Thermal unfolding of apo and holo Desulfovibrio desulfuricans flavodoxin: Cofactor stabilizes folded and intermediate states

Biochemistry

Volumn 43, Issue 40, 2004, Pages 12855-12864

  Muralidhara, B K ^a   Wittung Stafshede, Pernilla ^a,b  

^a RICE UNIVERSITY   (United States)

^b Dept of Biochem and Cell Biology ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENTHALPIC STABILIZATION; FLAVIN MONONUCLEOTIDE (FMN); THERMAL TRANSITIONS; THERMAL UNFOLDING;

ENTHALPY; FLUORESCENCE; HIGH TEMPERATURE EFFECTS; PH; PHASE TRANSITIONS; POLYPEPTIDES; PROTEINS; THERMOANALYSIS; THERMODYNAMIC STABILITY;

SULFUR;

FLAVINE MONONUCLEOTIDE; FLAVODOXIN;

ARTICLE; CIRCULAR DICHROISM; DESULFOVIBRIO; ENTHALPY; FLUORESCENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN STABILITY; TEMPERATURE DEPENDENCE; THERMODYNAMICS; THERMOSTABILITY; ULTRAVIOLET RADIATION;

APOPROTEINS; CIRCULAR DICHROISM; DESULFOVIBRIO DESULFURICANS; FLAVIN MONONUCLEOTIDE; FLAVODOXIN; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SPECTROMETRY, FLUORESCENCE; TEMPERATURE; THERMODYNAMICS;

DESULFOVIBRIO; DESULFOVIBRIO DESULFURICANS; NEGIBACTERIA;

EID: 4944267705     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048944e     Document Type: Article

References (37)

1. Jackson, S. E. (1998) How do small single-domain proteins fold?, Folding Des. 3, R81-R91.
2. Privalov, P. L. (1996) Intermediate states in protein folding, J. Mol. Biol. 258, 707-725.
3. States, D. J., Creighton, T. E., Dobson, C. M., and Karplus, M. (1987) Conformations of intermediates in the folding of the pancreatic trypsin inhibitor, J. Mol. Biol. 195, 731-739.
4. Fersht, A. (1999) Structure and Mechanism in Protein Science, W. H. Freeman, New York.
5. Wittung-Stafshede, P. (2002) Role of cofactors in protein folding, Acc. Chem. Res. 35, 201-208.
6. Wittung-Stafshede, P., Lee, J. C., Winkler, J. R., and Gray, H. B. (1999) Cytochrome b562-folding triggered by electron transfer: approaching the speed limit for formation of a four-helix-bundle protein, Proc. Natl. Acad. Sci. U.S.A. 96, 6587-6590.
7. Wittung-Stafshede, P., Malmstrom, B. G., Winkler, J. R., and Gray, H. B. (1998) Electron-transfer triggered folding of deoxymyo-globin, J. Phys. Chem. 102, 5599-5601.
8. Wittung-Stafshede, P., Malmstrom, B. G., Sanders, D., Fee, J. A., Winkler, J. R., and Gray, H. B. (1998) Effect of redox state on the folding free energy of a thermostable electron-transfer metalloprotein: the CuA domain of cytochrome oxidase from Thermus thermophilus, Biochemistry 37, 3172-3177.
9. Leckner, J., Wittung, P., Bonander, N., Karlsson, G., and Malm-strom, B. (1997) The effect of redox state on the folding free energy of azurin, J. Biol. Inorg. Chem. 2, 368-371.
10. Pozdnyakova, I., and Wittung-Stafshede, P. (2001) Copper binding before polypeptide folding speeds up formation of active (holo) Pseudomonas aeruginosa azurin, Biochemistry 40, 13728-13733.
11. Pozdnyakova, I., and Wittung-Stafshede, P. (2001) Biological relevance of metal binding before protein folding, J. Am. Chem. Soc. 123, 10135-10136.
12. Muller, F. (1992) Chemistry and Biochemistry of Flavoenzymes, CRC Press, Boca Raton, FL.
13. Watenpaugh, K. D., Sieker, L. C., and Jensen, L. H. (1973) The binding of riboflavin-5′-phosphate in a flavoprotein: flavodoxin at 2.0-angstrom resolution, Proc. Natl. Acad. Sci. U.S.A. 70, 3857-3860.
14. Lostao, A., El Harrous, M., Daoudi, F., Romero, A., Parody-Morreale, A., and Sancho, J. (2000) Dissecting the energetics of the apoflavodoxin-FMN complex, J. Biol. Chem. 275, 9518-9526.
15. Genzor, C. G., Perales-Alcon, A., Sancho, J., and Romero, A. (1996) Closure of a tyrosine/tryptophan aromatic gate leads to a compact fold in apo flavodoxin, Nat. Struct. Biol. 3, 329-332.
16. Steensma, E., and van Mierlo, C. P. (1998) Structural characterisation of apoflavodoxin shows that the location of the stable nucleus differs among proteins with a flavodoxin-like topology, J. Mol. Biol. 282, 653-666.
17. van Mierlo, C. P., and Steensma, E. (2000) Protein folding and stability investigated by fluorescence, circular dichroism (CD), and nuclear magnetic resonance (NMR) spectroscopy: the flavodoxin story, J. Biotechnol. 79, 281-298.
18. van Mierlo, C. P., van Dongen, W. M., Vergeldt, F., van Berkel, W. J., and Steensma, E. (1998) The equilibrium unfolding of Azotobacter vinelandii apoflavodoxin II occurs via a relatively stable folding intermediate, Protein Sci. 7, 2331-2344.
19. Irun, M. P., Garcia-Mira, M. M., Sanchez-Ruiz, J. M., and Sancho, J. (2001) Native hydrogen bonds in a molten globule: the apoflavodoxin thermal intermediate, J. Mol. Biol. 306, 877-888.
20. Genzor, C. G., Beldarrain, A., Gomez-Moreno, C., Lopez-Lacomba, J. L., Cortijo, M., and Sancho, J. (1996) Conformational stability of apoflavodoxin, Protein Sci. 5, 1376-1388.
21. Apiyo, D., and Wittung-Stafshede, P. (2002) Presence of the cofactor speeds up folding of Desulfovibrio desulfuricans flavodoxin, Protein Sci. 11, 1129-1135.
22. Apiyo, D., Guidry, J., and Wittung-Stafshede, P. (2000) No cofactor effect on equilibrium unfolding of Desulfovibrio desulfuricans flavodoxin, Biochim. Biophys. Acta 1479, 214-224.
23. Nuallain, B. O., and Mayhew, S. G. (2002) A comparison of the urea-induced unfolding of apoflavodoxin and flavodoxin from Desulfovibrio vulgaris, Eur. J. Biochem. 269, 212-223.
24. Helms, L. R., and Swenson, R. P. (1991) Cloning and characterization of the flavodoxin gene from Desulfovibrio desulfuricans, Biochim. Biophys. Acta 1089, 417-419.
25. Caldeira, J., Palma, P. N., Regalla, M., Lampreia, J., Calvete, J., Schafer, W., Legall, J., Moura, I., and Moura, J. J. (1994) Primary sequence, oxidation-reduction potentials and tertiary-structure prediction of Desulfovibrio desulfuricans ATCC 27774 flavodoxin, Eur. J. Biochem. 220, 987-995.
26. Romero, A., Caldeira, J., Legall, J., Moura, I., Moura, J. J., and Romao, M. J. (1996) Crystal structure of flavodoxin from Desulfovibrio desulfuricans ATCC 27774 in two oxidation states, Eur. J. Biochem. 239, 190-196.
27. Muralidhara, B. K., and Wittung-Stafshede, P. (2003) Can cofactor-binding sites in proteins be flexible? Desulfovibrio desulfuricans flavodoxin binds FMN dimer, Biochemistry 42, 13074-13080.
28. Luo, J., Iwakura, M., and Matthews, C. R. (1995) Detection of a stable intermediate in the thermal unfolding of a cysteine-free form of dihydrofolate reductase from Escherichia coli, Biochemistry 34, 10669-10675.
29. Privalov, P. (1997) Thermodynamics of protein folding, J. Chem. Thermodyn. 29, 447-474.
30. Privalov, P. L., and Potekhin, S. A. (1986) Scanning microcalorimetry in studying temperature-induced changes in proteins, Methods Enzymol. 131, 4-51.
31. Lopez, M. M., and Makhatadze, G. I. (2002) Isothermal titration calorimetry, Methods Mol. Biol. 173, 121-126.
32. Robinson, C. R., Liu, Y., Thomson, J. A., Sturtevant, J. M., and Sligar, S. G. (1997) Energetics of heme binding to native and denatured states of cytochrome b562, Biochemistry 36, 16141-16146.
33. Bertini, I., Cowan, J. A., Luchinat, C., Natarajan, K., and Piccioli, M. (1997) Characterization of a partially unfolded high potential iron protein, Biochemistry 36, 9332-9339.
34. Leckner, J., Bonander, N., Wittung-Stafshede, P., Malmstrom, B. G., and Karlsson, B. G. (1997) The effect of the metal ion on the folding energetics of azurin: a comparison of the native, zinc and apoprotein, Biochim. Biophys. Acta 1342, 19-27.
35. Goedken, E. R., Keck, J. L., Berger, J. M., and Marqusee, S. (2000) Divalent metal cofactor binding in the kinetic folding trajectory of Escherichia coli ribonuclease HI, Protein Sci. 9, 1914-1921.
36. Filimonov, V. V., Prieto, J., Martinez, J. C., Bruix, M., Mateo, P. L., and Serrano, L. (1993) Thermodynamic analysis of the chemotactic protein from Escherichia coli, CheY, Biochemistry 32, 12906-12921.
37. Fernandez-Recio, J., Genzor, C. G., and Sancho, J. (2001) Apoflavodoxin folding mechanism: an alpha/beta protein with an essentially off-pathway intermediate, Biochemistry 40, 15234-15245.