The first step of hen egg white lysozyme fibrillation, irreversible partial unfolding, is a two-state transition

Protein Science

Volumn 16, Issue 5, 2007, Pages 815-832

  Xu, Ming ^a   Shashilov, Victor A ^a   Ermolenkov, Vladimir V ^a   Fredriksen, Laura ^a   Zagorevski, Dmitri ^b   Lednev, Igor K ^a  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b Rensselaer Polytechnic Institute   (United States)

Author keywords

Amyloid fibrils; Chemometric analysis; Deep UV resonance Raman spectroscopy; Electrospray ionization mass spectrometry; Two state transition

Indexed keywords

EGG WHITE; LYSOZYME;

ALGORITHM; ANALYTICAL ERROR; ARTICLE; CHEMOMETRIC ANALYSIS; ELECTROSPRAY MASS SPECTROMETRY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME STRUCTURE; FLUORESCENCE SPECTROSCOPY; HEN; IN VITRO STUDY; INCUBATION TIME; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; RAMAN SPECTROMETRY; SENSITIVITY ANALYSIS; SPECTROFLUOROMETRY;

ANIMALS; CHICKENS; FEMALE; KINETICS; MODELS, STATISTICAL; MURAMIDASE; PHASE TRANSITION; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; SPECTROMETRY, FLUORESCENCE; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; SPECTRUM ANALYSIS, RAMAN; TRYPTOPHAN;

EID: 34247579524     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1110/ps.062639307     Document Type: Article

References (108)

1. Adams, S., Higgins, A.M., and Jones, R.A.L. 2002. Surface-mediated folding and misfolding of proteins at lipid/water interfaces. Langmuir 18: 4854-4861.
2. Anfinsen, C.B. 1973. Principles that govern the folding of protein chains. Science 181: 223-230.
3. Arnaudov, L.N. and De Vries, R. 2005. Thermally induced fibrillar aggregation of hen egg white lysozyme. Biophys. J. 88: 515-526.
4. Asher, S.A. 2001. Ultraviolet raman spectrometry. In Handbook of vibrational spectroscopy, pp. 557-571. John Wiley & Sons, New York.
5. Asher, S.A., Ludwig, M., and Johnson, C.R. 1986. UV resonance Raman excitation profiles of the aromatic amino acids. J. Am. Chem. Soc. 108: 3186-3197.
6. Ban, T., Yamaguchi, K., and Goto, Y. 2006. Direct observation of amyloid fibril growth, propagation, and adaptation. Acc. Chem. Res. 39: 663-670.
7. Bellotti, V., Mangione, P., and Merlini, G. 2000. Review: Immunoglobulin light chain amyloidosis - the archetype of structural and pathogenic variability. J. Struct. Biol. 130: 280-289.
8. Blanch, E.W., Morozova-Roche, L.A., Cochran, D.A.E., Doig, A.J., Hecht, L., and Barron, L.D. 2000. Is Polyproline II helix the killer conformation? A Raman optical activity study of the amyloidogenic prefibrillar intermediate of human lysozyme. J. Mol. Biol. 301: 553-563.
9. Bossy-Wetzel, E., Schwarzenbacher, R., and Lipton, S.A. 2004. Molecular pathways to neurodegeneration. Nat. Med. Suppl.: S2-S9.
10. Bucciantini, M., Calloni, G., Chiti, F., Formigli, L., Nosi, D., Dobson, C.M., and Stefani, M. 2004. Prefibrillar amyloid protein aggregates share common features of cytotoxicity. J. Biol. Chem. 279: 31374-31382.
11. Caddy, G.L. and Robinson, C.V. 2006. Insights into amyloid fibril formation from mass spectrometry. Protein Pept. Lett. 13: 255-260.
12. Canet, D., Sunde, M., Last, A.M., Miranker, A., Spencer, A., Robinson, C.V., and Dobson, C.M. 1999. Mechanistic studies of the folding of human lysozyme and the origin of amyloidogenic behavior in its disease-related variants. Biochemistry 38: 6419-6427.
13. Canet, D., Last, A.M., Tito, P., Sunde, M., Spencer, A., Archer, D.B., Redfield, C., Robinson, C.V., and Dobson, C.M. 2002. Local cooperativity in the unfolding of an amyloidogenic variant of human lysozyme. Nat. Struct. Biol. 9: 308-315.
14. Cao, A., Hu, D., and Lai, L. 2004. Formation of amyloid fibrils from fully reduced hen egg white lysozyme. Protein Sci. 13: 319-324.
15. Chamberlain, A.K., Receveur, V., Spencer, A., Redfield, C., and Dobson, C.M. 2001. Characterization of the structure and dynamics of amyloidogenic variants of human lysozyme by NMR spectroscopy. Protein Sci. 10: 2525-2530.
16. Chi, Z. and Asher, S.A. 1998. UV Raman determination of the environment and solvent exposure of Tyr and Trp residues. J. Phys. Chem. B 102: 9595-9602.
17. Chi, Z., Chen, X.G., Holtz, J.S., and Asher, S.A. 1998. UV resonance Raman-selective amide vibrational enhancement: Quantitative methodology for determining protein secondary structure. Biochemistry 37: 2854-2864.
18. Chowdhury, S.K., Katta, V., and Chait, B.T. 1990. Probing conformational changes in proteins by mass spectrometry. J. Am. Chem. Soc. 112: 9012-9013.
19. Craig, T.A., Benson, L.M., Bergen, H.R., Venyaminov, S.Y., Salisbury, J.L., Ryan, Z.C., Thompson, J.R., Sperry, J., Gross, M.L., and Kumar, R. 2006. Metal-binding properties of human centrin-2 determined by microelectrospray ionization mass spectrometry and UV spectroscopy. J. Am. Soc. Mass Spectrom. 17: 1158-1171.
20. Daggett, V. 2006. α-Sheet: The toxic conformer in amyloid diseases? Acc. Chem. Res. 39: 594-602.
21. Dantas, G., Kuhlman, B., Callender, D., Wong, M., and Baker, D. 2003. A large scale test of computational protein design: Folding and stability of nine completely redesigned globular proteins. J. Mol. Biol. 332: 449-460.
22. Demchenko, A.P. 1986. Ultraviolet spectroscopy of proteins. Springer-Verlag, Berlin.
23. Dobo, A. and Kaltashov, I.A. 2001. Detection of multiple protein conformational ensembles in solution via deconvolution of charge-state distributions in ESI MS. Anal. Chem. 73: 4763-4773.
24. Dobson, C.M. 2003. Protein folding and misfolding. Nature 426: 884-890.
25. Dumoulin, M., Canet, D., Last, A.M., Pardon, E., Archer, D.B., Muyldermans, S., Wyns, L., Matagne, A., Robinson, C.V., Redfield, C., et al. 2005. Reduced global cooperativity is a common feature underlying the amyloidogenicity of pathogenic lysozyme mutations. J. Mol. Biol. 346: 773-788.
26. Eisenberg, D., Nelson, R., Sawaya, M.R., Balbirnie, M., Sambashivan, S., Ivanova, M.I., Madsen, A.O., and Riekel, C. 2006. The structural biology of protein aggregation diseases: Fundamental questions and some answers. Acc. Chem. Res. 39: 568-575.
27. Fersht, A.R. and Sato, S. 2004. Φ-Value analysis and the nature of protein-folding transition states. Proc. Natl. Acad. Sci. 101: 7976-7981.
28. Fodor, S.P.A., Copeland, R.A., Grygon, C.A., and Spiro, T.G. 1989. Deep-ultraviolet Raman excitation profiles and vibronic scattering mechanisms of phenylalanine, tyrosine, and tryptophan. J. Am. Chem. Soc. 111: 5509-5518.
29. Frare, E., Polverino de Laureto, P., Zurdo, J., Dobson, C.M., and Fontana, A. 2004. A highly amyloidogenic region of hen lysozyme. J. Mol. Biol. 340: 1153-1165.
30. Furdui, C.M., Lew, E.D., Schlessinger, J., and Anderson, K.S. 2006. Autophosphorylation of FGFR1 kinase is mediated by a sequential and precisely ordered reaction. Mol. Cell 21: 711-717.
31. Glenner, G.G., Linke, R.P., and Pollock, P.S. 1976. Systemic amyloidosis and immunoglobulins. Amyloidosis, Proc. Sigrid Juselius Found. Symp., 5th: 233-246.
32. Goda, S., Takano, K., Yamagata, Y., Nagata, R., Akutsu, H., Maki, S., Namba, K., and Yutani, K. 2000. Amyloid protofilament formation of hen egg lysozyme in highly concentrated ethanol solution. Protein Sci. 9: 369-375.
33. Goers, J., Permyakov, S.E., Permyakov, E.A., Uversky, V.N., and Fink, A.L. 2002. Conformational prerequisites for α-lactalbumin fibrillation. Biochemistry 41: 12546-12551.
34. Grandori, R. 2002. Detecting equilibrium cytochrome c folding intermediates by electrospray ionisation mass spectrometry: Two partially folded forms populate the molten-globule state. Protein Sci. 11: 453-458.
35. Gu, Z., Zhu, X., Ni, S., Su, Z., and Zhou, H.-M. 2004. Conformational changes of lysozyme refolding intermediates and implications for aggregation and renaturation. Int. J. Biochem. Cell Biol. 36: 795-805.
36. Haq, S.K., Rasheedi, S., Sharma, P., Ahmad, B., and Khan, R.H. 2005. Influence of salts and alcohols on the conformation of partially folded intermediate of stem bromelain at low pH. Int. J. Biochem. Cell Biol. 37: 361-374.
37. Hardy, J. and Selkoe, D.J. 2002. The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297: 353-356.
38. Hearn, M.T.W., Quirino, J.P., Whisstock, J., and Terabe, S. 2002. Thermal unfolding of proteins studied by coupled reversed-phase HPLC-electrospray ionization mass spectrometry techniques based on isotope exchange effects. Anal. Chem. 74: 1467-1475.
39. Hirai, M., Arai, S., and Iwase, H. 1999. Complementary analysis of thermal transition multiplicity of hen egg-white lysozyme at low pH using X-ray scattering and scanning calorimetry. J. Phys. Chem. B 103: 549-556.
40. Hoaglund-Hyzer, C.S., Counterman, A.E., and Clemmer, D.E. 1999. Anhydrous protein ions. Chem. Rev. 99: 3037-3079.
41. Hooke, S.D., Eyles, S.J., Miranker, A., Radford, S.E., Robinson, C.V., and Dobson, C.M. 1995. Cooperative elements in protein folding monitored by electrospray ionization mass spectrometry. J. Am. Chem. Soc. 117: 7548-7549.
42. Hoshino, M., Hagihara, Y., Hamada, D., Kataoka, M., and Goto, Y. 1997. Trifluoroethanol-induced conformational transition of hen egg white lysozyme studied by small-angle X-ray scattering. FEBS Lett. 416: 72-76.
43. Ianoul, A., Mikhonin, A., Lednev, I.K., and Asher, S.A. 2002. UV resonance Raman study of the spatial dependence of α-helix unfolding. J. Phys. Chem. A 106: 3621-3624.
44. Jackson, S.E. 1998. How do small single-domain proteins fold? Fold. Des. 3: R81-R91.
45. Jiji, R.D., Balakrishnan, G., Hu, Y., and Spiro, T.G. 2006. Intermediacy of poly(L-proline) II and β-strand conformations in poly(L-lysine) β-sheet formation probed by temperature-jump/UV resonance Raman spectroscopy. Biochemistry 45: 34-41.
46. Johnson, M.L. 2000. Parameter correlations while curve fitting. Methods Enzymol. 321: 424-446.
47. Kaltashov, I.A. and Eyles, S.J. 2005. Mass spectrometry in biophysics: Conformation and dynamics of biomolecules. John Wiley & Sons, New York.
48. Kelly, J.W. 1997. Amyloid fibril formation and protein misassembly: A structural quest for insights into amyloid and prion diseases. Structure 5: 595-600.
49. Kelly, J.W. 1998a. The alternative conformations of amyloidogenic proteins and their multi-step assembly pathways. Curr. Opin. Struct. Biol. 8: 101-106.
50. Kelly, J.W. 1998b. The environmental dependency of protein folding best explains prion and amyloid diseases. Proc. Natl. Acad. Sci. 95: 930-932.
51. Khurana, R., Gillespie, J.R., Talapatra, A., Minert, L.J., Ionescu-Zanetti, C., Millett, I., and Fink, A.L. 2001. Partially folded intermediates as critical precursors of light chain amyloid fibrils and amorphous aggregates. Biochemistry 40: 3525-3535.
52. Kim, J.Y., Kim, K.W., Kwon, H.J., Lee, D.W., and Yoo, J.S. 2002. Probing lysine acetylation with a modification-specific marker ion using high-performance liquid chromatography electrospray-mass spectrometry with collision-induced dissociation. Anal. Chem. 74: 5443-5449.
53. Konermann, L. 2004. Fred Beamish award lecture - Exploring the dynamics of biological systems by mass spectrometry. Can. J. Chem. 82: 1565-1580.
54. Krebs, M.R.H., Wilkins, D.K., Chung, E.W., Pitkeathly, M.C., Chamberlain, A.K., Zurdo, J., Robinson, C.V., and Dobson, C.M. 2000. Formation and seeding of amyloid fibrils from wild-type hen lysozyme and a peptide fragment from the β-domain. J. Mol. Biol. 300: 541-549.
55. Kulkarni, S.K., Ashcroft, A.E., Carey, M., Masselos, D., Robinson, C.V., and Radford, S.E. 1999. A near-native state on the slow refolding pathway of hen lysozyme. Protein Sci. 8: 35-44.
56. Lashuel, H.A., Petre, B.M., Wall, J., Simon, M., Nowak, R.J., Walz, T., and Lansbury Jr., P.T. 2002. α-Synuclein, especially the Parkinson's disease-associated mutants, forms pore-like annular and tubular protofibrils. J. Mol. Biol. 322: 1089-1102.
57. Lednev, I.K., Karnoup, A.S., Sparrow, M.C., and Asher, S.A. 1999. α-Helix peptide folding and unfolding activation barriers: A nanosecond UV resonance Raman study. J. Am. Chem. Soc. 121: 8074-8086.
58. Lednev, I.K., Ermolenkov, V.V., He, W., and Xu, M. 2005. Deep-UV Raman spectrometer tunable between 193 and 205 nm for structural characterization of proteins. Anal. Bioanal. Chem. 381: 431-437.
59. Loo, J.A., Loo, R.R., Udseth, H.R., Edmonds, C.G., and Smith, R.D. 1991. Solvent-induced conformational changes of polypeptides probed by electrospray-ionization mass spectrometry. Rapid Commun. Mass Spectrom. 5: 101-105.
60. Malinowski, E.R. 2002. Factor analysis in chemistry, 3d ed. John Wiley & Sons, New York.
61. Matagne, A., Chung, E.W., Ball, L.J., Radford, S.E., Robinson, C.V., and Dobson, C.M. 1998. The origin of the α-domain intermediate in the folding of hen lysozyme. J. Mol. Biol. 277: 997-1005.
62. Matagne, A., Marc, J., Chung, E.W., Robinson, C.V., Radford, S.E., and Dobson, C.M. 2000. Thermal unfolding of an intermediate is associated with non-Arrhenius kinetics in the folding of hen lysozyme. J. Mol. Biol. 297: 193-210.
63. Matsuda, A., Nagao, H., Nakamura, K.G., and Kondo, K. 2003. Time-resolved Raman spectra of ring-stretching modes of benzene derivatives under laser-driven shock compression at 1 GPa. Chem. Phys. Lett. 372: 911-914.
64. McLaughlin, R.W., De Stigter, J.K., Sikkink, L.A., Baden, E.M., and Ramirez-Alvarado, M. 2006. The effects of sodium sulfate, glycosaminoglycans, and Congo red on the structure, stability, and amyloid formation of an immunoglobulin light-chain protein. Protein Sci. 15: 1710-1722.
65. Michalewicz, Z. 1996. Genetic algorithms + data structures = evolution programs, 3d ed. Springer-Verlag, New York.
66. Miranker, A., Robinson, C.V., Radford, S.E., and Dobson, C.M. 1996. Investigation of protein folding by mass spectroscopy. FASEB J. 10: 93-101.
67. Mirza, U.A. and Chait, B.T. 1997. Do proteins denature during droplet evolution in electrospray ionization? Int. J. Mass Spectrom. Ion Process. 162: 173-181.
68. Mohimen, A., Dobo, A., Hoerner, J.K., and Kaltashov, I.A. 2003. A chemometric approach to detection and characterization of multiple protein conformers in solution using electrospray ionization mass spectrometry. Anal. Chem. 75: 4139-4147.
69. Navea, S., Tauler, R., and Juan, A.D. 2006. Monitoring and modeling of protein processes using mass spectrometry, circular dichroism, and multivariate curve resolution methods. Anal. Chem. 78: 4768-4778.
70. Navea, S., Taulerb, R., and Juan, A.D. 2005. Application of the local regression method interval partial least-squares to the elucidation of protein secondary structure. Anal. Biochem. 336: 231-242.
71. Nelson, R., Sawaya, M.R., Balbirnie, M., Madsen, A.O., Riekel, C., Grothe, R., and Eisenberg, D. 2005. Structure of the cross-β spine of amyloid-like fibrils. Nature 435: 773-778.
72. Nettleton, E.J. and Robinson, C.V. 2000. Probing the nature of amyloidogenic proteins by mass spectrometry. In Mass spectrometry in biology and medicine. (eds. A.L. Burlingame et al.), pp. 53-72. Humana Press, Totowa, NJ.
73. Oliva, F.Y. and Muňoz, V. 2004. A simple thermodynamic test to discriminate between two-state and downhill folding. J. Am. Chem. Soc. 126: 8596-8597.
74. Oomens, J., Polfer, N., Moore, D.T., van der Meer, L., Marshall, A.G., Eyler, J.R., Meijere, G., and von Helden, G. 2005. Charge-state resolved mid-infrared spectroscopy of a gas-phase protein. Phys. Chem. Chem. Phys. 7: 1345-1348.
75. Pan, P. and McLuckey, S.A. 2003. Electrospray ionization of protein mixtures at low pH. Anal. Chem. 75: 1491-1499.
76. Pan, J., Rintala-Dempsey, A.C., Li, Y., Shaw, G.S., and Konermann, L. 2006. Folding kinetics of the S100A11 protein dimer studied by time-resolved electrospray mass spectrometry and pulsed hydrogen-deuterium exchange. Biochemistry 45: 3005-3013.
77. Pepys, M.B., Hawkins, P.N., Booth, D.R., Vigushin, D.M., Tennent, G.A., Soutar, A.K., Totty, N., Nguyen, O., Blake, C.C.F., Terry, C.J., et al. 1993. Human lysozyme gene mutations cause hereditary systemic amyloidosis. Nature 362: 553-557.
78. Pfeil, W. 1981. Thermodynamics of α-lactalbumin unfolding. Biophys. Chem. 13: 181-186.
79. Press, W.H. 2002. Numerical recipes in C++: the art of scientific computing, 2d ed. Cambridge University Press, Cambridge, UK.
80. Privalov, P.L. 1979. Stability of proteins: Small globular proteins. Adv. Protein Chem. 33: 167-241.
81. Privalov, P.L. and Khechinashvili, N.N. 1974. A thermodynamic approach to the problem of stabilization of globular protein structure: A calorimetric study. J. Mol. Biol. 86: 684-685.
82. Raleigh, D.P. and Plaxco, K.W. 2005. The protein folding transition state: What are Φ-values really telling us? Protein Pept. Lett. 12: 117-122.
83. Rencher, A.C. 1998. Multivariate statistical inference and applications. Wiley, New York.
84. Rockwood, A.L., Busman, M., Udseth, H.R., and Smith, R.D. 1991. Thermally induced dissociation of ions from electrospray mass spectrometry. Rapid Commun. Mass Spectrom. 5: 582-585.
85. Rodriguez-Cruz, S.E., Klassen, J.S., and Williams, E.R. 1997. Hydration of gas-phase gramicidin S (M + 2H)2+ ions formed by electrospray: The transition from solution to gas-phase structure. J. Am. Soc. Mass Spectrom. 8: 565-568.
86. Ross, C.A. and Poirier, M.A. 2004. Protein aggregation and neurodegenerative disease. Nat. Med. 10: S10-S17.
87. Ruotolo, B.T. and Robinson, C.V. 2006. Aspects of native proteins are retained in vacuum. Curr. Opin. Chem. Biol. 10: 402-408.
88. Samalikova, M., Matecko, I., Mueller, N., and Grandori, R. 2004. Interpreting conformational effects in protein nano-ESI-MS spectra. Anal. Bioanal. Chem. 378: 1112-1123.
89. Serpell, L.C. 2000. Alzheimer's amyloid fibrils: Structure and assembly. Biochim. Biophys. Acta 1502: 16-30.
90. Shashilov, V.A., Ermolenkov, V.V., and Lednev, I.K. 2006a. Multiple bicyclic diamide-lutetium complexes in solution: Chemometric analysis of deep-UV Raman spectroscopic data. Inorg. Chem. 45: 3606-3612.
91. Shashilov, V.A., Xu, M., Ermolenkov, V.V., and Lednev, I.K. 2006b. Latent variable analysis of Raman spectra for structural characterization of proteins. J. Quant. Spectrosc. Radiat. Transf. 102: 46-61.
92. Shenton, M.J., Herman, H., and Stevens, G.C. 2000. Using spectroscopy with chemometrics to measure polymer molar mass. Polym. Int. 49: 1007-1013.
93. Sunde, M. and Blake, C.C.F. 1998. From the globular to the fibrous state: Protein structure and structural conversion in amyloid formation. Q. Rev. Biophys. 31: 1-39.
94. Surewicz, W.K., Jones, E.M., and Apetri, A.C. 2006. The emerging principles of mammalian prion propagation and transmissibility barriers: Insight from studies in vitro. Acc. Chem. Res. 39: 654-662.
95. Svensson, O., Josefson, M., and Langkilde, F.W. 1999. Reaction monitoring using Raman spectroscopy and chemometrics. Chemometr. Intell. Lab. Syst. 49: 49-66.
96. Tycko, R. 2004. Progress towards a molecular-level structural understanding of amyloid fibrils. Curr. Opin. Struct. Biol. 14: 96-103.
97. Uversky, V.N. and Fink, A.L. 2004. Conformational constraints for amyloid fibrillation: The importance of being unfolded. Biochim. Biophys. Acta 1698: 131-153.
98. Valentine, S.J., Anderson, J.G., Ellington, A.D., and Clemmer, D.E. 1997. Disulfide-intact and -reduced lysozyme in the gas phase: Conformations and pathways of folding and unfolding. J. Phys. Chem. B 101: 3891-3900.
99. Velicelebi, G. and Sturtevant, J.M. 1979. Thermodynamics of the denaturation of lysozyme in alcohol-water mixtures. Biochemistry 18: 1180-1186.
100. Vernaglia, B.A., Huang, J., and Clark, E.D. 2004. Guanidine hydrochloride can induce amyloid fibril formation from hen egg-white lysozyme. Biomacromolecules 5: 1362-1370.
101. Westermark, P., Wernstedt, C., Wilander, E., Hayden, D.W., O'Brien, T.D., and Johnson, K.H. 1987. Amyloid fibrils in human insulinoma and islets of Langerhans of the diabetic cat are derived from a neuropeptide-like protein also present in normal islet cells. Proc. Natl. Acad. Sci. 84: 3881-3885.
102. Wetzel, R. 2002. Ideas of order for amyloid fibril structure. Structure 10: 1031-1036.
103. Wintrode, P.L., Rojsajjakul, T., Vadrevu, R., Matthews, C.R., and Smith, D.L. 2005. An obligatory intermediate controls the folding of the α-subunit of tryptophan synthase, a TIM barrel protein. J. Mol. Biol. 347: 911-919.
104. Wise, B.M., Gallagher, N.B., Bro, R., Shaver, J.M., Windig, W., and Koch, R.S. 2005. PLS_Toolbox 3.5 for use with Matlab. Eigenvector Research Inc., Wenatchee, WA.
105. Xu, M., Ermolenkov, V.V., He, W., Uversky, V.N., Fredriksen, L., and Lednev, I.K. 2005. Lysozyme fibrillation: Deep UV Raman spectroscopic characterization of protein structural transformation. Biopolymers 79: 58-61.
106. Yang, W.Y. and Gruebele, M. 2004. Detection-dependent kinetics as a probe of folding landscape microstructure. J. Am. Chem. Soc. 126: 7758-7759.
107. Yonezawa, Y., Tanaka, S., Kubota, T., Wakabayashi, K., Yutani, K., and Fujiwara, S. 2002. An insight into the pathway of the amyloid fibril formation of hen egg white lysozyme obtained from a small-angle X-ray and neutron scattering study. J. Mol. Biol. 323: 237-251.
108. Ziegler, L.D. and Albrecht, A.C. 1979. Ultraviolet preresonance Raman scattering of benzene derivatives. I. Excitation profiles for fundamentals. J. Chem. Phys. 70: 2634-2643.