Apo-azurin folds via an intermediate that resembles the molten-globule

Protein Science

Volumn 13, Issue 10, 2004, Pages 2628-2638

  Sandberg, Anders ^a   Leckner, Johan ^b   Karlsson, B Göran ^a,b  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

sandwich; Azurin; Cupredoxin; Greek key; Intermediate; Protein folding

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; ACID; ALANINE; APOAZURIN; AZURIN; BACTERIAL PROTEIN; GUANIDINE; LIGAND; MUTANT PROTEIN; SERINE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CALCULATION; CONFORMATIONAL TRANSITION; ENERGY; HYDROGEN BOND; KINETICS; MEASUREMENT; METAL BINDING; MOLECULAR MODEL; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; STRUCTURE ANALYSIS;

APOPROTEINS; AZURIN; HYDROGEN BONDING; KINETICS; MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; THERMODYNAMICS;

BACTERIA (MICROORGANISMS); NEGIBACTERIA; PSEUDOMONAS; PSEUDOMONAS AERUGINOSA;

EID: 4644362445     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.04848204     Document Type: Article

References (45)

1. Anfinsen, C.B. 1973. Principles that govern the folding of protein chains. Science 181: 223-230.
2. Arai, M. and Kuwajima, K. 2000. Role of the molten globule state in protein folding. Adv. Protein Chem. 53: 209-282.
3. Capaldi, A.P., Ferguson, S.J., and Radford, S.E. 1999. The Greek key protein apo-pseudoazurin folds through an obligate on-pathway intermediate. J Mol. Biol. 286: 1621-1632.
4. Chothia, C., Hubbard, T., Brenner, S., Barns, H., and Murzin, A. 1997. Protein folds in the all-β and all-α classes. Annu. Rev. Biophys. Biomol. Struct. 26: 597-627.
5. Clarke, J. and Fersht, A.R. 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.
6. Clarke, J., Cota, E., Fowler, S.B., and Hamill, S.J. 1999. Folding studies of immunoglobulin-like β-sandwich proteins suggest that they share a common folding pathway. Structure Fold. Des. 7: 1145-1153.
7. Denisov, V.P., Jonsson, B.H., and Halle, B. 1999. Hydration of denatured and molten globule proteins. Nat. Struct. Biol. 6: 253-260.
8. Dill, K.A. and Shortle, D. 1991. Denatured states of proteins. Annu. Rev. Biochem. 60: 795-825.
9. Eftink, M.R. 1991. Fluorescence techniques for studying protein structure. Methods Biochem. Anal. 35: 127-205.
10. Fersht, A. 1999. Structure and mechanism in protein science. A guide to enzyme catalysis and protein folding. W.H. Freeman and Company, New York.
11. Fowler, S.B. and Clarke, J. 2001. Mapping the folding pathway of an immunoglobulin domain, structural detail from Phi value analysis and movement of the transition state. Structure (Camb.) 9: 355-366.
12. Gray, H.B., Malmstrom, B.G., and Williams, R.J. 2000. Copper coordination in blue proteins. J. Biol. Inorg. Chem. 5: 551-559.
13. Haber, E. and Anfinsen, C.B. 1962. Side-chain interactions governing the pairing of half-cystine residues in ribonuclease. J. Biol. Chem. 237: 1839-1844.
14. Hoitink, C.W. 1993. "Engineering of the coppersite of azurin from Alcaligenes denitrificans." Ph.D. thesis, Leiden University, The Netherlands.
15. Jackson, S.E. 1998. How do small single-domain proteins fold? Fold. Des. 3: R81-R91.
16. Jackson, S.E. and Fersht, A.R. 1991a. Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry 30: 10428-10435.
17. -. 1991b. Folding of chymotrypsin inhibitor 2. 2. Influence of proline isomerization on the folding kinetics and thermodynamic characterization of the transition state of folding. Biochemistry 30: 10436-10443.
18. Karlsson, B.G., Pascher, T., Nordling, M., Arvidsson, R.H., and Lundberg, L.G. 1989. Expression of the blue copper protein azurin from Pseudomonas aeruginosa in Escherichia coli. FEBS Lett. 246: 211-217.
19. Kiefhaber, T., Kohler, H.H., and Schmid, F.X. 1992. Kinetic coupling between protein folding and prolyl isomerization. 1. Theoretical models. J Mol. Biol. 224: 217-229.
20. Kister, A.E., Finkelstein, A.V., and Gelfand, I.M. 2002. Common features in structures and sequences of sandwich-like proteins. Proc. Natl. Acad. Sci. 99: 14137-14141.
21. Koide, S., Dyson, H.J., and Wright, P.E. 1993. Characterization of a folding intermediate of apoplastocyanin trapped by proline isomerization. Biochemistry 32: 12299-12310.
22. Krantz, B.A., Mayne, L., Rumbley, J., Englander, S.W., and Sosnick, T.R. 2002. Fast and slow intermediate accumulation and the initial barrier mechanism in protein folding. J. Mol. Biol. 324: 359-331.
23. Kraulis, P.J. 1991. Molscript-A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24: 946-950.
24. Levinthal, C. 1968. Are there pathways for protein folding? J. Chim. Phys. 65: 44-45.
25. Makhatadze, G.I. 1999. Thermodynamics of protein interactions with urea and guanidinium hydrochloride. J. Phys. Chem. B 103: 4781-4785.
26. Matouschek, A. and Fersht, A.R. 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. 90: 7814-7818.
27. Monera, O.D., Kay, C.M., and Hodges, R.S. 1994. Protein denaturation with guanidine hydrochloride or urea provides a different estimate of stability depending on the contributions of electrostatic interactions. Protein Sci. 3: 1984-1991.
28. Nozaki, Y. 1972. The preparation of guanidine hydrochloride. Methods Enzymol. 26: 43-50.
29. Parker, M.J., Spencer, J., and Clarke, A.R. 1995. An integrated kinetic analysis of intermediates and transition states in protein folding reactions. J. Mol. Biol. 253: 771-786.
30. Plaxco, K.W., Simons, K.T., and Baker, D. 1998. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 277: 985-994.
31. Pozdnyakova, I. and Wittung-Stafshede, P. 2003. Approaching the speed limit for Greek Key β-barrel formation, transition-state movement tunes folding rate of zinc-substituted azurin. Biochim. Biophys. Acta 1651: 1-4.
32. Pozdnyakova, I., Guidry, J., and Wittung-Stafshede, P. 2001. Copper stabilizes azurin by decreasing the unfolding rate. Arch. Biochem. Biophys. 390: 146-148.
33. Ptitsyn, O.B. 1995. Molten globule and protein folding. Adv. Protein Chem. 47: 83-229.
34. Reader, J.S., Van Nuland, N.A., Thompson, G.S., Ferguson, S.J., Dobson, C.M., and Radford, S.E. 2001. A partially folded intermediate species of the β-sheet protein apo-pseudoazurin is trapped during proline-limited folding. Protein Sci. 10: 1216-1224.
35. Richardson, J.S. 1977. β-Sheet topology and the relatedness of proteins. Nature 268: 495-500.
36. Sanchez, I.E. and Kiefhaber, T. 2003. Evidence for sequential barriers and obligatory intermediates in apparent two-state protein folding. J. Mol. Biol. 325: 367-376.
37. Sandberg, A., Leckner, J., Shi, Y., Schwarz, F.P., and Karlsson, B.G. 2002. Effects of metal ligation and oxygen on the reversibility of the thermal denaturation of Pseudomonas aeruginosa azurin. Biochemistry 41: 1060-1069.
38. Santoro, M.M. and Bolen, D.W. 1988. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants. Biochemistry 27: 8063-8068.
39. 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 hydrophobic fluorescent probe. Biopolymers 31: 119-128.
40. Silow, M. and Oliveberg, M. 1997a. High-energy channeling in protein folding. Biochemistry 36: 7633-7637.
41. Silow, M. and Oliveberg, M. 1997b. Transient aggregates in protein folding are easily mistaken for folding intermediates. Proc. Natl. Acad. Sci. 94: 6084-6086.
42. Solomon, E.I., Baldwin, M.J., and Lowery, M.D. 1992. Electronic- structures of active-sites in copper proteins-Contributions to reactivity. Chem. Rev. 92: 521-542.
43. Solomon, E.I., LaCroix, L.B., and Randall, D.W. 1998. Electronic structure contributions to function in bioinorganic chemistry, the blue copper active site. Pure Appl. Chem. 70: 799-808.
44. Stryer, L. 1965. The interaction of a naphthalene dye with apomyoglobin and apohemoglobin. A fluorescent probe of nonpolar binding sites. J. Mol. Biol. 13: 482-495.
45. Wallace, L.A. and Matthews, C.R. 2002. Sequential vs. parallel protein-folding mechanisms, experimental tests for complex folding reactions. Biophys. Chem. 101-102: 113-131.