Effect of GroEL on the re-folding kinetics of α-lactalbumin

Journal of Molecular Biology

Volumn 258, Issue 5, 1996, Pages 827-838

  Katsumata, Kumiko ^a   Okazaki, Akira ^a   Kuwajima, Kunihiro ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

GroEL; Molten globule state; Protein folding; Stopped flow; lactalbumin

Indexed keywords

ALPHA LACTALBUMIN; CHAPERONIN;

ARTICLE; BINDING AFFINITY; FLUORESCENCE; KINETICS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION;

EID: 0029926871     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1996.0290     Document Type: Article

References (61)

1. Balbach, J., Forge, V., van Nuland, N. A. J., Winder, S. L., Hore, P. J. & Dobson, C. M. (1995). Following protein folding in real time using NMR spectroscopy. Nature Struct. Biol. 2, 865-870.
2. Bochkareva, E. S., Lissin, N. M., Flynn, G. C., Rothman, J. E. & Girshovich, A. S. (1992). Positive cooperativity in the functioning of molecular chaperone GroEL. J. Biol. Chem. 267, 6796-6800.
3. Braig, K., Otwinowski, Z., Hegde, R., Boisvert, D. C., Joachimiak, A., Horwich, A. L. & Sigler, P. B. (1994). The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature, 371, 578-586.
4. Brissette, P., Ballou, D. P. & Massey V. (1989). Determination of the dead time of a stopped-flow fluorometer. Anal. Biochem. 181, 234-238.
5. Buchner, J., Schmidt, M., Fuchs, M., Jaenicke, R., Rudolph, R., Schmid, F. X. & Kiefhaber, T. (1991). GroE facilitates re-folding of citrate synthase by suppressing aggregation. Biochemistry, 30, 1586-1591.
6. Chen, S., Roseman, A. M., Hunter, A. S., Wood, S. P., Burston, S. G., Ranson, N. A., Clarke, A. R. & Salbil, H. R. (1994). Location of a folding protein and shape changes in GroEL-GroES complexes imaged by cryo-electron microscopy. Nature, 371, 261-264.
7. Chyan, C. L., Wormald, C., Dobson, C. M., Evans, P. A. & Baum, J. (1993). Structure and stability of the molten globule state of guinea-pig α-lactalbumin: a hydrogen exchange study Biochemistry, 32, 5681-5691.
8. Corrales, F. J. & Fersht, A. R. (1995). The folding of GroEL-bound barnase as a model for chaperonin-mediated protein folding. Proc. Natl Acad. Sci. USA, 92, 5326-5330.
9. Ellis, R. J. & van der Vies, S. M. (1991). Molecular chaperones. Annu. Rev. Biochem. 60, 321-347.
10. Ewbank, J. J., Creighton, T. E., Hayer-Hartl, M. K. & Hartl, F. U. (1995). What is the molten globule? Nature Struct. Biol. 2, 10.
11. Gatenby A. A. & Ellis, R. J. (1990). Chaperone function: the assembly of ribulose bisphosphate carboxylase-oxygenase. Annu. Rev. Cell Biol. 6, 125-149.
12. Gething, M. J. & Sambrook, J. (1992). Protein folding in the cell. Nature, 355, 33-45.
13. Gill, S. C. & von Hippel P. H. (1989). Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182, 319-326.
14. Gray, T. E. & Fersht, A. R. (1993). Refolding of barnase in the presence of GroE. J. Mol. Biol. 232, 1197-1207.
15. Gray, T. E., Eder, J., Bycroft, M., Day, A. G. & Fersht, A. R. (1993). Refolding of barnase mutants and probarnase in the presence and absence of GroEL. EMBO J. 12, 4145-4150.
16. Hayer-Hartl, M. K. & Hartl, F. U. (1993). A comment on: "The aromatic amino acid content of the bacterial chaperone protein groEL (cpn60): evidence for the presence of a single tryptophan", by N. C. Price, S. M. Kelly, S. Wood & A. auf der Mauer (1991), FEBS Letters, 292, 9-12. FEBS Letters, 320, 83-84.
17. Hayer-Hartl, M. K. & Hartl, F. U. (1993). A comment on: "The aromatic amino acid content of the bacterial chaperone protein groEL (cpn60): evidence for the presence of a single tryptophan", by N. C. Price, S. M. Kelly, S. Wood & A. auf der Mauer (1991), FEBS Letters, 292, 9-12. FEBS Letters, 320, 83-84.
18. Hayer-Hartl, M. K. & Hartl, F. U. (1993). A comment on: "The aromatic amino acid content of the bacterial chaperone protein groEL (cpn60): evidence for the presence of a single tryptophan", by N. C. Price, S. M. Kelly, S. Wood & A. auf der Mauer (1991), FEBS Letters, 292, 9-12. FEBS Letters, 320, 83-84.
19. Hayer-Hartl, M. K., Ewbank, J. J., Creighton, T. E. & Hartl, F. U. (1994). Conformational specificity of the chaperonin GroEL for the compact folding intermediates of α-lactalbumin. EMBO J. 13, 3192-3202.
20. Hendrick, J. P. & Hartl, F. U. (1993). Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 62, 349-384.
21. Hill, R. L. & Brew, K. (1975). Lactose synthetase. Advan. Enzymol. Relat. Areas Mol. Biol. 43, 411-490.
22. Hiraoka, Y. & Sugai, S. (1985). Equilibrium and kinetic study of sodium- and potassium-induced conformational changes of apo-α-lactalbumin. Int. J. Pept. Protein Res. 26, 252-261.
23. Hiraoka, Y., Segawa, T., Kuwajima, K., Sugai, S. & Murai, N. (1980). α-Lactalbumin: a calcium metalloprotein. Biochem. Biophys. Res. Commun. 95, 1098-1104.
24. Höll-Neugebauer, B. & Rudolph, R. (1991). Reconstitution of a heat shock effect in vitro: influence of GroE on the thermal aggregation of α-glucosidase from yeast. Biochemistry, 30, 11609-11614.
25. Horowitz, P M., Hua, S. & Gibbons, D. L. (1995). Hydrophobic surfaces that are hidden in chaperonin Cpn60 can be exposed by formation of assembly-competent monomers or by ionic perturbation of the oligomer. J. Biol. Chem. 270, 1535-1542.
26. Horwich, A. L., Low, K. B., Fenton, W. A., Hirshfield, I. N. & Furtak, K. (1993). Folding in vivo of bacterial cytoplasmic proteins: role of GroEL. Cell, 74, 909-917.
27. 2+-induced alteration in the unfolding behavior of α-lactalbumin. J. Biochem. (Tokyo), 99, 1191-1201.
28. Ikeguchi, M., Kuwajima, K., Mitani, M. & Sugai, S. (1986b). 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.
29. Ito, K. & Akiyama, Y. (1991). In vivo analysis of integration of membrane proteins in Escherichia coli. Mol. Microbiol. 5, 2243-2253.
30. Koren, R. & Hammes, G. G. (1976). A kinetic study of protein-protein interactions. Biochemistry, 15, 1165-1171.
31. Kronman, M. J. (1989). Metal-ion binding and the molecular conformational properties of α-lactalbumin. CRC Crit. Rev. Biochem. Mol. Biol. 24, 565-667.
32. 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.
33. Kuwajima, K. (1992). Protein folding in vitro. Curr. Opin. Biotech. 3, 462-467.
34. Kuwajima, K., Nitta, K. & Sugai, S. (1980). Intramolecular perturbation of tryptophans induced by the protonation of ionizable groups in goat α-lactalbumin. Biochim. Biophys. Acta, 623, 389-401.
35. 2+ binding on the folding kinetics of α-lactalbumin. J. Mol. Biol. 206, 547-561.
36. Laminet, A. A., Ziegelhoffer, T., Georgopoulos, C. & Plückthun, A. (1990). The Escherichia coli heat-shock proteins GroEL and GroES modulate the folding of the β-lactamase precursor. EMBO J. 9, 2315-2319.
37. Landry S. J. & Gierasch, L. M. (1991). The chaperonin GroEL binds a polypeptide in an α-helical conformation. Biochemistry, 30, 7359-7362.
38. Landry, S. J. & Gierasch, L. M. (1994). Polypeptide interactions with molecular chaperones and their relationship to in vivo protein folding. Annu. Rev. Biophys. Biomol. Struct. 23, 645-669.
39. Langer, T., Pfeifer, G., Martin, J., Baumeister, W. & Hartl, F. U. (1992). Chaperonin-mediated protein folding: GroES binds to one end of the GroEL cylinder, which accommodates the protein substrate within its central cavity EMBO J. 11, 4757-4765.
40. Lilie, H. & Buchner, J. (1995). Interaction of GroEL with a highly structured folding intermediate: Iterative binding cycles do not involve unfolding. Proc. Natl Acad. Sci. USA, 92, 8100-8104.
41. Martin, J., Langer, T., Boteva, R., Schramel, A., Horwich, A. L. & Hartl, F. U. (1991). Caperonin-mediated protein folding at the surface of groEL through a 'molten globule'-like intermediate. Nature, 352, 36-42.
42. McKenzie, H. A. & White, F. H., Jr (1991). Lysozyme and α-lactalbumin: structure, function, and interrelationships. Advan. Protein Chem. 41, 173-315.
43. Mendoza, J. A., Rogers, E., Lorimer, G. H. & Horowitz, P. M. (1991). Chaperonins facilitate the in vitro folding of monomeric mitochondrial rhodanese. J. Biol. Chem. 266, 13044-13049.
44. Murai, N., Taguchi, H. & Yoshida, M. (1995). Kinetic analysis of interactions between GroEL and reduced α-lactalbumin. J. Biol. Chem. 270, 19957-19963.
45. Okazaki, A., Ikura, T., Nikaido, K. & Kuwajima, K. (1994). The chaperonin GroEL does not recognize apo-α-lactalbumin in the molten globule state. Nature Struct. Biol. 1, 439-446.
46. Okazaki, A., Ikura, T. & Kuwajima, K. (1995). What is the molten globule? Reply Nature Struct. Biol. 2, 10-11.
47. Permyakov, E. A., Morozova, L. A. & Burstein, E. A. (1985). Cation binding effects on the pH, thermal and urea denaturation transition in α-lactalbumin. Biophys. Chem. 21, 21-31.
48. Press, W. H., Flannery B. P., Teuklosky, S. A. & Vetteling, W. T. (1986). Numerical Recipes, Cambridge University Press, New York.
49. Ptitsyn, O. B. (1992). The molten globule state. In Protein folding (Creighton, T. E., ed.), pp. 243-300, W. H. Freeman and Company, New York.
50. Robinson, C. V., Gross, M., Eyles, S. J., Ewbank, J. J., Mayhew, M., Hartl, F. U., Dobson, C. M. & Radford, S. E. (1994). Conformation of GroEL-bound α-lactalbumin probed by mass spectrometry Nature, 372, 646-651.
51. Saibil, H. R., Zheng, D., Roseman, A. M., Hunter, A. S., Watson, G. M. F., Chen, S., auf der Macer, A., O'Hara, B. P., Wood, S. P., Mann, N. H., Barnett, L. K. & Ellis, R. J. (1993). ATP induces large quaternary rearrangements in a cage-like chaperonin structure. Curr. Biol. 3, 265-273.
52. Sommers, P B. & Kronman, M. J. (1980). Comparative fluorescence properties of bovine, goat, human and guinea pig α-lactalbumin. Characterization of the environments of individual tryptophan residues in partially folded conformers. Biophys. Chem. 11, 217-232.
53. Staniforth, R. A., Burston, S. G., Atkinson, T. & Clarke, A. R. (1994). Affinity of chaperonin-60 for a protein substrate and its modulation by nucleotides and chaperonin-10. Biochem. J. 300, 651-658.
54. Sugai, S. & Ikeguchi, M. (1994). Conformational comparison between α-lactalbumin and lysozyme. Advan. Biophys. 30, 37-84.
55. Viitanen, P. V., Gatenby A. A. & Lorimer, G. H. (1992). Purified chaperonin 60 (groEL) interacts with the nonnative states of a multitude of Escherichia coli proteins. Protein Sci. 1, 363-369.
56. Weissman, J. S., Kashi, Y., Fenton, W. A. & Horwich, A. L. (1994). GroEL-mediated protein folding proceeds by multiple rounds of binding and release of nonnative forms. Cell, 78, 693-702.
57. Wu, L. C., Peng, Z. & Kim, P. S. (1995). Bipartite structure of the α-lactalbumin molten globule. Nature Struct. Biol. 2, 281-286.
58. Yutani, K., Ogasahara, K. & Kuwajima, K. (1992). The absence of the thermal transition in apo-α-lactalbumin in the molten globule state: a study by differential scanning microcalorimetry J. Mol Biol. 228, 347-350.
59. Zahn, R. & Plückthun, A. (1992). GroE prevents the accumulation of early folding intermediates of pre-β-lactamase without changing the folding pathway Biochemistry, 31, 3249-3255.
60. Zahn, R. & Plückthun, A. (1994). Thermodynamic partitioning model for hydrophobic binding of polypeptides by GroEL. II. GroEL recognizes thermally unfolded mature β-lactamase. J. Mol. Biol. 242, 165-174.
61. Zahn, R., Axmann, S. E., Rücknagel, K. P., Jaeger, E., Laminet, A. A. & Plückthun, A. (1994). Thermodynamic partitioning model for hydrophobic binding of polypeptides by GroEL. I. GroELrecognizes the signal sequences of β-lactamase precursor. J. Mol. Biol. 242, 150-164.