Folding intermediate and folding nucleus for i → n and u → i → n transitions in apomyoglobin: contributions by conserved and nonconserved residues

Biophysical Journal

Volumn 98, Issue 8, 2010, Pages 1694-1702

  Samatova, Ekaterina N ^a   Melnik, Bogdan S ^a   Balobanov, Vitaly A ^a   Katina, Natalya S ^a   Dolgikh, Dmitry A ^b   Semisotnov, Gennady V ^a   Finkelstein, Alexei V ^a   Bychkova, Valentina E ^a  

^a Institute of Protein Research   (Russian Federation)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77951648827     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.12.4326     Document Type: Article

References (48)

1. Matouschek, A., J. T. Kellis, Jr., ..., A. R. Fersht. 1989. Mapping the transition state and pathway of protein folding by protein engineering. Nature. 340: 122-126. (Pubitemid 19175363)
2. Matouschek, A., J. T. Kellis, Jr, ...., A. R. Fersht. 1990. Transient folding intermediates characterized by protein engineering. Nature. 346: 440-445. (Pubitemid 120005916)
3. Itzhaki, L. S., D. E. Otzen, and A. R. Fersht. 1995. The structure of the transition, state for folding of chymotrypsin inhibitor 2 analyzed by protein engineering methods: evidence for a nucleation-condensation mechanism for protein folding. J. Mol. Biol. 254: 260-288.
4. Fulton, K. F., E. R. Main, ..., S. E. Jackson. 1999. Mapping the interactions present in the transition state for unfolding/folding of FKBP12. J. Mol. Biol. 291: 45-461.
5. Chiti, F., N. Taddei, ..., C. M. Dobson. 1999. Mutational analysis of acylphosphatase suggests the importance of topology and contact order in protein folding. Nat. Struct. Biol. 6: 1005-1009. (Pubitemid 29519592)
6. Villegas, V., J. C. Martinez, ..., L. Serrano. 1998. Structure of the transition state in the folding process of human procarboxypeptidase A2 activation domain. J. Mol. Biol. 83: 1027-1036. (Pubitemid 28515331)
7. Grantcharova, V. P., D. S. Riddle, ..., D. Baker. 1998. Important role of hydrogen bonds in the structurally polarized transition state for folding of the Src SH3 domain. Nat. Struct, Biol. 5: 714-720.
8. Kragelund, B. B., P. Osmark, ..., F. M. Poulsen. 1999. The formation of a native-like structure containing eight conserved hydrophobic residues is rate limiting in two-state protein folding of ACBP. Nat. Struct. Biol. 6: 594-601.
9. Jackson, S. E. 1998. How do small single-domain proteins fold? Fold. Des. 3: R81-R91.
10. Martínez, J. C., and L. Serrano. 1999. The folding transition state between SH3 domains is conformationally restricted and evolutionarily conserved. Nat. Struct. Biol. 6: 1010-1016. (Pubitemid 129751058)
11. Riddle, D. S., V. P. Grantcharova, ..., D. Baker. 1999. Experiment and theory highlight role of native state topology in SH3 folding. Nat. Struct. Biol. 6: 1016-1024.
12. Perl, D., C. Welker, ..., F. X. Schmid. 1998. Conservation of rapid two-state folding in mesophilie, thermophilic and hyperthermophilic cold shock proteins. Nat. Struct. Biol. 5: 229-235. (Pubitemid 28113755)
13. Steensma, E., and C. P. M. van Mierlo. 1998. Structural characterization of apoflavodoxin shows that the location of the stable nucleus differs among proteins with, a flavodoxin-like topology. J. Mol. Biol. 282: 653-666. (Pubitemid 28428859)
14. Clarke, A. R., and J. P. Waltho. 1997. Protein folding and intermediates. Curr. Opin. Biotechnol. 8:400-4-10.
15. Tanford, C. 1970. Protein denaturation. C. Theoretical models for the mechanism of denaturation. Adv. Protein Chem. 24:1-95.
16. Serrano, L., A. Matouschek, and A. R. Fersht. 1992. The folding of an enzyme. III. Structure of the transition state for unfolding of barnase analyzed by a protein engineering procedure. J. Mol. Biol. 224: 805-818.
17. López-Hemández, E., and L. Serrano. 1996. Structure of the transition state for folding of the 129 aa protein CheY resembles that of a smaller protein, CI-2. Fold. Des. 1:43-55. (Pubitemid 126748158)
18. Cota, E., and J. Clarke. 2000. Folding of β-sandwich proteins: threestate transition of a fibronectin type III module. Protein Sci. 9: 112-1.20.
19. Schymkowitz, J., F. Rousseau, ..., L. Itzhaki. 2000. The folding pathway of the cell-cycle regulatory protein p13suc1: clues for the mechanism of domain swapping. Struct. Fold. Des. 8: 89-100.
20. Nölting, B., R. Golbik, ..., A. R. Fersht. 1997. The folding pathway of a protein at high resolution from microseconds to seconds. Proc. Natl. Acad. Sci. USA. 94: 826-830. (Pubitemid 27074406)
21. Fowler, S. B., and J. Clarke. 2001. Mapping the folding pathway of an immunoglobulin domain: structural detail from -value analysis and movement of the transition state. Structure. 9: 355-366.
22. Baryshnikova, E. N., B. S. Melnik, ...., V. E. Bychkova. 2005. Threestate protein folding: experimental determination of free-energy profile. Protein. Sci. 14: 2658-2667.
23. Eliezer, D., and P. E. Wright. 1996. Is apomyoglobin a molten globule? Structural characterization by NMR. J. Mol. Biol. 263: 531-538. (Pubitemid 26382073)
24. Gast, K., H. Damaschun, ..., G. Damaschun. 1994. Compactness of protein, molten globules: temperature-induced structural changes of the apomyoglobin folding intermediate. Eur. Biophys. J. 23: 297-305. (Pubitemid 24331693)
25. Griko, Y. V., and P. L. Privalov. 1994. Thermodynamic puzzle of apomyoglobin. unfolding. J. Mol. Biol. 235: 1318-1325.
26. Lecomte, J. T., Y. H. Kao, and M. J. Coceo. 1996. The native state of apomyoglobin described by proton NMR spectroscopy: the A-B-G-H interface of wild-type sperm whale apomyoglobin. Proteins. 25: 267-285.
27. Pfeil, W. 1998. Stability and co-operative properties of partially folded proteins. Biochemistry (Mosc.). 63: 294-302. (Pubitemid 128588267)
28. Jennings, P. A., and P. E. Wright. 1993. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science. 262: 892-896.
29. Nishimura, C., H. J. Dyson, and P. E. Wright. 2002. The apomyoglobin folding pathway revisited: structural heterogeneity in the kinetic burst phase intermediate. J. Mol. Biol. 322: 483-489.
30. Nishimura, Ch., H. J. Dyson, and P. E. Wright. 2006. Identification of native and non-native structure in kinetic folding intermediates of apomyoglobin. J. Mol. Biol, 355: 139-156.
31. Jamin, M., and R. L. Baldwin. 1998. Two forms of the pH 4 folding intermediate of apomyoglobin. J. Mol. Biol. 276: 491-504.
32. Tsui, V., C. Garcia, ..., P. E. Wright. 1999. Quench-flow experiments combined with mass spectrometry show apomyoglobin folds through an obligatory intermediate. Protein Sci. 8:45-49. (Pubitemid 29035517)
33. Shakhnovich, E., V. Abkevich, and O. Ptitsyn. 1996. Conserved residues and the mechanism, of protein folding. Nature. 379: 96-98. (Pubitemid 3013008)
34. Ptitsyn, O. B., and K.-L. H. Ting. 1999. Non-functional conserved residues in globins and their possible role as a folding nucleus. J. Mol. Biol. 291: 671-682.
35. Garbuzinskii, S. A., A. V. Finkelstein, and O. V. Galzitskaia. 2005. [On prediction of folding nuclei in globular proteins]. Mol. Biol. (Most). 39: 1032-1041.
36. Samatova, E. N., N. S. Katina, ..., A. V. Finkelstein. 2009. How strong are side chain interactions in the folding intermediate? Protein Sci. 18: 2152-2159.
37. Jennings, P. A., M. J. Stone, and P. E. Wright. 1995. Overexpression of myoglobin and assignment of its amide, Ca and Cβ resonances. J. Biomol. NMR. 6:271-276.
38. Harrison, S. C., and E. R. Blout. 1965. Reversible conformational changes of myoglobin, and apomyoglobin. J. Biol. Chem. 240: 299-303.
39. Jaenicke, L. 1974. A rapid micromethod for the determination of nitrogen and phosphate in biological material. Anal, Biochem. 61: 623-627.
40. Baryshnikova, E. N., M. G. Sharapov, ..., V. E. Bychkova. 2005. Investigation of apomyoglobin stability depending on urea and temperature at two different pH values. Mol. Biol. (Mosc.). 39:292-297. (Pubitemid 40684855)
41. Parker, M. J., J. Spencer, and A. R. Clarke. 1995. An integrated kinetic analysis of intermediates and transition states in protein folding reactions. J. Mol. Biol. 253: 771-786.
42. Baldwin, R. L. 1996. On-pathway versus off-pathway folding intermediates. Fold. Des. 1;R1-R8.
43. Fersht, A. R. 2000. Structure and Mechanism in Protein Science, 3rd Ed. W. H. Freeman, New York.
44. Parker, M. J., M. Lorch, ..., A. R. Clarke. 1998. Thermodynamic properties of transient intermediates and transition states in the folding of two contrasting protein structures. Biochemistry. 37: 2538-2545.
45. Hughson, F. M., and R. L. Baldwin. 1989. Use of site-directed mutagenesis to destabilize native apomyoglobin relative to folding intermediates. Biochemistry. 28: 4415-4422.
46. Hargrove, M. S., S. Krzywda, ..., J. S. Olson. 1994. Stability of myoglobin: a model for the folding of heme proteins. Biochemistry. 33: 11767-11775. (Pubitemid 24327984)
47. Ptitsyn, O. B. 1995. Structures of folding intermediates. Curr. Opin. Struct. Biol, 5: 74-78.
48. Vojtechovský, J., K. Chu, ..., I. Schlichting. 1999. Crystal, structures of myoglobin-ligand complexes at near-atomic resolution. Biophys. J. 77: 2153-2174.