Effects of the stabilization of the molten globule state on the folding mechanism of α-lactalbumin: A study of a chimera of bovine and human α-lactalbumin

Proteins: Structure, Function and Genetics

Volumn 61, Issue 2, 2005, Pages 356-365

  Mizuguchi, Mineyuki ^a   Matsuura, Atsushi ^a   Nabeshima, Yuko ^a   Masaki, Kazuo ^b   Watanabe, Masahiro ^b   Aizawa, Tomoyasu ^b   Demura, Makoto ^b   Nitta, Katsutoshi ^b   Mori, Yoshihiro ^a   Shinoda, Hiroyuki ^a   Kawano, Keiichi ^a,b  

^a UNIVERSITY OF TOYAMA   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

lactalbumin; Local interaction; Molten globule; Protein folding; Stability

Indexed keywords

ALPHA LACTALBUMIN; TRYPTOPHAN;

ARTICLE; CATTLE; CHIMERA; CIRCULAR DICHROISM; ENERGY; FLUORESCENCE SPECTROSCOPY; HUMAN; HYDROPHOBICITY; KINETICS; MOLECULAR INTERACTION; NONHUMAN; PEPTIDE ANALYSIS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY;

AMINO ACID SEQUENCE; ANILINO NAPHTHALENESULFONATES; ANIMALS; CATTLE; FLUORESCENT DYES; GUANIDINE; HUMANS; HYDROPHOBICITY; KINETICS; LACTALBUMIN; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT FUSION PROTEINS; SPECTROMETRY, FLUORESCENCE;

BOVINAE;

EID: 26444524376     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/prot.20640     Document Type: Article

References (66)

1. Kim PS, Baldwin RL. Interactions in the folding reactions of small proteins. Annu Rev Biochem 1990;59:631-660.
2. Kuwajima K, Hiraoka Y, Ikeguchi M, Sugai S. Comparison of the transient folding intermediates in lysozyme and α-lactalbumin. Biochemistry 1985;24:874-881.
3. Roder H, Elöve GA, Englander SW. Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 1988;335:700-704.
4. Elöve GA, Chaffotte AF, Roder H, Goldberg ME. Early steps in cytochrome c folding probed by time-resolved circular dichroism and fluorescence spectroscopy. Biochemistry 1992;31:6876-6883.
5. Jennings PA, Wright PE. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 1993;262:892-896.
6. Balbach J, Forge V, van Nuland NAJ, Winder SL, Hore PJ, Dobson CM. Following protein folding in real time using NMR spectroscopy. Nat Struct Biol 1995;2:865-870.
7. Colon W, Elöve GA, Wakem LP, Sherman F, Roder H. Side chain packing of the N- and C-terminal helices plays a critical role in the kinetics of cytochrome c folding. Biochemistry 1996;35:5538-5549.
8. Raschke TM, Marqusee S. The kinetic folding intermediate of ribonuclease H resembles the acid molten globule and partially unfolded molecules detected under native conditions. Nat Struct Biol 1997;4:298-304.
9. Mizuguchi M, Arai M, Yue Ke, Nitta K, Kuwajima K. Equilibrium and kinetics of the folding of equine lysozyme studied by circular dichroism spectroscopy. J Mol Biol 1998;283:265-277.
10. Kuwajima K. The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins 1989;6:87-103.
11. Baldwin RL. Pulsed H/D exchange studies of folding intermediates. Curr Opin Struct Biol 1993;3:84-91.
12. Ptitsyn OB. Molten globule and protein folding. Adv Protein Chem 1995;47:83-229.
13. Arai M, Kuwajima K. The role of the molten globule state in protein folding. Adv Protein Chem 2000;53:209-282.
14. Acharya KR, Stuart DI, Walker NPC, Lewis M, Phillips DC. Refined structure of baboon α-lactalbumin at 1.7 Å resolution: comparison with c-type lysozyme. J Mol Biol 1989;208:99-127.
15. Acharya KR, Ren J, Stuart DI, Phillips DC, Fenna RE. Crystal structure of human α-lactalbumin at 1.7 Å resolution. J Mol Biol 1991;221:571-581.
16. Pike ACW, Brew K, Acharya KR. 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 1996;4:691-703.
17. Peng Z-y, Kim PS. A protein dissection study of a molten globule. Biochemistry 1994;33:2136-2141.
18. Schulman BA, Redfield C, Peng Z-y, Dobson CM, Kim PS. Different subdomains are most protected from hydrogen exchange in the molten globule and native states of human α-lactalbumin. J Mol Biol 1995;253:651-657.
19. Wu LC, Peng Z-y, Kim PS. Bipartite structure of the α-lactalbumin molten globule. Nat Struct Biol 1995;2:281-286.
20. Kuwajima K. The molten globule state of α-lactalbumin. FASEB J 1996;10:102-109.
21. Mizuguchi M, Masaki K, Demura M, Nitta K. Local and long-range interactions in the molten globule state: A study of chimeric proteins of bovine and human α-lactalbumin. J Mol Biol 2000;298: 985-995.
22. Uchiyama H, Perez-Prat EM, Watanabe K, Kumagai I, Kuwajima K. Effects of amino acid substitutions in the hydrophobic core of α-lactalbumin on the stability of the molten globule state. Protein Eng 1995;8:1153-1161.
23. Kay MS, Baldwin RL. Packing interactions in the apomyoglobin folding intermediate. Nat Struct Biol 1996;3:439-445.
24. Luo Y, Kay MS, Baldwin RL. Cooperativity of folding of the apomyoglobin pH 4 intermediate studied by glycine and proline mutations. Nat Struct Biol 1997;4:925-930.
25. Masaki K, Masuda R, Takase K, Kawano K, Nitta K. Stability of the molten globule state of a domain-exchanged chimeric protein between human and bovine α-lactalbumin. Protein Eng 2000;13: 1-4.
26. Gill SC, von Hippel PH. Calculation of protein extinction coefficients from amino acid sequence data. Anal Biochem 1989;182: 319-326.
27. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem 1951; 193:265-275.
28. Nozaki Y. The preparation of guanidine hydrochloride. In: Hirs CHW, Timasheff SN, editors. Methods in enzymology. Enzyme structure, part C, Vol 26. New York: Academic Press; 1972. p 43-50.
29. Santoro MM, Bolen DW. Unfolding free energy changes determined by the linear extrapolation method: 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants. Biochemistry 1988;27:8063-8068.
30. Stryer L. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of non-polar binding sites. J Mol Biol 1965;13:482-495.
31. Semisotnov GV, Rodionova NA, Kutyshenko VP, Ebert B, Blanck J, Ptitsyn OB. Sequential mechanism of refolding of carbonic anhydrase B. FEES Lett 1987;224:9-13.
32. Semisotnov GV, Rodionova NA, Razgulyaev OI, Uversky VN, Gripas' AF, Gilmanshin RI. Study of the "molten globule" intermediate state in protein folding by a hydrophobic fluorescent probe. Biopolymers 1991;31:119-128.
33. Arai M, Kuwajima K. Rapid formation of a molten globule intermediate in refolding of α-lactalbumin. Fold Des 1996;1:275-287.
34. Kuwajima K, Nitta K, Yoneyama M, Sugai S. Three-state denaturation of α-lactalbumin by guanidine hydrochloride. J Mol Biol 1976;106:359-373.
35. Pace CN. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol 1986;131: 266-280.
36. Mizuguchi M, Hashimoto D, Sakurai M, Nitta K. Cold denaturation of α-lactalbumin. Proteins 2000;38:407-413.
37. Forge V, Wijesinha RT, Balbach J, Brew K, Robinson CV, Redfield C, Dobson CM. Rapid collapse and slow structural reorganisation during the refolding of bovine α-lactalbumin. J Mol Biol 1999;288: 673-688.
38. 2+ binding on the folding kinetics of α-lactalbumin. J Mol Biol 1989;206:547-561.
39. Ikeguchi M, Kuwajima K, Mitani M, Sugai S. 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 1986;25:6965-6972.
40. Baldwin RL. On-pathway versus off-pathway folding intermediates. Fold Des 1996;1:R1-R8.
41. Saeki K, Arai M, Yoda T, Nakao M, Kuwajima K. Localized nature of the transition-state structure in goat α-lactalbumin folding. J Mol Biol 2004;341:589-604.
42. Baum J, Dobson CM, Evans PA, Hanley C. Characterization of a partly folded protein by NMR methods: studies on the molten globule state of guinea pig α-lactalbumin. Biochemistry 1989;28:7-13.
43. Alexandrescu AT, Evans PA, Pitkeathly M, Baum J, Dobson CM. Structure and dynamics of the acid-denatured molten globule state of α-lactalbumin: a two-dimensional NMR study. Biochemistry 1993;32:1707-1718.
44. Mu&ntidle;oz V, Serrano L. Elucidating the folding problem of helical peptides using empirical parameters. Nat Struct Biol 1994;1:399-409.
45. Demarest SJ, Fairman R, Raleigh DP. Peptide models of local and long-range interactions in the molten globule state of human α-lactalbumin. J Mol Biol 1998;283:279-291.
46. Reiersen H, Rees AR. Trifluoroethanol may form a solvent matrix for assisted hydrophobic interactions between peptide side chains. Protein Eng 2000;13:739-743.
47. Tanford C. Protein denaturation. C. Theoretical models for the mechanism of denaturation. Adv Protein Chem 1970;24:1-95.
48. Oobatake M, Ooi T. Hydration and heat stability effects on protein unfolding. Prog Biophys Mol Biol 1993;59:237-284.
49. Song J, Bai P, Luo L, Peng ZY. Contribution of individual residues to formation of the native-like tertiary topology in the α-lactalbumin molten globule. J Mol Biol 1998;280:167-174.
50. Wu LC, Kim PS. A specific hydrophobic core in the α-lactalbumin molten globule. J Mol Biol 1998;280:175-182.
51. Wijesinha-Bettoni R, Dobson CM, Redfield C. Comparison of the denaturant-induced unfolding of the bovine and human α-lactalbumin molten globules. J Mol Biol 2001;312:261-273.
52. Sweet RM, Eisenberg D. Correlation of sequence hydrophobicities measures similarity in three-dimensional protein structure. J Mol Biol 1983;171:479-488.
53. Matouschek A, Serrano L, Fersht AR. The folding of an enzyme: IV. Structure of an intermediate in the refolding of barnase analysed by a protein engineering procedure. J Mol Biol 1992;224: 819-835.
54. Serrano L, Matouschek A, Fersht AR. The folding of an enzyme: III. Structure and the transition state for unfolding of barnase analysed by a protein engineering procedure. J Mol Biol 1992;224: 805-818.
55. Jackson SE, Fersht AR. Folding of chymotrypsin inhibitor-2. 1. Evidence of a two-state transition. Biochemistry 1991;30:10436-10443.
56. Raschke TM, Kho J, Marqusee S. Confirmation of the hierarchical folding of RNase H: a protein engineering study. Nat Struct Biol 1999;6:825-831.
57. López-Hernández E, Cronet P, Serrano L, Muñoz V. Folding kinetics of Che Y mutants with enhanced native alpha-helix propensities. J Mol Biol 1997;266:610-620.
58. Wu LC, Kim PS. Hydrophobic sequence minimization of the α-lactalbumin molten globule. Proc Natl Acad Sci USA 1997;94: 14314-14319.
59. Privalov PL, Gill SL. Stability of protein structure and hydrophobic interaction. Adv Protein Chem 1988;39:191-234.
60. Minor DL Jr, Kim PS. Context is a major determinant of β-sheet propensity. Nature 1994;371:264-267.
61. Minor DL Jr, Kim PS. Context-dependent secondary structure formation of a designed protein sequence. Nature 1996;380:730-734.
62. Baldwin RL, Rose GD. Is protein folding hierarchic? I. Local structure and peptide folding. Trends Biochem Sci 1999;24:26-33.
63. Baldwin RL, Rose GD. Is protein folding hierarchic? II. Folding intermediates and transition states. Trends Biochem Sci 1999;24: 77-83.
64. Chakraborty S, Peng Z-y. Hierarchical unfolding of the α-lactalbumin molten globule: presence of a compact intermediate without a unique tertiary fold. J Mol Biol 2000;298:1-6.
65. Yoda T, Saito M, Arai M, Horii K, Tsumoto K, Matsushima M, Kumagai I, Kuwajima K. Folding-unfolding of goat α-lactalbumin studied by stopped-flow circular dichroism and molecular dynamics simulations. Proteins 2001;42:49-65.
66. Mizuguchi M, Masaki K, Nitta K. The molten globule state of a chimera of human α-lactalbumin and equine lysozyme. J Mol Biol 1999;292:1137-1148.