Structural characterisation of apoflavodoxin shows that the location of the stable nucleus differs among proteins with a flavodoxin-like topology

Journal of Molecular Biology

Volumn 282, Issue 3, 1998, Pages 653-666

  Steensma, Elles ^a   Van Mierlo, Carlo P M ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Apoflavodoxin; Deuterium exchange; Hydrogen; NMR spectroscopy; Protein folding; Protein stability

Indexed keywords

APOFLAVODOXIN; CUTINASE; DEUTERIUM; FLAVODOXIN; HYDROGEN; QUERCETIN; UNCLASSIFIED DRUG;

ARTICLE; AZOTOBACTER VINELANDII; CARBOXY TERMINAL SEQUENCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE;

AZOTOBACTER VINELANDII;

EID: 0032566696     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2045     Document Type: Article

References (45)

1. Bai, Y., Milne, J. S., Mayne, L. & Englander, S. W. (1993). Primary structure effects on peptide group hydrogen exchange. Proteins: Struct. Funct. Genet. 17, 75-86.
2. Bai, Y., Milne, J. S., Mayne, L. & Englander, S. W. (1994). Protein stability parameters measured by hydrogen exchange. Proteins: Struct. Funct. Genet. 20, 4-14.
3. Baldwin, T. O., Christopher, J. A., Raushel, F. M., Sinclair, J. F., Ziegler, M. M., Fisher, A. J. & Rayment, I. (1995). Structure of bacterial luciferase. Curr. Opin. Struct. Biol. 5, 798-809.
4. Brenner, S. E. (1997). Population statistics of protein structures: lessons from structural classifications. Curr. Opin. Struct. Biol. 7, 369-376.
5. Bruix, M., Muñoz, V., Campos-Olivas, R., Del Bosque, J. R., Serrano, L. & Rico, M. (1997). Characterisation of the isolated Che Y C-terminal fragment (79-129)-exploring the structure/stability/folding relationships of the α/β parallel protein Che Y. Eur. J. Biochem. 243, 384-392.
6. 15N resonance assignments of oxidized flavodoxin from Anacystis nidulans with 3D NMR. Biochemistry, 30, 7718-7730.
7. Creighton, T. E. (1992). Protein Folding, W. H. Freeman and Company, New York.
8. Creighton, T. E. (1994). The protein folding problem. In Mechanisms of Protein Folding (Pain, R. H., ed.), pp. 1-25, IRL Press, Oxford.
9. Edmondson, D. E. & Tollin, G. (1971). Chemical and physical characterization of the Shethna flavoprotein and apoprotein and kinetics and thermodynamics of flavin analog binding to the apoprotein. Biochemistry, 10, 124-132.
10. Eliezer, D. & Wright, P. E. (1996). Is apomyoglobin a molten globule? Structural characterization by NMR. J. Mol. Biol. 263, 531-538.
11. Englander, S. W. & Kallenbach, N. R. (1984). Hydrogen exchange and structural dynamics of proteins and nucleic acids. Quart. Rev. Biophys. 16, 521-655.
12. Englander, S. W. & Mayne, L. (1992). Protein folding studied using hydrogen-exchange labeling and two-dimensional NMR. Annu. Rev. Biophys. Biomol. Struct. 21, 243-265.
13. Englander, S. W., Sosnick, T. R., Englander, J. J. & Mayne, L. (1996). Mechanisms and uses of hydrogen exchange. Curr. Opin. Struct. Biol. 6, 18-23.
14. Genzor, C. G., Perales-Alcón, A., Sancho, J. & Romero, A. (1996). Closure of a tyrosine/tryptophan aromatic gate leads to a compact fold in apo flavodoxin. Nature Struct. Biol. 3, 329-332.
15. Grandori, R. & Carey, J. (1994). Six new candidate members of the α/β twisted open-sheet family detected by sequence similarity to flavodoxin. Protein Sci. 3, 2185-2193.
16. Hvidt, A. & Nielsen, S. O. (1966). Hydrogen exchange in proteins. Advan. Protein Chem. 21, 287-386.
17. Jeng, M.-F. & Dyson, H. J. (1995). Comparison of the hydrogen-exchange behavior of reduced and oxidized Escherichia coli thioredoxin. Biochemistry, 34, 611-619.
18. 1H-nuclear magnetic resonance spectroscopy in peptides related to the N terminus of bovine pancreatic trypsin inhibitor. J. Mol. Biol. 230, 312-322.
19. Knauf, M. A., Löhr, F., Curley, G. P., O'Farrell, P., Mayhew, S. G., Müller, F. & Rüterjans, H. (1993). Homonuclear and heteronuclear NMR studies of oxidized Desulfovibrio vulgaris flavodoxin - sequential assignments and identification of secondary structure elements. Eur. J. Biochem. 213, 167-184.
20. Lacroix, E., Bruix, M., López-Hernández, E., Serrano, L. & Rico, N. (1997). Amide hydrogen exchange and internal dynamics the chemotactic protein Chey from Escherichia coli. J. Mol. Biol. 271, 472-487.
21. Linderstrøm-Lang, K. (1955). Deuterium exchange between peptides and water. Chem. Soc. (London) Spec. Publ. 2, 1-20.
22. López-Hernández, E. & Serrano, L. (1996). Structure of the transition state for folding of the 129 aa protein CheY resembles that of a smaller protein, CI-2. Folding Design, 1, 43-55.
23. Orengo, C. A., Jones, D. T. & Thornton, J. M. (1994). Protein superfamilies and domain superfolds. Nature, 372, 631-634.
24. 13C backbone assignments and secondary solution structure of the flavodoxin. J. Biomol. NMR, 7, 315-330.
25. 15N NMR resonance assignments and solution secondary structure of oxidized Desulfovibrio desulfuricans flavodoxin. J. Biomol. NMR, 7, 225-235.
26. 15N resonance assignments of Fusarium solani pisi cutinase and preliminary features of the structure in solution. Protein Sci. 6, 2375-2384.
27. 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.
28. Sandalova, T. & Lindqvist, Y. (1993). Crystal structure of apo-glycolate oxidase. FEBS Letters, 327, 361-365.
29. Santoro, M. M. & 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.
30. Sanz, J. M. & Fersht, A. R. (1993). Rationally designing the accumulation of a folding intermediate of barnase by protein engineering. Biochemistry, 32, 13584-13592.
31. Sayle, R. A. & Milner-White, E. J. (1995). RasMol: biomolecular graphics for all. Trends Biochem. Sci. 20, 374-376.
32. Shortle, D. R. (1996). Structural analysis of non-native states of proteins by NMR methods. Curr. Opin. Struct. Biol. 6, 24-30.
33. Steensma, E., Heering, H. A., Hagen, W. R. & van Mierlo, C. P. M. (1996). Redox properties of wild-type, Cys69Ala, and Cys69Ser Azotobacter vinelandii flavodoxin II as measured by cyclic voltammetry and EPR spectroscopy. Eur. J. Biochem. 235, 167-172.
34. Steensma, E., Nijman, M. J. M., Bollen, Y. J. M., de Jager, P. A., van den Berg, W. A. M., van Dongen, W. M. A. M. & van Mierlo, C. P. M. (1998). Apparent local stability of the secondary structure of Azotobacter vinelandii holoflavodoxin II as probed by hydrogen exchange: implications for redox potential regulation and flavodoxin folding. Protein Sci. 7, 306-317.
35. Swint-Kruse, L. & Robertson, A. D. (1996). Temperature and pH dependences of hydrogen exchange and global stability for ovomucoid third domain. Biochemistry, 35, 171-180.
36. van Mierlo, C. P. M., Vervoort, J., Müller, F. & Bacher, A. (1990a). A two-dimensional 1H NMR study on Megasphaera elsdenii flavodoxin in the reduced state: sequential assignments. Eur. J. Biochem. 187, 521-541.
37. 1H NMR and restrained molecular dynamics. Eur. J. Biochem. 194, 185-198.
38. 15N relaxation measurements. J. Mol. Biol. 229, 1125-1146.
39. van Mierlo, C. P. M., van Dongen, W. M. A. M., Vergeldt, F., van Berkel, W. J. H. & Steensma, E. (1998). The equilibrium unfolding of Azotobacter vinelandii apoflavodoxin II occurs via a relatively stable folding intermediate. Protein Sci. In the press.
40. 13C-separated HMQC-NOESY-HMQC spectra using pulsed field gradients. J. Magn. Reson. B, 101, 210-213.
41. Wagner, G. & Wüthrich, K. (1979). Correlation between the amide proton exchange rates and the denaturation temperatures in globular proteins related to the basic pancreatic trypsin inhibitor. J. Mol. Biol. 130, 31-37.
42. 13C chemical-shift data. J. Biomol. NMR, 4, 171-180.
43. Wishart, D. S., Sykes, B. D. & Richards, F. M. (1992). The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry, 31, 1647-1651.
44. Woodward, C. K. (1994). Hydrogen exchange rates and protein folding. Curr. Opin. Struct. Biol. 4, 112-116.
45. Wüthrich, K. (1986). NMR of Proteins and Nucleic Acids, Wiley, New York.