unfolding of barstar. Biochemistry 42 (2003) 1551-1563