Protein dissection experiments reveal key differences in the equilibrium folding of α-lactalbumin and the calcium binding lysozymes

Biochemistry

Volumn 43, Issue 31, 2004, Pages 9961-9967

  Chowdhury, Farhana A ^a   Fairman, Robert ^b   Bi, Yuan ^a   Rigotti, Daniel J ^b   Raleigh, Daniel P ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b HAVERFORD COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; ENZYMES; MOLECULAR STRUCTURE; POLYPEPTIDES;

CANINE; PROTEIN DISSECTION;

BIOCHEMISTRY;

ALPHA LACTALBUMIN; GLOBULAR PROTEIN; LYSOZYME; PEPTIDE;

ARTICLE; CALCIUM BINDING; COMPARATIVE STUDY; DOG; HORSE; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

AMINO ACID SEQUENCE; ANIMALS; CALCIUM-BINDING PROTEINS; DOGS; ENZYME STABILITY; HORSES; HUMANS; LACTALBUMIN; MOLECULAR SEQUENCE DATA; MURAMIDASE; PEPTIDE FRAGMENTS; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; UREA;

CANIS FAMILIARIS; EQUIDAE; EQUUS CABALLUS;

EID: 3543062840     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi049277s     Document Type: Article

References (42)

1. Kuwajima, K. (1989) The molten globule state as a clue for understanding the folding and cooperatively of globular-protein structure. Proteins: Struct., Funct., Genet. 6, 87-103.
2. Creighton, T. E. (1997) How important is the molten globule for correct protein folding? Trends Biochem. Sci. 22, 6-10.
3. Ptitsyn, O. B. (1995) Molten globule and protein folding. Adv. Prot. Chem. 47, 83-217.
4. Arai, M., and Kuwajima, K. (2000) Role of the molten globule state in protein folding. Adv. Protein Chem. 53, 209-271.
5. Fink, A. L. (1995) Compact intermediate states in protein folding. Annu. Rev. Biomol. Struct. 24, 495-522.
6. Dolgikh, D. A., Gilmanshin, R. I., Brazhnikov, E. V., Bychkova, V. E., Semisotnov, G. V., Venyaminov, S. Y., and Ptitsyn, O. B. (1981) α-Lactalbumin: compact state with fluctuating tertiary structure? FEBS Lett. 136, 311-315.
7. Ohgushi, M. a. W., A. (1983) "Molten globule state": a compact form of globular proteins with mobile side-chains. FEBS Lett. 164, 21-24.
8. 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.
9. Chamberlain, A. K., and Marqusee, S. (2000) Comparison of equilibrium and kinetic approaches for determining protein folding mechanisms. Adv. Prot. Chem. 53, 283-328.
10. Engelhard, M., and Evans, P. A. (1995) Kinetics of interaction of partially folded proteins with a hydrophobic dye: Evidence that molten globule character is maximal in early folding intermediate. Protein Sci. 4, 1553-1562.
11. Kelly, J. W. (1998) The alternative conformations of amyloidogenic proteins and their multistep assembly pathways. Curr. Opin. Struct. Biol. 8, 101-106.
12. Uversky, V. N., and Ptitsyn, O. B. (1994) "Partly folded" state, a new equilibrium state of protein molecules: four-state guanidinium chloride-induced unfolding of β-lactamase at low temperature. Biochemistry 33, 2782-2791.
13. Uversky, V. N., and Ptitsyn, O. B. (1996) Further evidence on the equilibrium "pre-molten globule state": four-state guanidinium chloride-induced unfolding of carbonic anhydrase B at low temperature. J. Mol. Biol. 255, 215-228.
14. Qasba, P. K., and Kumar, S. (1997) Molecular divergence of lysozymes and α-lactalbumin. CRC Crit. Rev. Biochem. 32, 255-306.
15. Acharya, K. R., Ren, J., Stuart, D. I., Phillips, D. C., and Fenna, R. E. (1991) Crystal structure of human α-lactalbumin at 1.7 Å resolution. J. Mol. Biol. 221, 571-581.
16. Grobler, J. A., Ramakrishna, R. K., Pervaiz, S., and Brew, K. (1994) Sequences of two highly different canine type C lysozymes: implications for the evolutionary origins of the lysozyme/α-lactalbumin superfamily. Arch. Biochem. Biophys. 313, 360-366.
17. Dobson, C. M., Evans, P. A., and Radford, S. E. (1994) Understanding how proteins fold: the lysozyme story so far. Trends Biochem. Sci. 19, 31-37.
18. Ikeguchi, M., Kuwajima, K., Mitani, M., and 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.
19. Morozova-Roche, L. A., Arico-Muendel, C. C., Haynie, D. T., Emelyanenko, V. I., Van Dael, H., and Dobson, C. M. (1997) Structural characterization and comparison of the native and A-state of equine lysozyme. J. Mol. Biol. 268, 903-921.
20. Mizuguchi, M., Arai, M., Ke, Y., Nitta, K., and Kuwajima, K. (1998) Equilibrium and kinetics of the folding of equine lysozyme studied by circular dichroism spectroscopy. J. Mol. Biol. 283, 265-277.
21. 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.
22. Morozova, L. A., Haezebrouck, P., and Van Cauwelaert, F. (1991) Stability of equine lysozyme. 1. Thermal unfolding behavior. Biophys. Chem. 41, 185-191.
23. Van Dael, H., Haezebrouck, P., Morozova, L., Arico-Muendel, C., and Dobson, C. M. (1993) Partially folded states of equine lysozyme. Structural characterization and significance for protein folding. Biochemistry 32, 11886-11894.
24. Joniau, M., Haezebrouck, P., Noyelle K., and Van Dael, H. (2001) Structural basis for the appearance of a molten globule state in chimeric molecules derived from lysozyme and α-lactalbumin. Proteins: Struct., Funct., Genet. 44, 1-11.
25. Hendrix, T. M., Griko, Y. V., and Privalov, P. L. (1996) Energetics of structural domains in α-lactalbumin. Protein Sci. 5, 923-931.
26. Radford, S. E., Woolfson, D. N., Martin, S. R., Lowe, G., and Dobson, C. M. (1991) A three-disulphide derivative of hen lysozyme. Structure, dynamics, and stability. Biochem. J. 273, 211-217.
27. Peng, Z.-y., and Kim, P. S. (1994) A protein dissection study of a molten globule. Biochemistry 30, 3248-3252.
28. Baum, J., Dobson, C. M., Evans, P. A., and Hanely, 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.
29. Polverino de Laureto, P., Scaramella, E., Frigo, M., Gefter Wondrich, F., De Filippis, V., and Fontana A. (1999) Limited proteolysis of bovine α-lactalbumin: isolation and characterization of protein domains. Protein Sci. 8, 2290-2303.
30. Schulman, B. A., Kim, P. S., Dobson, C. M., and Redfield, C. (1997) A residue-specific NMR view of the noncooperative unfolding of a molten globule. Nat. Struct. Biol. 4, 630-634.
31. Schulman, B. A., Redfield, C., Peng, Z.-y., Dobson, C. M., and Kim, P. S. (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.
32. Demarest, S. J., Zhou, S.-Q., Robblee, J., Fairman, R., Chu, B., and Raleigh, D. P. (2001 A) A comparative study of peptide models of the α-domain of α-lactalbumin, lysozyme, and α-lactalbumin/ lysozyme chimeras allows the elucidation of critical factors that contribute to the ability to form stable partially folded states. Biochemistry 40, 2138-2147.
33. Demarest, S. J., Homg, J.-C., and Raleigh, D. P. (2001B) A protein dissection study demonstrates that two specific hydrophobic clusters play a key role in stabilizing the core structure of the molten globule state of human α-lactalbumin. Proteins: Struct., Funct., Genet. 42, 237-242.
34. Demarest, S. J., Fairman, R., and Raleigh, D. P. (1998) Peptide models of local and long-range interactions in the molten globule state of human α-lactalbumin. J. Mol. Biol. 283, 279-291.
35. Demarest, S. J., Boice, J. A., Fairman, R., and Raleigh, D. P. (1999) Defining the core structure of the α-lactalbumin molten globule state. J. Mol. Biol. 294, 213-221.
36. 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.
37. Semisotnov, G. V., Rodionova, N. A., Razgulyaev, O. I., Uversky, V. N., Gripas, A. F., and Gilmanshin, R. I. (1991) Study of the "molten globule" intermediate state in protein folding by a hydrpophobic fluorescent probe. Biopolymers 31, 119-128.
38. Matullis, D., and Lovrien, R. (1998) 1-Anilino-8-naphthalene sulfonate anion-protein binding depends primarily on ion pair formation. Biophys. J. 74, 422-429.
39. Rohl, C. A., and Baldwin, R. L. (1997) Comparison of NH exchange and circular dichroism as techniques for measuring the parameters of helix-coil transition in peptides. Biochemistry 36, 8435-8442.
40. Horng, J.-C., Demarest, S., and Raleigh, D. P. (2003) pH-dependent stability of the human α-lactalbumin molten globule state: contrasting roles of the 6-120 disulfide and the β-subdomain at low and neutral pH. Proteins: Struct., Funct., Genet. 52, 193-202.
41. Kraulis, P. J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr 24, 946-950.
42. Acharya, K. R., Stuart, D. I., Walker, N. P. C., Lewis, M., and Phillips, D. C. (1989) Refined structure of baboon α-lactalbumin at 1.7 Å resolution. J. Mol. Biol. 208, 99-127.