Diffusive motions control the folding and unfolding kinetics of the apomyoglobin pH 4 molten globule intermediate

Biochemistry

Volumn 46, Issue 14, 2007, Pages 4379-4389

  Ramos, Carlos H I ^a   Weisbuch, Sebastien ^b   Jamin, Marc ^c  

^a LABORATÓRIO NACIONAL DE LUZ SÍNCROTRON   (Brazil)

^b CEA GRENOBLE   (France)

^c EUROPEAN MOLECULAR BIOLOGY LABORATORY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMIMETIC MATERIALS; ENERGY BARRIERS; FLUORESCENCE; REACTION KINETICS; SOLVENTS;

APOMYOGLOBIN; LINEAR FREE ENERGY RELATIONSHIPS; STABILIZING EFFECT; VISCOGENIC COSOLVENTS;

PROTEIN FOLDING;

APOMYOGLOBIN;

ARTICLE; DIFFUSION; FLUORESCENCE; KINETICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN STRUCTURE; SPERM WHALE; STRUCTURE ANALYSIS; VISCOSITY;

ANIMALS; APOPROTEINS; CIRCULAR DICHROISM; DIFFUSION; DOSE-RESPONSE RELATIONSHIP, DRUG; HYDROGEN-ION CONCENTRATION; KINETICS; MOTION; MYOGLOBIN; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SOLVENTS; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY, ULTRAVIOLET; SPERM WHALE; SUCROSE; TEMPERATURE; THERMODYNAMICS; UREA; VISCOSITY;

PHYSETERIDAE;

EID: 34147152785     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi602574x     Document Type: Article

References (93)

1. Bilsel, O., and Matthews, C. R. (2000) Barriers in protein folding reactions, Adv. Protein Chem. 53, 153-207.
2. Karplus, M., and Weaver, D. L. (1976) Protein-folding dynamics, Nature 260, 404-406.
3. Sadqi, M., Lapidus, L. J., and Munoz, V. (2003) How fast is protein hydrophobic collapse?, Proc. Natl. Acad. Sci. U.S.A. 100, 12117-12122.
4. Schwarz, G. (1965) On the kinetics of the helix-coil transition of polypeptides in solution, J. Mol. Biol. 11, 64-77.
5. Hammes, G. G., and Roberts, P. B. (1969) Dynamics of the helixcoil transition in poly-L-ornithine, J. Am. Chem. Soc. 91, 1812-1816.
6. Munoz, V., Thompson, P. A., Hofrichter, J., and Eaton, W. A. (1997) Folding dynamics and mechanism of beta-hairpin formation, Nature 390, 196-199.
7. Hagen, S. J., Carswell, C. W., and Sjolander, E. M. (2001) Rate of intrachain contact formation in an unfolded protein: temperature and denaturant effects, J. Mol. Biol. 305, 1161-1171.
8. Lapidus, L. J., Eaton, W. A., and Hofrichter, J. (2001) Dynamics of intramolecular contact formation in polypeptides: distance dependence of quenching rates in a room-temperature glass, Phys. Rev. Lett. 87, 258101.
9. Buscaglia, M., Kubelka, J., Eaton, W. A., and Hofrichter, J. (2005) Determination of ultrafast protein folding rates from loop formation dynamics, J. Mol. Biol. 347, 657-664.
10. Buscaglia, M., Schuler, B., Lapidus, L. J., Eaton, W. A., and Hofrichter, J. (2003) Kinetics of intramolecular contact formation in a denatured protein, J. Mol. Biol. 332, 9-12.
11. Krieger, F., Fierz, B., Bieri, O., Drewello, M., and Kiefhaber, T. (2003) Dynamics of unfolded polypeptide chains as model for the earliest steps in protein folding, J. Mol. Biol. 332, 265-274.
12. Hagen, S. J., Hofrichter, J., Szabo, A., and Eaton, W. A. (1996) Diffusion-limited contact formation in unfolded cytochrome c: estimating the maximum rate of protein folding, Proc. Natl. Acad. Sci. U.S.A. 93, 11615-11617.
13. Jas, G. S., Eaton, W. A., and Hofrichter, J. (2001) Effects of viscosity on the kinetics of α-helix and β-hairpin formation, J. Phys. Chem. B 105, 261-272.
14. Thompson, P. A., Eaton, W. A., and Hofrichter, J. (1997) Laser temperature jump study of the helix ↔ coil kinetics of an alanine peptide interpreted with a "kinetic zipper" model, Biochemistry 36, 9200-9210.
15. Arai, M., and Kuwajima, K. (2000) Role of the molten globule state in protein folding, Adv. Protein Chem. 53, 209-282.
16. Takahashi, S., Yeh, S. R., Das, T. K., Chan, C. K., Gottfried, D. S., and Rousseau, D. L. (1997) Folding of cytochrome c initiated by submillisecond mixing, Nat. Struct. Biol. 4, 44-50.
17. Shastry, M. C., and Roder, H. (1998) Evidence for barrier-limited protein folding kinetics on the microsecond time scale, Nat. Struct. Biol. 5, 385-392.
18. Uzawa, T., Akiyama, S., Kimura, T., Takahashi, S., Ishimori, K., Morishima, I., and Fujisawa, T. (2004) Collapse and search dynamics of apomyoglobin folding revealed by submillisecond observations of alpha-helical content and compactness, Proc. Natl. Acad. Sci. U.S.A. 101, 1171-1176.
19. Roder, H., Maki, K., and Cheng, H. (2006) Early events in protein folding explored by rapid mixing methods, Chem. Rev. 106, 1836-1861.
20. Jennings, P. A., and Wright, P. E. (1993) Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin, Science 262, 892-896.
21. Chamberlain, A. K., and Marqusee, S. (2000) Comparison of equilibrium and kinetic approaches for determining protein folding mechanisms, Adv. Protein Chem. 53, 283-328.
22. Raschke, T. M., and Marqusee, S. (1997) The kinetic folding intermediate of ribonuclease H resembles the acid molten globule and partially unfolded molecules detected under native conditions, Nat. Struct. Biol. 4, 298-304.
23. Jacob, M., and Schmid, F. X. (1999) Protein folding as a diffusional process, Biochemistry 38, 13773-13779.
24. Kramers, H. A. (1940) Brownian motion in a field of force and the diffusion model of chemical reactions, Physica 7, 284-304.
25. Bhattacharyya, R. P., and Sosnick, T. R. (1999) Viscosity dependence of the folding kinetics of a dimeric and monomelic coiled coil, Biochemistry 38, 2601-2609.
26. Ansati, A., Jones, C. M., Henry, E. R., Hofrichter, J., and Eaton, W. A. (1992) The role of solvent viscosity in the dynamics of protein conformational changes, Science 256, 1796-1798.
27. Kubelka, J., Hofrichter, J., and Eaton, W. A. (2004) The protein folding "speed limit", Curr. Opin. Struct. Biol. 14, 76-88.
28. Pabit, S. A., Roder, H., and Hagen, S. J. (2004) Internal friction controls the speed of protein folding from a compact configuration, Biochemistry 43, 12532-12538.
29. Qiu, L., and Hagen, S. J. (2004) A limiting speed for protein folding at low solvent viscosity, J. Am. Chem. Soc. 126, 3398-3399.
30. Plaxco, K. W., and Baker, D. (1998) Limited internal friction in the rate-limiting step of a two-state protein folding reaction, Proc. Natl. Acad. Sci. U.S.A. 95, 13591-13596.
31. Haas, E., Katchalski-Katzir, E., and Steinberg, I. Z. (1978) Effect of the orientation of donor and acceptor on the probability of energy transfer involving electronic transitions of mixed polarization, Biochemistry 17, 5064-5070.
32. Qiu, L., Pabit, S. A., Roitberg, A. E., and Hagen, S. J. (2002) Smaller and faster: the 20-residue Trp-cage protein folds in 4 μs, J. Am. Chem. Soc. 124, 12952-12953.
33. Klimov, D. K., and Thirumalai, D. (1997) Viscosity dependence of the folding rates of proteins, Phys. Rev. Lett. 79, 317-320.
34. Zagrovic, B., and Pande, V. (2003) Solvent viscosity dependence of the folding rate of a small protein: distributed computing study, J. Comput. Chem. 24, 1432-1436.
35. Goldberg, J. M., and Baldwin, R. L. (1998) Kinetic mechanism of a partial folding reaction. 2. Nature of the transition state, Biochemistry 37, 2556-2563.
36. Waldburger, C. D., Jonsson, T., and Sauer, R. T. (1996) Barriers to protein folding: formation of buried polar interactions is a slow step in acquisition of structure, Proc. Natl. Acad. Sci. U.S.A. 93, 2629-2634.
37. Jacob, M., Geeves, M., Holtermann, G., and Schmid, F. X. (1999) Diffusional barrier crossing in a two-state protein folding reaction, Nat. Struct. Biol. 6, 923-926.
38. Jacob, M., Schindler, T., Balbach, J., and Schmid, F. X. (1997) Diffusion control in an elementary protein folding reaction, Proc. Natl. Acad. Sci. U.S.A. 94, 5622-5627.
39. Matthews, C. R., and Hurle, M. R. (1987) Mutant sequences as probes of protein folding mechanisms, BioEssays 6, 254-257.
40. Chrunyk, B. A., and Matthews, C. R. (1990) Role of diffusion in the folding of the alpha subunit of tryptophan synthase from Escherichia coli, Biochemistry 29, 2149-2154.
41. Teschner, W., Rudolph, R., and Garel, J. R. (1987) Intermediates on the folding pathway of octopine dehydrogenase from Pecten jacobaeus, Biochemistry 26, 2791-2796.
42. Vaucheret, H., Signon, L., Le Bras, G., and Garel, J. R. (1987) Mechanism of renaturation of a large protein, aspartokinase-homoserine dehydrogenase, Biochemistry 26, 2785-2790.
43. Viguera, A. R., and Serrano, L. (1997) Loop length, intramolecular diffusion and protein folding, Nat. Struct. Biol. 4, 939-946.
44. Jamin, M., and Baldwin, R. L. (1998) Two forms of the pH 4 folding intermediate of apomyoglobin, J. Mol. Biol. 276, 491-504.
45. Nishimura, C., Dyson, H. J., and Wright, P. E. (2006) Identification of native and non-native structure in kinetic folding intermediates of apomyoglobin, J. Mol. Biol. 355, 139-156.
46. Tsui, V., Garcia, C., Cavagnero, S., Siuzdak, G., Dyson, H. J., and Wright, P. E. (1999) Quench-flow experiments combined with mass spectrometry show apomyoglobin folds through and obligatory intermediate, Protein Sci. 8, 45-49.
47. Hughson, F. M., Wright, P. E., and Baldwin, R. L. (1990) Structural characterization of a partly folded apomyoglobin intermediate, Science 249, 1544-1548.
48. Barrick, D., and Baldwin, R. L. (1993) Three-state analysis of sperm whale apomyoglobin folding, Biochemistry 32, 3790-3796.
49. Griko, Y. V., Privalov, P. L., Venyaminov, S. Y., and Kutyshenko, V. P. (1988) Thermodynamic study of the apomyoglobin structure, J. Mol. Biol. 202, 127-138.
50. Eliezer, D., Chung, J., Dyson, H. J., and Wright, P. E. (2000) Native and non-native secondary structure and dynamics in the pH 4 intermediate of apomyoglobin, Biochemistry 39, 2894-2901.
51. Kataoka, M., Nishii, I., Fujisawa, T., Ueki, T., Tokunaga, F., and Goto, Y. (1995) Structural characterization of the molten globule and native states of apomyoglobin by solution X-ray scattering, J. Mol. Biol. 249, 215-228.
52. Bertagna, A. M., and Barrick, D. (2004) Nonspecific hydrophobic interactions stabilize an equilibrium intermediate of apomyoglobin at a key position within the AGH region, Proc. Natl. Acad. Sci. U.S.A. 101, 12514-12519.
53. Kay, M. S., Ramos, C. H., and Baldwin, R. L. (1999) Specificity of native-like interhelical hydrophobic contacts in the apomyoglobin intermediate, Proc. Natl. Acad. Sci. U.S.A. 96, 2007-2012.
54. Eliezer, D., Yao, J., Dyson, H. J., and Wright, P. E. (1998) Structural and dynamic characterization of partially folded states of apomyoglobin and implications for protein folding, Nat. Struct. Biol. 5, 148-155.
55. Nishimura, C., Dyson, H. J., and Wright, P. E. (2005) Enhanced picture of protein-folding intermediates using organic solvents in H/D exchange and quench-flow experiments, Proc. Natl. Acad. Sci. U.S.A. 102, 4765-4770.
56. Nishimura, C., Dyson, H. J., and Wright, P. E. (2002) The apomyoglobin folding pathway revisited: structural heterogeneity in the kinetic burst phase intermediate, J. Mol. Biol. 322, 483-489.
57. Jamin, M., and Baldwin, R. L. (1996) Refolding and unfolding kinetics of the equilibrium folding intermediate of apomyoglobin, Nat. Struct. Biol. 3, 613-618.
58. Jamin, M., Yeh, S. R., Rousseau, D. L., and Baldwin, R. L. (1999) Submillisecond unfolding kinetics of apomyoglobin and its pH 4 intermediate, J. Mol. Biol. 292, 731-740.
59. Weisbuch, S., Gerard, F., Pasdeloup, M., Cappadoro, J., Dupont, Y., and Jamin, M. (2005) Cooperative sub-millisecond folding kinetics of apomyoglobin pH 4 intermediate, Biochemistry 44, 7013-7023.
60. Timasheff, S. N. (1993) The control of protein stability and association by weak interactions with water: how do solvents affect these processes?, Annu. Rev. Biophys. Biomol. Struct. 22, 67-97.
61. Edelhoch, H. (1967) Spectroscopic determination of tryptophan and tyrosine in proteins, Biochemistry 6, 1948-1954.
62. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single quantum NMR spectroscopy of aqueous solutions, J. Biomol. NMR 2, 661-665.
63. Hwang, T.-L., and Shaka, A. J. (1995) Water suppression that works. Excitation sculpting using arbitrary waveforms and pulsed field gradients, J. Magn. Reson. A112, 275-279.
64. Peterman, B. F. (1979) Measurement of the dead time of a fluorescence stopped-flow instrument, Anal. Biochem. 93, 442-444.
65. Tanford, C. (1970) Protein denaturation. C. Theoretical models for the mechanism of denaturation, Adv. Protein Chem. 24, 1-95.
66. Perl, D., Jacob, M., Bano, M., Stupak, M., Antalik, M., and Schmid, F. X. (2002) Thermodynamics of a diffusional protein folding reaction, Biophys. Chem. 96, 173-190.
67. Sober, H. A. (1970) Handbook of Biochemistry, 2nd ed., Chemical Rubber Co., Cleveland, OH.
68. Weast, R. C. (1989) Handbook of Chemistry and Physics, 69 ed., CRC Press, Cleveland, OH.
69. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants, Biochemistry 27, 8063-8068.
70. Gilmanshin, R., Williams, S., Callender, R. H., Woodruff, W. H., and Dyer, R. B. (1997) Fast events in protein folding: relaxation dynamics and structure of the I form of apomyoglobin, Biochemistry 36, 15006-15012.
71. Ladurner, A. G., and Fersht, A. R. (1999) Upper limit of the time scale for diffusion and chain collapse in chymotrypsin inhibitor 2, Nat. Struct. Biol. 6, 28-31.
72. Srinivasan, R., and Rose, G. D. (1995) LINUS: a hierarchic procedure to predict the fold of a protein, Proteins 22, 81-99.
73. Reymond, M. T., Merutka, G., Dyson, H. J., and Wright, P. E. (1997) Folding propensities of peptide fragments of myoglobin, Protein Sci. 6, 706-716.
74. Pappu, R. V., and Weaver, D. L. (1998) The early folding kinetics of apomyoglobin, Protein Sci. 7, 480-490.
75. Bashford, D., Weaver, D. L., and Karplus, M. (1984) Diffusion-collision model for the folding kinetics of the lambda-repressor operator-binding domain, J. Biomol. Struct. Dyn. 1, 1243-1255.
76. Wolynes, P., Luthey-Schulten, Z., and Onuchic, J. (1996) Fastfolding experiments and the topography of protein folding energy landscapes, Chem. Biol. 3, 425-432.
77. Frauenfelder, H., Fenimore, P. W., Chen, G., and McMahon, B. H. (2006) Protein folding is slaved to solvent motions, Proc. Natl. Acad. Sci. U.S.A. 103, 15469-15472.
78. Kay, M. S., and Baldwin, R. L. (1996) Packing interactions in the apomyglobin folding intermediate, Nat. Struct. Biol. 3, 439-445.
79. Moglich, A., Joder, K., and Kiefhaber, T. (2006) End-to-end distance distributions and intrachain diffusion constants in unfolded polypeptide chains indicate intramolecular hydrogen bond formation, Proc. Natl. Acad. Sci. U.S.A. 103, 12394-12399.
80. Williams, S., Causgrove, T. P., Gilmanshin, R., Fang, K. S., Callender, R. H., Woodruff, W. H., and Dyer, R. B. (1996) Fast events in protein folding: helix melting and formation in a small peptide, Biochemistry 35, 691-697.
81. Eaton, W. A., Munoz, V., Hagen, S. J., Jas, G. S., Lapidus, L. J., Henry, E. R., and Hofrichter, J. (2000) Fast kinetics and mechanisms in protein folding, Annu. Rev. Biophys. Biomol. Struct. 29, 327-359.
82. Luo, Y., Kay, M. S., and Baldwin, R. L. (1997) Cooperativity of folding of the apomyoglobin pH 4 intermediate studied by glycine and proline mutations, Nat. Struct. Biol. 4, 925-930.
83. Maskill, H. (1985) The Physical Basis of Organic Chemistry, Oxford University Press, Oxford.
84. Fersht, A. R. (2004) Relationship of Leffler (Bronsted) alpha values and protein folding Phi values to position of transition-state structures on reaction coordinates, Proc. Natl. Acad. Sci. U.S.A. 101, 14338-14342.
85. Bolen, D. W., and Baskakov, I. V. (2001) The osmophobic effect: natural selection of a thermodynamic force in protein folding, J. Mol. Biol. 310, 955-963.
86. Auton, M., Ferreon, A. C., and Bolen, D. W. (2006) Metrics that differentiate the origins of osmolyte effects on protein stability: a test of the surface tension proposal, J. Mol. Biol. 361, 983-992.
87. Street, T. O., Bolen, D. W., and Rose, G. D. (2006) A molecular mechanism for osmolyte-induced protein stability, Proc. Natl. Acad. Sci. U.S.A. 103, 13997-14002.
88. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding, Protein Sci. 4, 2138-2148.
89. Prabhu, N. P., and Bhuyan, A. K. (2006) Prediction of folding rates of small proteins: empirical relations based on length, secondary structure content, residue type, and stability, Biochemistry 45, 3805-3812.
90. Schindler, T., and Schmid, F. X. (1996) Thermodynamic properties of an extremely rapid protein folding reaction, Biochemistry 35, 16833-16842.
91. Segawa, S., and Sugihara, M. (1984) Characterization of the transition state of lysozyme unfolding. I. Effect of protein-solvent interactions on the transition state, Biopolymers 23, 2473-2488.
92. Kiefhaber, T., Labhardt, A. M., and Baldwin, R. L. (1995) Direct NMR evidence for an intermediate preceding the rate-limiting step in the unfolding of ribonuclease A, Nature 375, 513-515.
93. Finkelstein, A. V., and Shakhnovich, E. I. (1989) Theory of cooperative transitions in protein molecules. II. Phase diagram for a protein molecule in solution, Biopolymers 28, 1681-1694.