Solvation and Desolvation Dynamics in Apomyoglobin Folding Monitored by Time-resolved Infrared Spectroscopy

Journal of Molecular Biology

Volumn 373, Issue 2, 2007, Pages 491-502

  Nishiguchi, Shingo ^a   Goto, Yuji ^a   Takahashi, Satoshi ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

apomyoglobin; protein folding; rapid mixing; solvation; time resolved infrared spectroscopy

Indexed keywords

EID: 34548849769     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.08.003     Document Type: Article

References (78)

1. Rose G.D. Editor of Unfolded Proteins. Advances in Protein Chemistr. vol. 62 (2002), Academic, San Diego
2. Chothia C. Structural invariants in protein folding. Nature 254 (1975) 304-308
3. Fersht A. Structure and Mechanism in Protein Science (1998), W. H. Freeman and Company, New York
4. Finkelstein A.V., and Ptitsyn O.B. Protein Physics (2002), Academic Press, London
5. Levy Y., and Onuchic J.N. Water mediation in protein folding and molecular recognition. Annu. Rev. Biophys. Biomol. Struct. 35 (2006) 389-415
6. Kohn J.E., Millett I.S., Jacob J., Zagrovic B., Dillon T., Cingel N., et al. Random-coil behavior and the dimensions of chemically unfolded proteins. Proc. Natl Acad. Sci. USA 101 (2004) 12491-12496
7. Flory P.J. Principles in Polymer Chemistry (1953), Cornel Univ. Press, Ithaca, NY
8. Akiyama S., Takahashi S., Kimura T., Ishimori K., Morishima I., Nishikawa Y., and Fujisawa T. Conformational landscape of cytochrome c folding studied by microsecond-resolved small-angle X-ray scattering. Proc. Natl Acad. Sci. USA 99 (2002) 1329-1334
9. Uzawa T., Akiyama S., Kimura T., Takahashi S., Ishimori K., Morishima I., and Fujisawa T. Collapse and search dynamics of apomyoglobin folding revealed by submillisecond observations of α-helical content and compactness. Proc. Natl Acad. Sci. USA 101 (2004) 1171-1176
10. Kimura T., Uzawa T., Ishimori K., Morishima I., Takahashi S., Konno T., et al. Specific collapse followed by slow hydrogen-bond formation of beta-sheet in the folding of single-chain monellin. Proc. Natl Acad. Sci. USA 102 (2005) 2748-2753
11. Uzawa T., Kimura T., Ishimori K., Morishima I., Matsui T., Ikeda-Saito M., et al. Time-resolved small-angle X-ray scattering investigation of the folding dynamics of heme oxygenase: implication of the scaling relationship for the submillisecond intermediates of protein folding. J. Mol. Biol. 357 (2006) 997-1008
12. Luo P., and Baldwin R.L. Interaction between water and polar groups of the helix backbone: an important determinant of helix propensities. Proc. Natl Acad. Sci. USA 96 (1999) 4930-4935
13. Albelj F., and Baldwin R.L. Role of backbone solvation in determining thermodynamic β propensities of the amino acids. Proc. Natl Acad. Sci. USA 99 (2002) 1309-1313
14. Walkenhorst W.F., Edwards J.A., Markley J.L., and Roder H. Early formation of a beta hairpin during folding of staphylococcal nuclease H124L as detected by pulsed hydrogen exchange. Protein Sci. 11 (2002) 82-91
15. Sauder J.M., and Roder H. Amide protection in an early folding intermediate of cytochrome c. Fold. Des. 3 (1998) 293-301
16. Krishna M.M.G., Hoang L., Lin Y., and Englander S.W. Hydrogen exchange methods to study protein folding. Methods 34 (2004) 51-64
17. Hummer G., Garde S., Garcia A.E., Pohorille A., and Pratt L.R. An information theory model of hydrophobic interactions. Proc. Natl Acad. Sci. USA 93 (1996) 8951-8955
18. Hummer G., Garde S., Garcia A.E., Paulaitis M.E., and Pratt L.R. The pressure dependence of hydrophobic interactions is consistent with the observed pressure denaturation of proteins. Proc. Natl Acad. Sci. USA 95 (1998) 1552-1555
19. Cheung M.S., Garcia A.E., and Onuchic J.N. Protein folding mediated by solvation: water expulsion and formation of the hydrophobic core occur after the structural collapse. Proc. Natl Acad. Sci. USA 99 (2002) 685-690
20. Fernandez-Escamilla A.M., Cheung M.S., Vega M.C., Wilmanns M., Onuchic J.N., and Serrano L. Solvation in protein folding analysis: combination of theoretical and experimental approaches. Proc. Natl Acad. Sci. USA 101 (2004) 2834-2839
21. Papoian G.A., Ulander J., Eastwood M.P., Luthey-Schulten Z., and Wolynes P.G. Water in protein structure prediction. Proc. Natl Acad. Sci. USA 101 (2004) 3352-3357
22. Kataoka M., Nishii I., Fujisawa T., Ueki T., Tokunaga F., and Goto Y. Structural characterization of the molten globule and native states of apomyoglobin by solution X-ray scattering. J. Mol. Biol. 249 (1995) 215-228
23. Eliezer D., and Wright P.E. Is apomyoglobin a molten globule? Structural characterization by NMR. J. Mol. Biol. 263 (1996) 531-538
24. Yao J., Chung J., Eliezer D., Wright P.E., and Dyson H.J. NMR structural and dynamic characterization of the acid-unfolded state of apomyoglobin provides insights into the early events in protein folding. Biochemistry 40 (2001) 3561-3571
25. Mohana-Borges R., Goto N.K., Kroon G.J.A., Dyson H.J., and Wright P.E. Structural characterization of unfolded states of apomyoglobin using residual dipolar couplings. J. Mol. Biol. 340 (2004) 1131-1142
26. Hughson F.M., Wright P.E., and Baldwin R.L. Structural characterization of a partly folded apomyoglobin intermediate. Science 249 (1990) 1544-1548
27. Eliezer D., Yao J., Dyson H.J., and Wright P.E. Structural and dynamic characterization of partially folded states of apomyoglobin and implications for protein folding. Nature Struct. Biol. 5 (1998) 148-155
28. Kay M.S., and Baldwin R.L. Packing interactions in the apomyoglobin folding intermediate. Nature Struct. Biol. 3 (1996) 439-445
29. Kay M.S., Ramos C.H.I., and Baldwin R.L. Specificity of native-like interhelical hydrophobic contacts in the apomyoglobin intermediate. Proc. Natl Acad. Sci. USA 96 (1999) 2007-2012
30. Bertagna A.M., and Barrick D. Nonspecific hydrophobic interactions stabilize an equilibrium intermediate of apomyoglobin at a key position within the AGH region. Proc. Natl Acad. Sci. USA 101 (2004) 12514-12519
31. Jennings P.A., and Wright P.E. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 262 (1993) 892-896
32. Kimura T., Takahashi S., Akiyama S., Uzawa T., Ishimori K., and Morishima I. Direct observation of the multistep helix formation of poly-L-glutamic acids. J. Am. Chem. Soc. 124 (2002) 11596-11597
33. Phillips C.M., Mizutani Y., and Hochstrasser R.M. Ultrafast thermally induced unfolding of RNase A. Proc. Natl Acad. Sci. USA 92 (1995) 7292-7296
34. Gilmanshin R., Williams S., Callender R.H., Woodruff W.H., and Dyer R.B. Fast events in protein folding: relaxation dynamics of secondary and tertiary structure in native apomyoglobin. Proc. Natl Acad. Sci. USA 94 (1997) 3709-3713
35. Troullier A., Reinstadler D., Dupont Y., Naumann D., and Forge V. Transient non-native secondary structures during the refolding of α-lactalbumin detected by infrared spectroscopy. Nature Struct. Biol. 7 (2000) 78-86
36. Kauffmann E., Darnton N.C., Austin R.H., Batt C., and Gerwert K. Lifetimes of intermediates in the β-sheet to α-helix transition of β-lactoglobulin by using a diffusional IR mixer. Proc. Natl Acad. Sci. USA 98 (2001) 6646-6649
37. Manas E.S., Getahun Z., Wright W.W., DeGrado W.F., and Vanderkooi J.M. Infrared spectra of amide groups in α-helical proteins: evidence for hydrogen bonding between helices and water. J. Am. Chem. Soc. 122 (2000) 9883-9890
38. Walsh S.T.R., Cheng R.P., Wright W.W., Alonso D.O.V., Daggett V., Vanderkooi J.M., and Degrado W.F. The hydration of amides in helices; a comprehensive picture from molecular dynamics, IR, and NMR. Protein Sci. 12 (2003) 520-531
39. Gnanakaran S., Hochstrasser R.M., and Garcia A.E. Nature of structural inhomogeneities on folding a helix and their influence on spectral measurements. Proc. Natl Acad. Sci. USA 101 (2004) 9229-9234
40. Eliezer D., Jennings P.A., Dyson H.J., and Wright P.E. Populating the equilibrium molten globule state of apomyoglobin under conditions suitable for structural characterization by NMR. FEBS Letters 417 (1997) 92-96
41. Kamatari Y.O., Ohji S., Konno T., Seki Y., Soda K., Kataoka M., and Akasaka K. The compact and expanded denatured conformations of apomyoglobin in the methanol-water solvent. Protein Sci. 8 (1999) 873-882
42. Byler D.M., and Susi H. Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25 (1986) 469-487
43. Surewicz W.K., and Mantsch H.H. New insight into protein secondary structure from resolution-enhanced infrared spectra. Biochim. Biophys. Acta 952 (1988) 115-130
44. Dong A., Huang P., and Caughey W.S. Protein secondary structures in water from second-derivative amide I infrared spectra. Biochemistry 29 (1990) 3303-3308
45. Haris P.I., and Chapman D. The conformational analysis of peptides using Fourier transform IR spectroscopy. Biopolymers 37 (1995) 251-263
46. Fabian H., and Naumann D. Methods to study protein folding by stopped-flow FT-IR. Methods 34 (2004) 28-40
47. Gai F., Du D., and Xu Y. Infrared temperature-jump study of the folding dynamics of alpha-helices and beta-hairpins. Methods Mol. Biol. 350 (2007) 1-20
48. Gilmanshin R., Williams S., Callender R.H., Woodruff W.H., and Dyer R.B. Fast events in protein folding: relaxation dynamics and structure of the I form of apomyoglobin. Biochemistry 36 (1997) 15006-15012
49. Gilmanshin R., Callender R.H., and Dyer R.B. The core of apomyoglobin E-form folds at the diffusion limit. Nature Struct. Biol. 5 (1998) 363-365
50. Krimm S., and Bandekar J. Vibrational spectroscopy and conformation of peptides, polypeptides, and proteins. Adv. Protein Chem. 38 (1986) 181-364
51. Torii H., Tastumi T., and Tasumi M. Effects of hydration on the structure, vibrational wavenumbers, vibrational force field and resonance Raman intensities of N-methylacetamide. J. Raman. Spectrosc. 29 (1998) 537-546
52. Torii H. Vibrational interactions in the amide I subspace of the oligomers and hydration clusters of N-methylacetamide. J. Phys. Chem. ser. A 108 (2004) 7272-7280
53. Torii H., and Tasumi M. Ab initio molecular orbital study of the amide I vibrational interactions between the peptide groups in di- and tripeptides and considerations on the conformation of the extended helix. J. Raman. Spectrosc. 29 (1998) 81-86
54. Torii H., and Tasumi M. Model calculations on the amide-I infrared bands of globular proteins. J. Phys. Chem. 96 (1992) 3379-3387
55. Brauner J.W., Flach C.R., and Mendelsohn R. A quantitative reconstruction of the amide I contour in the IR spectra of globular proteins: from structure to spectrum. J. Am. Chem. Soc. 127 (2005) 100-109
56. Jackson M., and Mantsch H.H. The use and misuse of FTIR spectroscopy in the determination of protein structure. Crit. Rev. Biochem. Mol. Biol. 30 (1995) 95-120
57. Lietzow M.A., Jamin M., Dyson H.J., and Wright P.E. Mapping long-range contacts in a highly unfolded protein. J. Mol. Biol. 322 (2002) 655-662
58. Shweitzer-Stenner R., Eker F., Griebenow K., Cao X., and Nafie L.A. The conformation of tetraalanine in water determined by polarized Raman, FT-IR, and VCD spectroscopy. J. Am. Chem. Soc. 126 (2004) 2768-2776
59. Eker F., Griebenow K., and Shweitzer-Stenner R. Aβ(1-28) fragment of the amyloid peptide predominantly adopts a polyproline II conformation in an acidic solution. Biochemistry 43 (2004) 6893-6898
60. Petty S.A., and Volk M. Fast folding dynamics of an α-helical peptide with bulky side chains. Chem. Phys. Phys. Chem. 6 (2004) 1022-1030
61. Shi Z., Chen K., Liu Z., and Kallenbach N.R. Conformation of the backbone in unfolded proteins. Chem. Rev. 106 (2006) 1877-1897
62. Jamin M., and Baldwin R.L. Two forms of the pH 4 folding intermediate of apomyoglobin. J. Mol. Biol. 276 (1998) 491-504
63. Jamin M., Yeh S.-R., Rousseau D.L., and Baldwin R.L. Sub-millisecond unfolding kinetics of apomyoglobin and its pH 4 intermediate. J. Mol. Biol. 292 (1999) 731-740
64. Weisbuch S., Gerard F., Pasdeloup M., Cappadoro J., Dupont Y., and Jamin M. Cooperative sub-millisecond folding kinetics of apomyoglobin pH 4 intermediate. Biochemistry 44 (2005) 7013-7023
65. Haruta N., and Kitagawa T. Time-resolved UV resonance Raman investigation of protein folding using a rapid mixer: characterization of kinetic folding intermediates of apomyoglobin. Biochemistry 41 (2002) 6595-6604
66. Cavagnero S., Nishimura C., Schwarzinger S., Dyson H.J., and Wright P.E. Conformational and dynamic characterization of the molten globule state of an apomyoglobin mutant with an altered folding pathway. Biochemistry 40 (2001) 14459-14467
67. Kitahara R., Yamada H., Akasaka K., and Wright P.E. High pressure NMR reveals that apomyoglobin is an equilibrium mixture from the native to the unfolded. J. Mol. Biol. 320 (2002) 311-319
68. Feng Z., Ha J.-H., and Loh S.N. Identifying the site of initial tertiary structure disruption during apomyoglobin unfolding. Biochemistry 38 (1999) 14433-14439
69. Ten Wolde P.R., and Chandler D. Drying-induced hydrophobic polymer collapse. Proc. Natl Acad. Sci. USA 99 (2002) 6539-6543
70. Zhou R., Huang X., Margulis C.J., and Berne B.J. Hydrophobic collapse in multidomain protein folding. Science 305 (2004) 1605-1609
71. Liu P., Huang X., Zhou R., and Berne B.J. Observation of a dewetting transition in the collapse of the melittin tetramer. Nature 437 (2005) 159-162
72. Shea J.-E., Onuchic J.N., and Brooks III C.L. Probing the folding free energy landscape of the Src-SH3 protein domain. Proc. Natl Acad. Sci. USA 99 (2002) 16064-16068
73. Makhatadze G.I., and Privalov P.L. Energetics of protein structure. Adv. Protein Chem. 47 (1995) 307-425
74. Liu Z., and Chan H.S. Desolvation is a likely origin of robust enthalpic barriers to protein folding. J. Mol. Biol. 349 (2005) 872-889
75. Teale F.W.J. Cleavage of the heme-protein link by acid methylethylketone. Biochem. Biophys. Acta 35 (1959) 543
76. Tonomura B., Nakatani H., Ohnishi M., Yamaguchi-Ito J., and Hitomi K. Test reactions for a stopped-flow apparatus. Anal. Biochem. 84 (1978) 370-383
77. Peterman B.F. Measurement of the dead time of a fluorescence stopped-flow instrument. Anal. Biochem. 93 (1979) 442-444
78. Madden H.H. Comments on the Savitzky-Golay convolution method for least-squares fit smoothing and differential of digital data. Anal. Chem. 50 (1978) 1383-1386