Equilibrium and kinetics of the folding and unfolding of canine milk lysozyme

Biochemistry

Volumn 46, Issue 17, 2007, Pages 5238-5251

  Nakatani, Hiroyasu ^a   Maki, Kosuke ^a   Saeki, Kimiko ^a   Aizawa, Tomoyasu ^b   Demura, Makoto ^b   Kawano, Keiichi ^b   Tomoda, Shuji ^a   Kuwajima, Kunihiro ^a,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

^c OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DICHROISM; ENZYMES; FLUORESCENCE SPECTROSCOPY; PEPTIDES; PHASE TRANSITIONS;

CANINE MILK; FOLDING PATHWAYS; KINETIC REFOLDING CURVES;

PROTEIN FOLDING;

ALPHA LACTALBUMIN; LYSOZYME; MILK PROTEIN;

ARTICLE; BINDING SITE; CALCIUM BINDING; CIRCULAR DICHROISM; DOG; ENZYME BINDING; ENZYME KINETICS; FLUORESCENCE SPECTROSCOPY; MILK; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING;

ANIMALS; CIRCULAR DICHROISM; DOGS; KINETICS; MILK; MURAMIDASE; PROTEIN DENATURATION; PROTEIN FOLDING; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 34247859221     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi602464v     Document Type: Article

References (43)

1. Anfinsen, C. B. (1973) Principles that govern the folding of protein chains, Science 181, 223-230.
2. Kuwajima, K. (1989) The molten globule state as a clue of understanding the folding and cooperativity of globular-protein structure, Proteins 6, 87-103.
3. Ptitsyn, O. B. (1995) Molten globule and protein folding, Adv. Protein Chem. 47, 83-229.
4. Arai, M., and Kuwajima, K. (2000) Role of the molten globule state in protein folding, Adv. Protein Chem. 53, 209-282.
5. Jackson, S. E. (1998) How do small single-domain proteins fold? Folding Des. 3, R81-R91.
6. Arai, M., and Kuwajima, K. (1996) Rapid formation of a molten globule intermediate in refolding of α-lactalbumin, Folding Des. 1, 275-287.
7. 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.
8. Raschke, T. M., Kho. J., and Marqusee, S. (1999) Confirmation of the hierarchical folding of RNase H: a protein engineering study, Nat. Struct. Biol. 6, 825-831.
9. Pervaiz, S., and Brew, K. (1986) Purification and characterization of the major whey proteins from the milks of the bottlenose dolphin (Tursiops truncates), the florida manatee (Trichechus manatus latirostris), and the beagle (Canis familiaris), Arch. Biochem. Biophys. 246, 846-854.
10. Kikuchi, M., Kawano, K., and Nitta, K. (1998) Calcium-binding and structural stability of echidna and canine milk lysozyme, Protein Sci. 7, 2150-2155.
11. Nitta, K., and Sugai, S. (1989) The evolution of lysozyme and α-lactalbumin, Eur. J. Biochem. 182, 111-118.
12. Grobler, J. A., Rao, K. R., Pervaiz, S., and Brew, K. (1994) Sequences of two highly divergent canine type c lysozymes: implications for the evolutionary origins of the lysozyme/α-lactalbumin superfamily, Arch. Biochem. Biophys. 313, 360-366.
13. Koshiba, T., Yao, M., Kobashigawa, Y., Demura, M., Nakagawa, A., Tanaka, I., Kuwajima, K., and Nitta, K. (2000) Structure and thermodynamics of the extraordinarily stable molten globule state of canine milk lysozyme, Biochemistry 39, 3248-3257.
14. Koshiba, T, Hayashi, T., Ishido, M., Kumagai, I., Ikura, T., Kawano, K., and Nitta, K., and Kuwajima, K. (1999) Expression of a synthetic gene encoding canine milk lysozyme in Escherichia coli and characterization of the expressed protein, Protein Eng. 12, 429-435.
15. Kobashigawa, Y., Demura, M., Koshiba, T., Kumaki, Y., Kuwajima, K., and Nitta, K. (2000) Hydrogen exchange study of canine milk lysozyme: stabilization mechanism of the molten globule, Proteins 40, 579-589.
16. Nakao, M., Arai, M., Koshiba, T., Nitta, K., and Kuwajima, K. (2003) Folding mechanism of canine milk lysozyme studied by circular dichroism and fluorescence spectroscopy, Spectroscopy 17, 183-193.
17. Van Dael, H., Haezebrouck, P., and Joniau, M. (2003) Equilibrium and kinetic studies on folding of canine milk lysozyme, Protein Sci. 12, 609-619.
18. Nakao, M., Maki, K., Arai, M., Koshiba, T., Nitta, K., and Kuwajima, K. (2005) Characterization of kinetic folding intermediates of recombinant canine milk lysozyme by stopped-flow circular dichroism, Biochemistry 44, 6685-6692.
19. Takano, K., Tsuchimori, K., Yamagata, Y., and Yutani, K. (1999) Effect of foreign N-terminal residues on the conformational stability of human lysozyme, Eur. J. Biochem. 266, 675-682.
20. Chaudhuri, T. K., Horii, K., Yoda, T., Arai, M., Nagata, S., Terada, T. P., Uchiyama, H., Ikura, T., Tsumoto, K., Kataoka, H., Matsushima, M., Kuwajima, K., and Kumagai, I. (1999) Effect of the extra N-terminal methionine residue on the stability and folding of recombinant α-lactalbumin expressed in Escherichia coli, J. Mol. Biol. 285, 1179-1194.
21. Akieda, D., Yasui, M., Nonaka, Y., Watanabe, M., Yao, M., Watanabe, N., Tanaka, I., Aizawa, T., Nitta, K., Demura, M., and Kawano, K. Construction of an expression system of canine milk lysozyme in the methylotrophic yeast Pichia pastoris, unpublished work.
22. Pace, C. N. (1986) Determination and analysis of urea and guanidine hydrochloride denaturation curves, Methods Enzymol. 131, 266-280.
23. Santoro, M. M., and Bolen, D. W. (1992) A test of the linear extrapolation of unfolding free energy changes over an extended denaturant concentration range, Biochemistry 31, 4901-4907.
24. 2+ binding on the folding kinetics of α-lactalbumin, J. Mol. Biol. 206, 547-561.
25. Saeki, K., Arai, M., Yoda, T., Nakao, M., and Kuwajima, K. (2004) Localized nature of the transition-state structure in goat α-lactalbumin folding, J. Mol. Biol. 341, 589-604.
26. Tanford, C. (1970) Protein denaturation, Adv. Protein Chem. 24, 1-95.
27. Mizuguchi, M., Arai, M., Ke, Y., Nitta, K., and Kuwajima, K. (1998) Equilibrium and kinetics of the folding of equine milk lysozyme studied by circular dichroism spectroscopy, J. Mol. Biol. 283, 265-277.
28. 2+-induced alternation in the unfolding behavior of α-lactalbumin, J. Biochem. 99, 1191-1201.
29. Tsuge, H., Ago, H., Noma, M., Nitta, K., Sugai, S., and Miyano, M. (1992) Crystallographic studies of a calcium binding lysozyme from equine milk at 2.5 Å resolution, J. Biochem. (Tokyo), 111, 141-143.
30. Chrysina, E. D., Brew, K., and Acharya, K. R. (2000) Crystal structures of apo- and holo-bovine α-lactalbumin at 22-Å resolution reveal an effect of calcium on inter-lobe interactions, J. Biol. Chem. 47, 37021-37029.
31. Aune, K. C., and Tanford, C. (1969) Thermodynamics of the denaturation of lysozyme by guanidine hydrochloride. II. Dependence on denaturant concentration at 25 degrees, Biochemistry 8, 4586-4590.
32. Pfeil, W., and Privalov, P. L. (1976) Thermodynamic investigations of proteins. 1. Standard functions for proteins with lysozyme as an example, Biophys. Chem. 4, 23-32.
33. Griko, Y. V., Freire, E., Privalov, G., Van Dael, H., and Privalov, P. L. (1995) The unfolding thermodynamics of c-type lysozymes: A calorimetric study of the heat denaturation of equine lysozyme, J. Mol. Biol. 252, 447-259.
34. Matouschek, A., Kellis, J. T., Serrano, L., and Fersht, A. R. (1989) Mapping the transition state and pathway of protein folding by protein engineering, Nature, 340, 122-126.
35. Nishimura, C., Prytulla, S., Dyson, H. I., and Wright, P. E. (2000) Conservation of folding pathways in evolutionarily distant globin sequences, Nat. Struct. Biol. 7, 679-686.
36. Forge, V., Wijesinha, R. T., Balbach, J., Brew, K., Robinson, C. V., Redfield, C., and Dobson, C. M. (1999) Rapid collapse and slow structural reorganization during the refolding of bovine alpha-lactalbumin, J. Mol. Biol. 288, 673-688.
37. Zhang, H. J., Sheng, X. R., Niu, W. D., Pan, X. M., and Zhou, J. M. (1998) Evidence for at least two native forms of rabbit muscle adenylate kinase in equilibrium in aqueous solution, J. Biol. Chem. 13, 7448-7456.
38. 1H NMR spectroscopy, Proc. Natl. Acad. Sci. U.S.A. 86, 2195-2198.
39. Doyle, S. M., Bilsel, O., and Teschke, C. M. (2004) SecA folding kinetics: A large dimeric protein rapidly forms multiple native states, J. Mol. Biol. 341, 199-214.
40. Jennings, P. A., Finn, B. E., and Matthews, C. R. (1993) A reexamination of the folding mechanism of dihydrofolate reductase from Escherichia coli: Verification and refinement of a four-channel model, Biochemistry 32, 3783-3789.
41. Evance, P. A., Dobson, C. M., Kauz, R. A., Hatfull, G., and Fox, R. O. (1987) Proline isomerism in staphylococcal nuclease characterized by NMR and site directed mutagenesis, Nature, 329, 266-268.
42. Ionescu, R. M., Smith, V. F., O'Neil, J. C., Jr., and Matthews, C. R. (2000) Multistate equilibrium unfolding of Escherichia coli dihydrofolate reductase: thermodynamic and spectroscopic description of the native, intermediate, and unfolded ensembles, Biochemistry, 39, 9540-9550.
43. Sheng, X. R., Li, X., and Pan, X. M. (1999) An iso-random Bi Bi mechanism for adenylate kinase, J. Biol. Chem. 274, 22238-22242.