Thermodynamic and kinetic characterization of the association of triosephosphate isomerase: The role of diffusion

Kramers, 1940, Brownian motion in a field of force and the diffusion model of chemical reactions, Physica, 7, 284, 10.1016/S0031-8914(40)90098-2 Karplus, 1994, Protein folding dynamics: the diffusion-collision model and experimental data, Protein Sci., 3, 650, 10.1002/pro.5560030413 Tsong, 1978, Effects of solvent viscosity and different guanidine salts on the kinetics of ribonuclease A chain folding, Biopolymers, 17, 1669, 10.1002/bip.1978.360170705 Tsong, 1982, Viscosity-dependent conformational relaxation of ribonuclease A in the thermal unfolding zone, Biochemistry, 21, 1493, 10.1021/bi00536a005 Teschner, 1987, Intermediates on the folding pathway of octopine dehydrogenase from Pecten jacobeus, Biochemistry, 26, 2791, 10.1021/bi00384a021 Vaucheret, 1987, Mechanism of renaturation of a large protein, aspartokinase-homoserine dehydrogenase, Biochemistry, 26, 2785, 10.1021/bi00384a020 Creighton, 1997, Protein folding: does diffusion determine the folding rate?, Curr. Biol., 7, R380, 10.1016/S0960-9822(06)00180-1 Gekko, 1981, Thermodynamic and kinetic examination of protein stabilization by glycerol, Biochemistry, 20, 4677, 10.1021/bi00519a024 Gekko, 1981, Mechanism of protein stabilization by glycerol: preferential hydration in glycerol–water mixtures, Biochemistry, 20, 4667, 10.1021/bi00519a023 Zancan, 2005, Trehalose and glycerol stabilize and renature yeast inorganic pyrophosphatase inactivated by very high temperatures, Arch. Biochem. Biophys., 444, 52, 10.1016/j.abb.2005.09.014 Hurle, 1987, Characterization of a slow folding reaction for the α subunit of tryptophan synthase, Proteins: Struc. Func. Gen., 2, 54, 10.1002/prot.340020107 Chrunyk, 1990, Role of diffusion in the folding of the α subunit of tryptophan synthase from Escherichia coli, Biochemistry, 29, 2149, 10.1021/bi00460a027 Jacob, 1997, Diffusion control in an elementary protein folding reaction, Proc. Natl. Acad. Sci. U. S. A., 94, 5622, 10.1073/pnas.94.11.5622 Plaxco, 1998, Limited internal friction in the rate-limiting step of a two-state protein folding reaction, Proc. Natl. Acad. Sci. U. S. A., 95, 13591, 10.1073/pnas.95.23.13591 Bhattacharyya, 1999, Viscosity dependence of the folding kinetics of a dimeric and monomeric coiled coil, Biochemistry, 38, 2601, 10.1021/bi982209j Tollinger, 2006, Characterization of the hydrodynamic properties of the folding transition state of an SH3 domain by magnetization transfer NMR spectroscopy, Biochemistry, 45, 6434, 10.1021/bi060268o Ladurner, 1999, Upper limit of the time scale for diffusion and chain collapse in chymotrypsin inhibitor 2, Nat. Struct. Biol., 6, 28, 10.1038/4899 Silow, 2003, High concentrations of viscogens decrease the protein folding rate constant by prematurely collapsing the coil, J. Mol. Biol., 326, 263, 10.1016/S0022-2836(02)01331-1 Jacob, 1999, Diffusional barrier crossing in a two-state protein folding reaction, Nat. Struct. Biol., 6, 923, 10.1038/13289 Gabdoulline, 2002, Biomolecular diffusional association, Curr. Opin. Struct. Biol., 12, 204, 10.1016/S0959-440X(02)00311-1 Schreiber, 2002, Kinetic studies of protein–protein interactions, Curr. Opin. Struct. Biol., 12, 41, 10.1016/S0959-440X(02)00287-7 Raman, 1992, Diffusion-limited rates for monoclonal antibody binding to cytochrome c, Biochemistry, 31, 10370, 10.1021/bi00157a027 Stone, 1995, Inhibitory mechanism of serpins. Interaction of thrombin with antithrombin and protease nexin 1, Biochemistry, 34, 5164, 10.1021/bi00015a030 Goldberg, 1998, Kinetic mechanism of a partial folding reaction. 2. Nature of the transition state, Biochemistry, 37, 2556, 10.1021/bi972403q Schreiber, 1996, Rapid, electrostatically assisted association of proteins, Nat. Struct. Biol., 3, 427, 10.1038/nsb0596-427 Waldburgerer, 1996, Barriers to protein folding: formation of buried polar interactions is a slow step in acquisition of structure, Proc. Natl. Acad. Sci. U. S. A., 93, 2629, 10.1073/pnas.93.7.2629 Mateu, 1999, Mechanism of folding and assembly of a small tetrameric protein domain from tumor suppressor p53, Nat. Struct. Biol., 6, 191, 10.1038/5880 Mei, 2005, The importance of being dimeric, FEBS J., 272, 16, 10.1111/j.1432-1033.2004.04407.x Knowles, 1977, Perfection in enzyme catalysis: the energetics of triosephosphate isomerase, Acc. Chem. Res., 10, 105, 10.1021/ar50112a001 Lolis, 1990, Structure of yeast triosephosphate isomerase at 1.9-Å resolution, Biochemistry, 29, 6609, 10.1021/bi00480a009 Knowles, 1991, Enzyme catalysis: not different, just better, Nature (London), 350, 121, 10.1038/350121a0 Rozovsky, 2001, Solution-state NMR investigations of triosephosphate isomerase active site loop motion: ligand release in relation to active site loop dynamics, J. Mol. Biol., 310, 271, 10.1006/jmbi.2001.4673 Jogl, 2003, Optimal alignment for enzymatic proton transfer: structure of the Michaelis complex of triosephosphate isomerase at 1.2 Å resolution, Proc. Natl. Acad. Sci. U. S. A., 100, 50, 10.1073/pnas.0233793100 Xiang, 2004, Entropy effects on protein hinges: the reaction catalyzed by triosephosphate isomerase, Biochemistry, 43, 11436, 10.1021/bi049208d Blacklow, 1988, Triosephosphate isomerase catalysis is diffusion controlled, Biochemistry, 27, 1158, 10.1021/bi00404a013 Waley, 1973, Refolding of triosephosphate isomerase, Biochem. J., 135, 165, 10.1042/bj1350165 Zabori, 1980, Folding and association of triosephosphate isomerase from rabbit muscle, Z. Naturforsch., 35, 999, 10.1515/znc-1980-11-1224 Garza-Ramos, 1992, Dimerization and reactivation of triosephosphate isomerase in reverse micelles, Eur. J. Biochem., 208, 389, 10.1111/j.1432-1033.1992.tb17199.x Fernández-Velasco, 1995, Water requirements in monomer folding and dimerization of triosephosphate isomerase in reverse micelles. Intrinsic fluorescence of conformers related to reactivation, Biochemistry, 34, 361, 10.1021/bi00001a044 Chánez-Cárdenas, 2002, Unfolding of triosephosphate isomerase from Trypanosoma brucei: identification of intermediates and insight into the denaturation pathway using tryptophan mutants, Arch. Biochem. Biophys., 399, 117, 10.1006/abbi.2001.2749 Nájera, 2003, Thermodynamic characterization of yeast triosephosphate isomerase refolding: insights into the interplay between function and stability as reasons for the oligomeric nature of the enzyme, Biochem. J., 370, 785, 10.1042/bj20021439 Chánez-Cárdenas, 2005, Reversible equilibrium unfolding of triosephosphate isomerase from Trypanosoma cruzi in guanidinium hydrochloride involves stable dimeric and monomeric intermediates, Biochemistry, 44, 10883, 10.1021/bi047687a Rodríguez-Romero, 2002, Structure and inactivation of triosephosphate isomerase from Entamoeba histolytica, J. Mol. Biol., 322, 669, 10.1016/S0022-2836(02)00809-4 Borchert, 1994, Design, creation, and characterization of a stable, monomeric triosephosphate isomerase, Proc. Natl. Acad. Sci. U. S. A., 91, 1515, 10.1073/pnas.91.4.1515 Schliebs, 1997, A double mutation at the tip of the dimer interface loop of triosephosphate isomerase generates active monomers with reduced stability, Biochemistry, 36, 9655, 10.1021/bi963086a Saab-Rincón, 2001, Different strategies to recover the activity of monomeric triosephosphate isomerase by directed evolution, Protein Eng., 14, 149, 10.1093/protein/14.3.149 Mainfroid, 1996, Three hTIM mutants that provide new insights on why TIM is a dimer, J. Mol. Biol., 257, 441, 10.1006/jmbi.1996.0174 Rietveld, 1998, Kinetics and energetics of subunit dissociation / unfolding of TIM: the importance of oligomerization for conformational persistence and chemical stability of proteins, Biochemistry, 37, 933, 10.1021/bi9721593 Pan, 2004, Equilibrium and kinetic folding of rabbit muscle triosephosphate isomerase by hydrogen exchange mass spectrometry, J. Mol. Biol., 336, 1251, 10.1016/j.jmb.2003.12.076 Gokhale, 1999, Unfolding of Plasmodium falciparum triosephosphate isomerase in urea and guanidinium chloride: evidence for a novel disulfide exchange reaction in a covalently cross-linked mutant, Biochemistry, 38, 423, 10.1021/bi981087s Lambeir, 2000, The ionization of a buried glutamic acid is thermodynamically linked to the stability of Leishmania mexicana triosephosphate isomerase, Eur. J. Biochem., 267, 2516, 10.1046/j.1432-1327.2000.01254.x Zomosa-Signoret, 2003, Control of the reactivation kinetics of homodimeric triosephosphate isomerase from unfolded monomers, Biochemistry, 42, 3311, 10.1021/bi0206560 Morgan, 2000, A compact monomeric intermediate identified by NMR in the denaturation of dimeric triosephosphate isomerase, J. Mol. Biol., 300, 11, 10.1006/jmbi.2000.3834 Benítez-Cardoza, 2001, Temperature-induced denaturation and renaturation of triosephosphate isomerase from Saccharomyces cerevisiae: evidence of dimerization coupled to refolding of the thermally unfolded protein, Biochemistry, 40, 9049, 10.1021/bi010528w González-Mondragón, 2004, Conserved cysteine 126 in triosephosphate isomerase is required not for enzymatic activity but for proper folding and stability, Biochemistry, 43, 3255, 10.1021/bi036077s Vázquez-Contreras, 2000, Equilibrium unfolding of yeast triosephosphate isomerase: a monomeric intermediate in guanidine–HCl and two-state behaviour in urea, Prot. Peptide Letters, 7, 57 Norton, 1972, Triosephosphate isomerase from Bakers' yeast. Preliminary crystallographic data, Biochemistry, 11, 4435, 10.1021/bi00774a003 Rozacky, 1971, Studies on human triosephosphate isomerase. I. Isolation and properties of the enzyme from erythrocytes, Arch. Biochem. Biophys., 146, 312, 10.1016/S0003-9861(71)80069-3 Plaut, 1972, pH-dependence of the triosephosphate isomerase reaction, Biochem. J., 129, 311, 10.1042/bj1290311 Chien, 1948, Kinetic analysis of irreversible consecutive reactions, J. Am. Chem. Soc., 70, 2256, 10.1021/ja01186a078 Steinfeld, 1989, 21 Silverman, 2002, The equilibrium unfolding pathway of a (β/α)8 barrel, J. Mol. Biol., 240, 184 Eder, 1992, Stable substructures of eightfold βα-barrel proteins: fragment complementation of phosphoribosylanthranilate isomerase, Biochemistry, 31, 3617, 10.1021/bi00129a010 Jasanoff, 1994, Detection of an intermediate in the folding of the (beta alpha)8-barrel N-(5′-phosphoribosyl) anthranilate isomerase from Escherichia coli, Biochemistry, 33, 6350, 10.1021/bi00186a039 Ogasahara, 1994, Unfolding–refolding kinetics of the tryptophan synthase alpha subunit by CD and fluorescence measurements, J. Mol. Biol., 236, 1227, 10.1016/0022-2836(94)90023-X Bertolaet, 1995, Complementation of fragments of triosephosphate isomerase defined by exon boundaries, Biochemistry, 34, 5736, 10.1021/bi00017a005 Saab-Rincón, 1996, Mutagenic and thermodynamic analyses of residual structure in the alpha subunit of tryptophan synthase, Biochemistry, 35, 1988, 10.1021/bi951726o Gualfetti, 1999, The progressive development of structure and stability during the equilibrium folding of the alpha subunit of tryptophan synthase from Escherichia coli, Protein Sci., 8, 1623, 10.1110/ps.8.8.1623 Hocker, 2001, Dissection of a (beta alpha)8-barrel enzyme into two folded halves, Nat. Struct. Biol., 8, 32, 10.1038/83021 Rojsajjakul, 2004, Multi-state unfolding of the alpha subunit of tryptophan synthase, a TIM barrel protein: Insights into the secondary structure of the stable equilibrium intermediates by hydrogen exchange mass spectrometry, J. Mol. Biol., 341, 241, 10.1016/j.jmb.2004.05.062 Shukla, 2004, Folding of beta/alpha-unit scrambled forms of S. cerevisiae triosephosphate isomerase: evidence for autonomy of substructure formation and plasticity of hydrophobic and hydrogen bonding interactions in core of (beta/alpha)8-barrel, Proteins, 55, 548, 10.1002/prot.20066 Akanuma, 2005, Identification and characterization of key substructures involved in the early folding events of a (β/α)8-barrel protein as studied by experimental and computational methods, J. Mol. Biol., 353, 1161, 10.1016/j.jmb.2005.08.070 Pan, 2003, Quaternary structure of aldolase leads to differences in its folding and unfolding intermediates, Biochemistry, 42, 5713, 10.1021/bi027388q Forsyth, 2002, Folding mechanism of indole-3-glycerol phosphate synthase from Sulfolobus solfaticarus: a test of the conservation of folding mechanisms hypothesis in (β/α)8 barrels, J. Mol. Biol., 320, 1119, 10.1016/S0022-2836(02)00557-0 Kuttner, 2005, Separating the contribution of translational and rotational diffusion to protein association, J. Am. Chem. Soc., 127, 15138, 10.1021/ja053681c Gutfreund, 1995, 249 Janin, 1997, The kinetics of protein–protein recognition, Proteins, 28, 153, 10.1002/(SICI)1097-0134(199706)28:2<153::AID-PROT4>3.0.CO;2-G Schlosshauer, 2004, Realistic protein–protein association rates from a simple diffusional model neglecting long-range interactions, free energy barriers, and landscape ruggedness, Protein Sci., 13, 1660, 10.1110/ps.03517304 Berg, 1985, Diffusion-controlled macromolecular interactions, Annu. Rev. Biophys. Biophys. Chem., 14, 131, 10.1146/annurev.bb.14.060185.001023 Ansari, 1992, The role of solvent viscosity in the dynamics of protein conformational changes, Science, 256, 1796, 10.1126/science.1615323