Probing the equilibrium unfolding of ketosteroid isomerase through xenon-perturbed 1H–15N multidimensional NMR spectroscopy

Binkowski TA, Naghibzadeh S, Liang J (2003) CASTp: computed atlas of surface topography of proteins. Nucleic Acids Res 31:3352–3355 Blobel J, Schmidl S, Vidal D, Nisius L, Bernado P, Millet O, Brunner E, Pons M (2007) Protein tyrosine phosphatase oligomerization studied by a combination of 15N NMR relaxation and 129Xe NMR. Effect of buffer containing arginine and glutamic acid. J Am Chem Soc 129:5946–5953 Burgering MJ, Hald M, Boelens R, Breg JN, Kaptein R (1995) Hydrogen exchange studies of the Arc repressor: evidence for a monomeric folding intermediate. Biopolymers 35:217–226 Dubois L, Da Silva P, Landon C, Huber JG, Ponchet M, Vovelle F, Berthault P, Desvaux H (2004) Probing the hydrophobic cavity of lipid transfer protein from Nicotiana tabacum through xenon-based NMR spectroscopy. J Am Chem Soc 126:15738–15746 Gloss LM, Mathews CR (1997) Urea and thermal equilibrium denaturation studies on the dimerization domain of Escherichia coli Trp repressor. Biochemistry 36:5612–5623 Gröger C, Moglich A, Pons M, Koch B, Hengstenberg W, Kalbitzer HR, Brunner E (2003) NMR-spectroscopic mapping of an engineered cavity in the I14A mutant of HPr from Staphylococcus carnosus using xenon. J Am Chem Soc 125:8726–8727 Ha NC, Choi G, Choi KY, Oh BH (2001) Structure and enzymology of Δ5-3-ketosteroid isomerase. Curr Opin Struct Biol 11:674–678 Jang DS, Lee HJ, Lee B, Hong BH, Cha HJ, Yoon J, Lim K, Yoon YJ, Kim J, Ree M, Lee HC, Choi KY (2006) Detection of an intermediate during the unfolding process of the dimeric ketosteroid isomerase. FEBS Lett 580:4166–4171 Kay LE, Keifer P, Saarinen T (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J Am Chem Soc 114:10663–10665 Kim DH, Nam GH, Jang DS, Yun S, Choi G, Lee HC, Choi KY (2001) Roles of dimerization in folding and stability of ketosteroid isomerase from Pseudomonas putida biotype B. Protein Sci 10:741–752 Kim SW, Cha SS, Cho HS, Kim JS, Ha NC, Cho MJ, Joo S, Kim KK, Choi KY, Oh BH (1997) High-resolution crystal structures of Δ5-3-ketosteroid isomerase with and without a reaction intermediate analogue. Biochemistry 36:14030–14036 Korzhnev DM, Bezsonova I, Evanics F, Taulier N, Zhou Z, Bai Y, Chalikian TV, Prosser RS, Kay LE (2006) Probing the transition state ensemble of a protein folding reaction by pressure-dependent NMR relaxation dispersion. J Am Chem Soc 128:5262–5269 Kumar A, Srivastava S, Kumar Mishra R, Mittal R, Hosur RV (2006) Residue-level NMR view of the urea-driven equilibrium folding transition of SUMO-1 (1–97): native preferences do not increase monotonously. J Mol Biol 361:180–194 Lowery TJ, Doucleff M, Ruiz EJ, Rubin SM, Pines A, Wemmer DE (2005) Distinguishing multiple Chemotaxis Y protein conformations with laser-polarized 129Xe NMR. Protein Sci 14:848–855 Mallam AL, Jackson SE (2006) Probing nature’s knots: the folding pathway of a knotted homodimeric protein. J Mol Biol 359:1420–1436 Marion D, Driscoll PC, Kay LE, Wingfield PT, Bax A, Gronenborn AM, Clore GM (1989) Overcoming the overlap problem in the assignment of 1H NMR spectra of larger proteins by use of three-dimensional heteronuclear 1H-15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: application to interleukin 1β. Biochemistry 28:6150–6156 Miranker AD, Dobson CM (1996) Collapse and cooperativity in protein folding. Curr Opin Struct Biol 6:31–42 Pervushin K, Riek R, Wider G, Wuthrich K (1997) Attenuated T 2 relaxation by mutual cancellation of dipole–dipole coupling and chemical shift anisotropy indicates an avenue to NMR structures of very large biological macromolecules in solution Proc Natl Acad Sci USA 94:12366–12371 Piotto M, Saudek V, Sklenar V (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR 2:661–665 Pollack RM (2004) Enzymatic mechanisms for catalysis of enolization: ketosteroid isomerase. Bioorg Chem 32:341–353 Pollack RM, Thornburg LD, Wu ZR, Summers MF (1999) Mechanistic insights from the three-dimensional structure of 3-oxo-Δ5-steroid isomerase. Arch Biochem Biophys 370:9–15 Quillin ML, Breyer WA, Griswold IJ, Matthews BW (2000) Size versus polarizability in protein-ligand interactions: binding of noble gases within engineered cavities in phage T4 lysozyme. J Mol Biol 302:955–977 Rubin SM, Lee SY, Ruiz EJ, Pines A, Wemmer DE (2002) Detection and characterization of xenon-binding sites in proteins by 129Xe NMR spectroscopy. J Mol Biol 322:425–440 Rubin SM, Spence MM, Dimitrov IE, Ruiz EJ, Pines A, Wemmer DE (2001) Detection of a conformational change in maltose binding protein by 129Xe NMR spectroscopy. J Am Chem Soc 123:8616–8617 Sklenar V, Piotto M, Leppik R, Saudek V (1993) Gradient-tailored water suppression for 1H-15N HSQC experiments optimized to retain full sensitivity. J Magn Reson A 102:241–245 Tang Y, Grey MJ, McKnight J, Palmer AG 3rd, Raleigh DP (2006) Multistate folding of the villin headpiece domain. J Mol Biol 355:1066–1077 Tanner JW, Johansson JS, Liebman PA, Eckenhoff RG (2001) Predictability of weak binding from X-ray crystallography: inhaled anesthetics and myoglobin. Biochemistry 40:5075–5080 Tilton RF Jr, Kuntz ID Jr, Petsko GA (1984) Cavities in proteins: structure of a metmyoglobin-xenon complex solved to 1.9 Å. Biochemistry 23:2849–2857 Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ, Oldfield E, Markley JL, Sykes BD (1995) 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 6:135–140 Zeeb M, Lipps G, Lilie H, Balbach J (2004) Folding and association of an extremely stable dimeric protein from Sulfolobus islandicus. J Mol Biol 336:227–240 Zhao Q, Abeygunawardana C, Mildvan AS (1997) NMR studies of the secondary structure in solution and the steroid binding site of Δ5–3-ketosteroid isomerase in complexes with diamagnetic and paramagnetic steroids. Biochemistry 36:3458–3472