Transition state in the folding of α-lactalbumin probed by the 6-120 disulfide bond

Protein Science

Volumn 7, Issue 7, 1998, Pages 1564-1574

  Ikeguchi, Masamichi ^a   Fujino, Motoaki ^b   Kato, Masao ^a   Kuwajima, Kunihiro ^c   Sugai, Shintaro ^a  

^a SOKA UNIVERSITY   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Chain entropy; Folding kinetics; Lysozyme; Molten globule; Stopped flow

Indexed keywords

ALPHA LACTALBUMIN;

ARTICLE; CROSS LINKING; DATA ANALYSIS; DISULFIDE BOND; ENTROPY; GENE MUTATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN STRUCTURE;

EID: 0031822735     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1002/pro.5560070710     Document Type: Article

References (74)

1. Alexandrescu AT, Evans PA, Pitkeathly M, Baum J, Dobson CM. 1993. Structure and dynamics of the acid-denatured molten globule state of α-lactalbumin: A 2-dimensional NMR study. Biochemistry 32:1707-1718.
2. Alonso DOV, Dill KA. 1991. Solvent denaturation and stabilization of globular proteins. Biochemistry 30:5974-5985.
3. Arai M, Kuwajima K. 1996. Rapid formation of a molten globule intermediate in refolding of α-lactalbumin. Folding Design 1:275-287.
4. Balbach J, Forge V, Lau WS, van Nuland NAJ, Brew K, Dobson CM. 1996. Protein folding monitored at individual residues during a two-dimensional NMR experiment. Science 274:1161-1163.
5. Baum J, Dobson CM, Evans PA, Hanley C. 1989. Characterization of a partly folded protein by NMR methods: Studies on the molten globule state of guinea pig α-lactalbumin. Biochemistry 28:7-13.
6. Balbach J, Forge V, van Nuland NAJ, Winder SL, Hore PJ, Dobson CM. 1995. Following protein folding in real time using NMR spectroscopy. Nature Struct Biol 2:865-870.
7. Betz SF. 1993. Disulfide bonds and the stability of globular proteins. Protein Sci 2:1551-1558.
8. Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG. 1995. Funnels, pathways, and the energy landscape of protein folding: A synthesis. Proteins Struct Funct Genet 27:167-195.
9. Chaffotte AF, Guillou Y, Goldberg ME. 1992. Kinetic resolution of peptide bond and side chain far-UV circular dichroism during the folding of hen egg white lysozyme. Biochemistry 31:9694-9702.
10. Chan HS, Dill KA. 1989. Intrachain loops in polymers: Effects of excluded volume. J Chem Phys 90:492-509.
11. Chan HS, Dill KA. 1990. The effects of internal constraints on the configurations of chain molecules. J Chem Phys 92:3118-3135.
12. Chen BL, Baase WA, Nicholson H, Schellman JA. 1992. Folding kinetics of T4 lysozyme and nine mutants at 12 °C. Biochemistry 31:1464-1476.
13. Chyan CL, Wormald C, Dobson CM, Evans PA, Baum J. 1993. Structure and stability of the molten globule state of guinea-pig α-lactalbumin: A hydrogen exchange study. Biochemistry 32:5681-5691.
14. Clarke J, Fersht AR. 1993. Engineered disulfide bonds as probes of the folding pathway of barnase: Increasing the stability of proteins against the rate of denaturation. Biochemistry 32:4322-4329.
15. Creighton TE. 1997. How important is the molten globule for correct protein folding? Trends Biochem Sci 22:6-10.
16. Denton ME, Rothwarf DM, Scheraga HA. 1994. Kinetics of folding of guanidine-denatured hen egg white lysozyme and carboxymethyl(Cys(6),Cys(127))-lysozyme: A stopped-flow absorbance and fluorescence study. Biochemistry 33:11225-11236.
17. Dill KA, Chan HS. 1997. From Levinthal to pathway to funnels. Nature Struct Biol 4:10-19.
18. Ewbank JJ, Creighton TE. 1993a. Pathway of disulfide-coupled unfolding and refolding of bovine α-lactalbumin. Biochemistry 32:3677-3693.
19. Ewbank JJ, Creighton TE. 1993b. Structural characterization of the disulfide folding intermediates of bovine α-lactalbumin. Biochemistry 32:3694-3707.
20. Eyles SJ, Radford SE, Robinson CV, Dobson CM. 1994. Kinetic consequences of the removal of a disulfide bridge on the folding of hen lysozyme. Biochemistry 33:13038-13048.
21. Fersht AR. 1995. Characterizing transition states in protein folding: An essential step in the puzzle. Curr Opin Struct Biol 5:79-84.
22. Fersht AR. 1997. Nucleation mechanisms in protein folding. Curr Opin Struct Biol 7:3-9.
23. Flory PJ. 1956. Theory of elastic mechanisms in fibrous proteins. J Am Chem Soc 78:5222-5235.
24. Gohda S, Shimizu A, Ikeguchi M, Sugai S. 1995. The superreactive disulfide bonds in α-lactalbumin and lysozyme. J Protein Chem 14:731-737.
25. Goto Y, Hamaguchi K. 1982. Unfolding and refolding of the reduced constant fragment of the immunoglobulin light chain. Kinetic role of the intrachain disulfide bond. J Mol Biol 156:911-926.
26. Griko YV, Freire E, Privalov PL. 1994. Energetics of the α-lactalbumin states: A calorimetric and statistical thermodynamic study. Biochemistry 33:1889-1899.
27. Harrison PM, Sternberg MJE. 1994. Analysis and classification of disulfide connectivity in proteins: The entropic effect of cross-linkage. J Mol Biol 244:448-463.
28. Harushima Y, Kuwajima K, Sugai S. 1988. Hydrogen exchange of the tryptophan residues in bovine α-lactalbumin studied by UV spectroscopy. Biopolymers 27:629-644.
29. Hendrix TM, Griko Y, Privalov P. 1996. Energetics of structural domains in α-lactalbumin. Protein Sci 5:923-931.
30. Ikeguchi M, Hoshino N, Hirata T, Shimizu A, Sugai S. 1996. Structure of the two disulfide folding intermediate of bovine α-lactalbumin. Prog Biophys Mol Biol 65S1:58.
31. Ikeguchi M, Kuwajima K, Mitani M, Sugai S. 1986. Evidence for identity between the equilibrium unfolding intermediate and a transient folding intermediate: A comparative study of the folding reactions of α-lactalbumin and lysozyme. Biochemistry 25:6965-6972.
32. Ikeguchi M, Sugai S, Fujino M, Sugawara T, Kuwajima K. 1992. Contribution of the 6-120-disulfide bond of α-lactalbumin to the stabilities of its native and molten globule states. Biochemistry 31:12695-12700.
33. Itzhaki LS, Evans PA, Dobson CM, Radford SE. 1994. Tertiary interactions in the folding pathway of hen lysozyme: Kinetic studies using fluorescent probes. Biochemistry 33:5212-5220.
34. Jacobson H, Stockmayer WH. 1950. Intramolecular reaction in polycondensations. I. The theory of linear systems. J Chem Phys 18:1600-1606.
35. Kalnin NN, Kuwajima K. 1995. Kinetic folding and unfolding of staphylococcal nuclease and its six mutants studied by stopped-flow circular dichroism. Proteins Struct Funct Genet 23:163-176.
36. Kato S, Okamura M, Shimamoto N, Utiyama H. 1980. Spectral evidence for a rapidly formed structural intermediate in the refolding kinetics of hen egg-white lysozyme. Biochemistry 20:1080-1085.
37. Kato S, Shimamoto N, Utiyama H. 1981. Identification and characterization of the direct folding process of hen egg-white lysozyme. Biochemistry 21: 38-43.
38. Kiefhaber T. 1995. Kinetic traps in lysozyme folding. Proc Natl Acad Sci USA 92:9029-9033.
39. Kraulis PJ. 1991. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J Appl Cryst 24:946-950.
40. Kuwajima K. 1989. The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins Struct Funct Genet 6:87-103.
41. Kuwajima K. 1996. The molten globule state of α-lactalbumin. FASEB J 10:102-109.
42. Kuwajima K, Hiraoka Y, Ikeguchi M, Sugai S. 1985. Comparison of the transient folding intermediates in lysozyme and α-lactalbumin. Biochemistry 24:847-881.
43. Kuwajima K, Ikeguchi M, Sugawara T, Hiraoka Y, Sugai S. 1990. Kinetics of disulfide bond reduction in α-lactalbumin by dithiothreitol and molecular basis of superreactivity of the Cys6-Cys120 disulfide bond. Biochemistry 29:8240-8249.
44. 2+ binding on the folding kinetics of α-lactalbumin. J Mol Biol 206:574-561.
45. 41)-ribonuclease A. Biochemistry 23:5504-5512.
46. Lopez-Hernandez E, Serrano L. 1996. Structure of the transition state for folding of the 129 aa protein CheY resembles that of a smaller protein, CI-2. Folding Design 1:43-55.
47. Matagne A, Radford SE, Dobson CM. 1997. Fast and slow tracks in lysozyme folding: Insight into the role of domains in the folding process. J Mol Biol 267:1068-1074.
48. Matouschek A, Fersht AR. 1993. Application of physical organic chemistry to engineered mutants of proteins: Hammond postulate behavior in the transition state of protein folding. Proc Natl Acad Sci USA 90:7814-7818.
49. Milla ME, Brown BM, Waldburger CD, Sauer RT. 1995. P22 arc repressor: Transition state properties inferred from mutational effects on the rates of protein unfolding and refolding. Biochemistry 34:13914-13919.
50. Miranker A, Robinson CV, Radford SE, Aplin RT, Dobson CM. 1993. Detection of transient protein folding populations by mass spectrometry. Science 262:896-900.
51. Motoshima H, Ueda T, Imoto T. 1996. Analysis of the transition state in the unfolding of hen lysozyme by introduction of Gly-Pro and Pro-Gly sequences at the same site. J Biochem 119:1019-1023.
52. Myers JK, Pace CN, Scholtz JM. 1995. Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding. Protein Sci 4:2138-2148.
53. Nozaka M, Kuwajima K, Nitta K, Sugai S. 1978. Detection and characterization of the folding pathway of human α-lactalbumin. Biochemistry 17:3753-3758.
54. 1 with zero, one, and two intact disulfide bonds. J Biol Chem 263:11820-11825.
55. Parker MJ, Spencer J, Clarke AR. 1995. An integrated kinetic analysis of intermediates and transition states in protein folding reactions. J Mol Biol 253:771-786.
56. Pfeil W. 1998. Is the molten globule a third thermodynamic state of protein? The example of alpha-lactalbumin. Proteins Struct Funct Genet 30:43-48.
57. Pike ACW, Brew K, Acharya KR. 1996. Crystal structures of guinea-pig, goat and bovine α-lactalbumin highlight the enhanced conformational flexibility of regions that are significant for its action in lactose synthase. Structure 4:691-703.
58. Poland DC, Scheraga HA. 1965. Statistical mechanics of noncovalent bonds in polyamino acids. VIII. Covalent loops in proteins. Biopolymers 3:379-399.
59. Radford SE, Dobson CM, Evans PA. 1992. The folding of hen lysozyme involves partially structured intermediates and multiple pathways. Nature 358:302-307.
60. Schellman JA. 1955. The stability of hydrogen-bonded peptide structures in aqueous solution. Compt Rend Lab Carlsberg Ser Chim 29:230-259.
61. Schellman JA. 1978. Solvent denaturation. Biopolymers 17:1305-1322.
62. Schulman BA, Kim PS. 1996. Proline scanning mutagenesis of a molten globule reveals non-cooperative formation of a protein's overall topology. Nature Struct Biol 3:682-687.
63. Schulman BA, Kim PS, Dobson CM, Redfield C. 1997. A residue-specific NMR view of the non-cooperative unfolding of a molten globule. Nature Struct Biol 4:630-634.
64. Schulman BA, Redfield C, Peng ZY, Dobson CM, Kim PS. 1995. Different subdomains are most protected from hydrogen exchange in the molten globule and native states of human α-lactalbumin. J Mol Biol 253:651-657.
65. Segawa S, Sugihara M. 1984a. Characterization of the transition state of lysozyme unfolding. I. Effect of protein-solvent interactions on the transition state. Biopolymers 23:2473-2488.
66. Segawa S, Sugihara M. 1984b. Characterization of the transition state of lysozyme unfolding. II. Effects of the intrachain crosslinking and the inhibitor binding on the transition state. Biopolymers 23:2489-2498.
67. 1H NMR. Biochemistry 32:13198-13203.
68. Strausberg S, Alexander P, Wang L, Gallagher T, Gilliland G, Bryan P. 1993. An engineered disulfide cross-link accelerates the refolding rate of calcium-free subtilisin by 850-fold. Biochemistry 32:10371-10377.
69. Tanford C. 1968. Protein denaturation. Adv Protein Chem 23:121-282.
70. Wildegger G, Kiefhaber T. 1997. Three-state model for lysozyme folding: Triangular folding mechanism with an energetically trapped intermediate. J Mol Biol 270:294-304.
71. Wilson G, Hecht L, Barron LD. 1996. The native-like tertiary fold in the molten globule α-lactalbumin appears to be controlled by a continuous phase transition. J Mol Biol 261:341-347.
72. Wu LC, Peng ZY, Kim PS. 1995. Bipartite structure of the α-lactalbumin molten globule. Nature Struct Biol 2:281-286.
73. Wu LC, Schulman BA, Peng ZY, Kim PS. 1996. Disulfide determinants of calcium-induced packing in α-lactalbumin. Biochemistry 35:859-863.
74. Yamasaki K, Ogasahara K, Yutani K, Oobatake M, Kanaya S. 1995. Folding pathway of Escherichia coli ribonuclease HI: A circular dichroism, fluorescence, and NMR study. Biochemistry 34:16552-16562.