Guanidine hydrochloride- and urea-induced unfolding of Toxoplasma gondii ferredoxin-NADP+ reductase: Stabilization of a functionally inactive holo-intermediate

Journal of Biochemistry

Volumn 145, Issue 6, 2009, Pages 721-731

  Singh, Kulwant ^a   Bhakuni, Vinod ^a  

^a CENTRAL DRUG RESEARCH INSTITUTE   (India)

Author keywords

Flavin adenine dinucleotide; Flavoproteins; Folding unfolding; Holo intermediate; Protein stabilization destabilization

Indexed keywords

FERREDOXIN NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE REDUCTASE; FLAVINE ADENINE NUCLEOTIDE; GUANIDINE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UREA;

ARTICLE; CONTROLLED STUDY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN MODIFICATION; PROTEIN STABILITY; PROTEIN STRUCTURE; TOXOPLASMA GONDII;

ANIMALS; CIRCULAR DICHROISM; FERREDOXIN-NADP REDUCTASE; GUANIDINE; PROTEIN CONFORMATION; PROTEIN FOLDING; SPECTROMETRY, FLUORESCENCE; TEMPERATURE; TOXOPLASMA; UREA;

TOXOPLASMA GONDII;

EID: 67651166675     PISSN: 0021924X     EISSN: 17562651     Source Type: Journal    
DOI: 10.1093/jb/mvp029     Document Type: Article

References (40)

1. Dobson, C.M. and Karplus, M. (1999) The fundamentals of protein folding: bringing together theory and experiment. Curr. Opin. Struct. Biol. 9, 92-101
2. Samuel, D., Kumar, T.K., Balamurugan, K., Lin, W.Y., Chin, D.H., and Yu, C. (2001) Structural events during the refolding of an all β-sheet protein. J. Biol. Chem. 276, 4134-4141
3. Englander, S.W. (2000) Protein folding intermediates and pathways studied by hydrogen exchange. Annu. Rev. Biophys. Biomol. Struct. 29, 213-238
4. Gokhale, R.S., Ray, S.S., Balaram, H., and Balaram, P. (1999) Unfolding of Plasmodium falciparum triosephosphate isomerase in urea and guanidinium chloride: evidence for a novel disulfide exchangereaction in a covalently cross-linked mutant. Biochemistry 38, 423-431 (Pubitemid 29035713)
5. Hornby, J.A., Luo, J.K., Stevens, J.M., Wallace, L.A., Kaplan, W., Armstrong, R.N., and Dirr, H.W. (2000) Equilibrium folding of dimeric class mu glutathione transferases involves a stable monomeric intermediate. Biochemistry 39, 12336-12344 (Pubitemid 30761172)
6. Fersht, A.R. and Daggett, V. (2002) Protein folding and unfolding at atomic resolution. Cell 108, 573-582 (Pubitemid 34260881)
7. Hartl, F.U. (1994) Protein folding. Secrets of a doubledoughnut. Nature 371, 557-559
8. Jaenicke, R. (1999) Stability and folding of domain proteins. Prog. Biophys. Mol. Biol. 71, 155-241
9. Rossmann, M.G. and Argos, P. (1981) Protein folding. Annu. Rev. Biochem. 50, 497-532
10. Carrillo, N. and Ceccarelli, E.A. (2003) Open questions in ferredoxin-NADP+ reductase catalytic mechanism. Eur. J. Biochem. 270, 1900-1915
11. Arakaki, A.K., Ceccarelli, E.A., and Carrillo, N. (1997) Plant-type ferredoxin-NADP + reductases: a basal structural framework and a multiplicity of functions. FASEB J. 11, 133-140
12. Vollmer, M., Thomsen, N., Wiek, S., and Seeber, F. (2001) Apicomplexan parasites possess distinct nuclear-encoded, but apicoplast-localized, plant-type ferredoxin-NADP+ reductase and ferredoxin. J. Biol. Chem. 276, 5483-5490
13. Pandini, V., Caprini, G., Thomsen, N., Aliverti, A., Seeber, F., and Zanetti, G. (2002) Ferredoxin-NADP+ reductase and ferredoxin of the protozoan parasite Toxoplasma gondii interact productively in vitro and in vivo. J. Biol. Chem. 277, 48463-48471
14. Rohrich, R.C., Englert, N., Troschke, K., Reichenberg, A., Hintz, M., Seeber, F., Balconi, E., Aliverti, A., Zanetti, G., Kohler, U., Pfeiffer, M., Beck, E., Jomaa, H., and Wiesner, J. (2005) Reconstitution of an apicoplast-localised electron transfer pathway involved in the isoprenoid biosynthesis of Plasmodium falciparum. FEBS Lett. 579, 6433-6438 (Pubitemid 41612164)
15. Seeber, F., Aliverti, A., and Zanetti, G. (2005) The planttype ferredoxin-NADP+ reductase/ferredoxin redox system as a possible drug target against apicomplexan human parasites. Curr. Pharm. Des. 11, 3159-3172
16. Aliverti, A., Pandini, V., Pennati, A., de Rosa, M., and Zanetti, G. (2008) Structural and functional diversity of ferredoxin-NADP(+) reductases. Arch. Biochem. Biophys. 474, 283-291
17. Karplus, P.A. and Faber, H.R. (2004) Structural aspects of plant ferredoxin: NADP(+) oxidoreductases. Photosynth. Res. 81, 303-315
18. Hanke, G.T., Kurisu, G., Kusunoki, M., and Hase, T. (2004) (eds.) FNR electron transfer complexes: evolutionary refinement of structural interactions. Photosynth. Res. 81, 317-327
19. Shukla, N., Bhatt, A.N., Aliverti, A., Zanetti, G., and Bhakuni, V. (2005) Guanidinium chloride- and urea-induced unfolding of FprA, a mycobacterium NADPH-ferredoxin reductase: stabilization of an apo-protein by GdmCl. FEBS J. 272, 2216-2224 (Pubitemid 40646791)
20. Milani, M., Balconi, E., Aliverti, A., Mastrangelo, E., Seeber, F., Bolognesi, M., and Zanetti, G. (2007) Ferredoxin-NADP+ reductase from Plasmodium falciparum undergoes NADP+-dependent dimerization and inactivation: functional and crystallographic analysis. J. Mol. Biol. 367, 501-513
21. Bednarek, A., Wiek, S., Lingelbach, K., and Seeber, F. (2003) Toxoplasma gondii: analysis of the active site insertion of its ferredoxin-NADP(+)- reductase by peptidespecific antibodies and homology-based modeling. Exp. Parasitol. 103, 68-77
22. Thomsen-Zieger, N., Pandini, V., Caprini, G., Aliverti, A., Cramer, J., Selzer, P.M., Zanetti, G., and Seeber, F. (2004) A single in vivo-selected point mutation in the active center of Toxoplasma gondii ferredoxin-NADP+ reductase leads to an inactive enzyme with greatly enhanced affinity for ferredoxin. FEBS Lett. 576, 375-380 (Pubitemid 39388631)
23. Pandini, V., Caprini, G., Tedeschi, G., Seeber, F., Zanetti, G., and Aliverti, A. (2006) Roles of the speciesspecific subdomain and the N-terminal peptide of Toxoplasma gondii ferredoxin-NADP+ reductase in ferredoxin binding. Biochemistry 45, 3563-3571
24. Singh, K. and Bhakuni, V. (2008) Toxoplasma gondii ferredoxin-NADP(+) reductase: role of ionic interactions in stabilization of native conformation and structural cooperativity. Proteins 71, 1879-1888 (Pubitemid 351732941)
25. Tsuge, H. and Mitsuda, H. (1973) Studies on the molecular complex of flavins. IV. Activity and FAD-fluorescence change caused by the chemical modification of tryptophyl and tyrosyl residues in glucose oxidase. J. Biochem. 73, 199-206
26. Akhtar, M.S., Ahmad, A., and Bhakuni, V. (2002) Guanidinium chloride- and urea-induced unfolding of the dimeric enzyme glucose oxidase. Biochemistry 41, 3819-3827 (Pubitemid 34224697)
27. Lakowicz, J.R. (1983) Principles of Fluoresence Spectroscopy. Plenum Press, New York
28. Das, M. and Dasgupta, D. (1998) Enhancement of transcriptional activity of T7 RNA polymerase by guanidine hydrochloride. FEBS Lett. 427, 337-340 (Pubitemid 28244302)
29. Milano. Spectroscopy 16, 199-206
30. Buchanan, S.K. (1999) Beta-barrel proteins from bacterial outer membranes: structure, function and refolding. Curr. Opin. Struct. Biol. 9, 455-461
31. Wang, L. and Kallenbach, N.R. (1998) Proteolysis as a measure of the free energy difference between cytochrome c and its derivatives. Protein Sci. 7, 2460-2464 (Pubitemid 28506963)
32. Ellison, D., Hinton, J., Hubbard, S.J., and Beynon, R.J. (1995) Limited proteolysis of native proteins: the interaction between avidin and proteinase K. Protein Sci. 4, 1337-1345
33. Mayr, L.M. and Schmid, F.X. (1993) Stabilization of a protein by guanidinium chloride. Biochemistry 32, 7994-7998
34. Makhatadze, G.I., Lopez, M.M., Richardson, J.M. III, and Thomas, S.T. (1998) Anion binding to the ubiquitin molecule. Protein Sci. 7, 689-697
35. Bollen, Y.J., Nabuurs, S.M., van Berkel, W.J., and van Mierlo, C.P. (2005) Last in, first out: the role of cofactor binding in flavodoxin folding. J. Biol. Chem. 280, 7836-7844
36. Maeda, M., Hamada, D., Hosino, M., Onda, Y., Hase, T., and Goto, Y. (2002) Partially folded structure of flavin adenine dinucleotide-depleted ferredoxin-NADP+ reductase with residual NADP+ binding domain. J. Biol. Chem. 277, 17101-17107
37. Lee, Y.H., Tamura, K., Maeda, M., Hoshino, M., Sakurai, K., Takahashi, S., Ikegami, T., Hase, T., and Goto, Y. (2007) Cores and pH-dependent dynamics of ferredoxin-NADP+ reductase revealed by hydrogen/ deuterium exchange. J. Biol. Chem. 282, 5959-5967
38. Bhuyan, A.K. (2002) Protein stabilization by urea and guanidine hydrochloride. Biochemistry 41, 13386-13394
39. Kumar, R., Prabhu, N.P., Yadaiah, M., and Bhuyan, A.K. (2004) Protein stiffening and entropic stabilization in the subdenaturing limit of guanidine hydrochloride. Biophys. J. 87, 2656-2662
40. Brandts, J.F., Hu, C.Q., Lin, L.N., and Mos, M.T. (1989) A simple model for proteins with interacting domains. Applications to scanning calorimetry data. Biochemistry 28, 8588-8596