A single dipeptide sequence modulates the redox properties of a whole enzyme family

Bardwell, 1991, Identification of a protein required for disulfide bond formation in vivo, Cell, 67, 581, 10.1016/0092-8674(91)90532-4 Kamitani, 1992, Identification and characterization of Escherichia coli gene required for the formation of correctly folded alkaline phosphatase, a periplasmic enzyme, EMBO J, 11, 57, 10.1002/j.1460-2075.1992.tb05027.x Akiyama, 1992, In vitro catalysis of oxidative folding of disulfide-bonded proteins by the Escherichia coli dsbA (ppfA) gene product, J. Biol. Chem, 267, 22440, 10.1016/S0021-9258(18)41691-2 Wunderlich, 1993, Bacterial protein disulfide isomerase: efficient catalysis of oxidative protein folding at acidic pH, Biochemistry, 32, 12251, 10.1021/bi00096a039 Zapun, 1994, Effects of DsbA on the disulfide folding of bovine pancreatic trypsin inhibitor and α-lactalbumin, Biochemistry, 33, 5202, 10.1021/bi00183a025 Darby, 1995, Catalytic mechanism of DsbA and its comparison with that of protein disulfide isomerase, Biochemistry, 34, 3576, 10.1021/bi00011a012 Wunderlich, 1995, Efficient catalysis of disulfide formation during protein folding with a single active-site cysteine, J. Mol. Biol, 247, 28, 10.1006/jmbi.1995.0119 Frech, 1996, Preferential binding of unfolded protein to DsbA, EMBO J, 15, 392, 10.1002/j.1460-2075.1996.tb00369.x Frech, 1996, Competition between DsbA-mediated oxidation and conformational folding of RTEM1 β-lactamase, Biochemistry, 35, 11386, 10.1021/bi9608525 Bardwell, 1993, A pathway for disulfide bond formation in vivo, Proc. Natl Acad. Sci. USA, 90, 1038, 10.1073/pnas.90.3.1038 Kishigami, 1995, DsbA-DsbB Interaction through their active site cysteines: evidence from an odd cysteine mutant of DsbA, J. Biol. Chem, 280, 17072, 10.1074/jbc.270.29.17072 Guilhot, 1995, Evidence that the pathway of disulfide bond formation in Escherichia coli involves interactions between the cysteines of DsbA and DsbB, Proc. Natl Acad. Sci. USA, 92, 9895, 10.1073/pnas.92.21.9895 Kishigami, 1996, Roles of cysteine residues of DsbB in its activity to reoxidize DsbA, the protein disulphide bond catalyst of Escherichia coli, Genes Cells, 1, 201, 10.1046/j.1365-2443.1996.d01-233.x Martin, 1993, Crystal structure of the DsbA protein required for disulphide bond formation in vivo, Nature, 365, 464, 10.1038/365464a0 Guddat, 1997, The uncharged surface features surrounding the active site of Escherichia coli DsbA are conserved and are implicated in peptide binding, Protein Sci, 6, 1148, 10.1002/pro.5560060603 Martin, 1995, Thioredoxin -  a fold for all reasons, Structure, 3, 245, 10.1016/S0969-2126(01)00154-X Katti, 1990, Crystal structure of thioredoxin from Escherichia coli at 1.68 å Resolution, J. Mol. Biol, 212, 167, 10.1016/0022-2836(90)90313-B Dyson, 1990, Three-dimensional solution structure of the reduced form of Escherichia coli thioredoxin determined by nuclear magnetic resonance spectroscopy, Biochemistry, 29, 4129, 10.1021/bi00469a016 Sodano, 1991, Sequence-specific 1H n.m.r. assignments and determination of the three-dimensional structure of reduced Escherichia coli glutaredoxin, J. Mol. Biol, 221, 1311, 10.1016/0022-2836(91)90935-Y Forman-Kay, 1991, High-resolution three-dimensional structure of reduced recombinant human thioredoxin in solution, Biochemistry, 30, 2685, 10.1021/bi00224a017 Eklund, 1992, Structure of oxidized bacteriophage T4 glutaredoxin (thioredoxin), J. Mol. Biol, 228, 596, 10.1016/0022-2836(92)90844-A Xia, 1992, NMR structure of oxidized Escherichia coli glutaredoxin: comparison with reduced E. coli glutaredoxin and functionally related proteins, Protein Sci, 1, 310, 10.1002/pro.5560010302 Jeng, 1994, High-resolution solution structures of oxidized and reduced Escherichia coli thioredoxin, Structure, 2, 853, 10.1016/S0969-2126(94)00086-7 Katti, 1995, Crystal structure of thioltransferase at 2.2 å resolution, Protein Sci, 4, 1998, 10.1002/pro.5560041005 Kemmink, 1995, Nuclear magnetic resonance characterization of the N-terminal thioredoxin-like domain of protein disulfide isomerase, Protein Sci, 4, 2587, 10.1002/pro.5560041216 Kemmink, 1996, Structure determination of the N-terminal thioredoxin-like domain of protein disulfide isomerase using multidimensional heteronuclear 13C/15N NMR spectroscopy, Biochemistry, 35, 7684, 10.1021/bi960335m Zapun, 1993, The reactive and destabilizing disulfide bond of DsbA, a protein required for protein disulfide bond formation in vivo, Biochemistry, 32, 5083, 10.1021/bi00070a016 Zapun, 1994, Replacement of the active-site cysteine residue of DsbA, a protein required for disulfide bond formation in vivo, Biochemistry, 33, 1907, 10.1021/bi00173a038 Gilbert, 1990, Molecular and cellular aspects of thiol-disulfide exchange, Adv. Enzymol, 63, 69 Chivers, 1996, The CXXC motif: imperatives for the formation of native disulfide bonds in the cell, EMBO J, 15, 2659, 10.1002/j.1460-2075.1996.tb00626.x Chivers, 1997, The CXXC motif: a rheostat in the active site, Biochemistry, 36, 4061, 10.1021/bi9628580 Mössner, 1997, Characterization of E. coli thioredoxin variants mimicking the active-site of other thiol/disulfide oxidoreductases, Protein Sci. Rost, 1964, Reduction-potential of glutathione, Nature, 201, 185, 10.1038/201185a0 Nelson, 1994, Reactivity and ionization of the active site cysteine residues of DsbA, a protein required for disulfide bond formation in vivo, Biochemistry, 33, 5974, 10.1021/bi00185a039 Grauschopf, 1995, Why is DsbA such an oxidizing disulfide catalyst?, Cell, 83, 947, 10.1016/0092-8674(95)90210-4 Hennecke, 1997, Influence of acidic residues and the kink in the active-site helix on the properties of the disulfide oxidoreductase DsbA, J. Biol. Chem, 272, 189, 10.1074/jbc.272.1.189 Jacobi, 1997, Elimination of all charged residues in the vicinity of the active-site helix of the disulfide oxidoreductase DsbA, J. Biol. Chem, 272, 21692, 10.1074/jbc.272.35.21692 Forman-Kay, 1992, Relationship between electrostatics and redox function in human thioredoxin: characterization of pH titration shifts using two-dimensional homo-  and heteronuclear NMR, Biochemistry, 31, 3442, 10.1021/bi00128a019 Dyson, 1997, Effects of buried charged groups on cysteine thiol ionization and reactivity in Escherichia coli thioredoxin: structural and functional characterization of mutants of Asp 26 and Lys 57, Biochemistry, 36, 2622, 10.1021/bi961801a Kortemme, 1996, Electrostatic interactions in the active site of the N-terminal thioredoxin-like domain of protein disulfide isomerase, Biochemistry, 35, 14503, 10.1021/bi9617724 Gan, 1990, Yeast thioltransferase -  the active site cysteines display differential reactivity, Arch. Biochem. Biophys, 282, 110, 10.1016/0003-9861(90)90093-E Mieyal, 1991, Thioltransferase in human red blood cells: kinetics and equilibrium, Biochemistry, 30, 8883, 10.1021/bi00100a023 Wunderlich, 1993, The redox properties of protein disulfide isomerase (DsbA) of Escherichia coli result from a tense conformation of its oxidized form, J. Mol. Biol, 233, 559, 10.1006/jmbi.1993.1535 Szajewski, 1980, Rate constants and equilibrium constants for thiol-disulfide interchange reactions involving oxidized glutathione, J. Am. Chem. Soc, 102, 2011, 10.1021/ja00526a042 Gane, 1995, A molecular model for the redox potential difference between thioredoxin and DsbA, based on electrostatics calculations, J. Mol. Biol, 249, 376, 10.1006/jmbi.1995.0303 Warwicker, 1996, Calculation of Cys 30 ΔpKa's and oxidising power for DsbA mutants, FEBS Lett, 385, 105, 10.1016/0014-5793(96)00358-4 Guddat, 1997, Structural analysis of three His32 mutants of DsbA: support for an electrostatic role of His32 in DsbA stability, Protein Sci, 6, 1893, 10.1002/pro.5560060910 Krause, 1991, Mimicking the active site of protein disulfide-isomerase by substitution of proline 34 in Escherichia coli thioredoxin, J. Biol. Chem, 266, 9494, 10.1016/S0021-9258(18)92848-6 Holst, 1997, Active site mutations in yeast protein disulfide isomerase cause dithiothreitol sensitivity and a reduced rate of protein folding in the endoplasmic reticulum, J. Cell Biol, 138, 1229, 10.1083/jcb.138.6.1229 Holmgren, 1985, Thioredoxin, Annu. Rev. Biochem, 54, 237, 10.1146/annurev.bi.54.070185.001321 Wunderlich, 1993, Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli, Protein Sci, 2, 717, 10.1002/pro.5560020503 Hennecke, 1997, Quenching of tryptophan fluorescence by the active-site disulfide bridge in the DsbA protein from Escherichia coli, Biochemistry, 36, 6391, 10.1021/bi963017w Kelley, 1987, Equilibrium and kinetic measurements of the conformational transition of reduced thioredoxin, Biochemistry, 26, 1406, 10.1021/bi00379a029 Langsetmo, 1989, Escherichia coli thioredoxin folds into two compact forms of different stability to urea denaturation, Biochemistry, 28, 3211, 10.1021/bi00434a015 Lin, 1989, Urea dependence of thiol-disulfide equilibria in thioredoxin: confirmation of the linkage relationship and a sensitive assay for structure, Biochemistry, 28, 5282, 10.1021/bi00438a054 Pace, 1986, Determination and analysis of urea and guanidine hydrochloride denaturation curves, Methods Enzymol, 131, 266, 10.1016/0076-6879(86)31045-0 Santoro, 1988, Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl α-chymotrypsin using different denaturants, Biochemistry, 27, 8063, 10.1021/bi00421a014 Rossmann, 1997, Replacement of Pro109 by His in TlpA, a thioredoxin-like protein from Bradyrhizobium japonicum, alters its redox properties but not its in vivo functions, FEBS Lett, 406, 249, 10.1016/S0014-5793(97)00270-6 Kortemme, 1995, Ionisation of cysteine residues at the termini of model α-helical peptides. Relevance to unusual thiol pKa values in proteins of the thioredoxin family, J. Mol. Biol, 253, 799, 10.1006/jmbi.1995.0592 Hol, 1985, The role of the α-helix dipole in protein function and structure, Prog. Biophys. Mol. Biol, 45, 149, 10.1016/0079-6107(85)90001-X Šali, 1988, Stabilization of protein structure by interaction of α-helix dipole with a charged side chain, Nature, 335, 740, 10.1038/335740a0 Serrano, 1989, Capping and α-helix stability, Nature, 342, 296, 10.1038/342296a0 Sancho, 1992, Histidine residues at the N-  and C-termini of α-helices: perturbed pKas and protein stability, Biochemistry, 31, 2253, 10.1021/bi00123a006 Walter, 1995, Destabilization of a protein helix by electrostatic interactions, J. Mol. Biol, 252, 133, 10.1006/jmbi.1995.0480 Qin, 1994, The high-resolution three-dimensional structures of the oxidized and reduced states of human thioredoxin, Structure, 2, 503, 10.1016/S0969-2126(00)00051-4 Weichsel, 1996, Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer, Structure, 4, 735, 10.1016/S0969-2126(96)00079-2 Åslund, 1996 Ruddock, 1996, pH-dependence of the dithiol-oxidizing activity of DsbA (a periplasmic protein thiol:disulphide oxidoreductase) and protein disulphide-isomerase: studies with a novel simple peptide substrate, Biochem. J, 315, 1001, 10.1042/bj3151001 Myers, 1995, Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding, Protein Sci, 4, 2138, 10.1002/pro.5560041020 Sambrook, 1989 Kunkel, 1987, Rapid and efficient site-specific mutagenesis without phenotypic selection, Methods Enzymol, 154, 367, 10.1016/0076-6879(87)54085-X Wunderlich, 1993, In vivo control of redox potential during protein folding catalyzed by bacterial protein disulfide-isomerase (DsbA), J. Biol. Chem, 268, 24547, 10.1016/S0021-9258(19)74500-1 Gill, 1989, Calculation of protein extinction coefficients from amino acid sequence data, Anal. Biochem, 182, 319, 10.1016/0003-2697(89)90602-7 Ellman, 1959, Tissue sulfhydryl groups, Arch. Biochem. Biophys, 82, 70, 10.1016/0003-9861(59)90090-6 Loferer, 1995, A bacterial thioredoxin-like protein that is exposed to the periplasm has redox properties comparable with those of cytoplasmic thioredoxins, J. Biol. Chem, 270, 26178, 10.1074/jbc.270.44.26178 Darby, 1995, Characterization of the active site cysteine residues of the thioredoxin-like domains of protein disulfide isomerase, Biochemistry, 34, 16770, 10.1021/bi00051a027 Lundström, 1993, Determination of the reduction-oxidation potential of the thioredoxin-like domains of protein disulfide-isomerase from the equilibrium with glutathione and thioredoxin, Biochemistry, 32, 6649, 10.1021/bi00077a018 O'Donnell, 1983, Proton stoichiometry in the reduction of the FAD and disulfide of Escherichia coli thioredoxin reductase, J. Biol. Chem, 258, 13795, 10.1016/S0021-9258(17)43988-3 Prongay, 1992, Oxidation-reduction properties of Escherichia coli thioredoxin reductase altered at each active site cysteine residue, J. Biol. Chem, 267, 25181, 10.1016/S0021-9258(19)74022-8 Berglund, 1970, A thioredoxin induced by bacterio-phage T4. Purification and characterization, J. Biol. Chem, 245, 6030, 10.1016/S0021-9258(18)62658-4 Gleason, 1992, Mutation of conserved residues in Escherichia coli thioredoxin: effects on stability and function, Protein Sci, 1, 609, 10.1002/pro.5560010507 Koradi, 1996, MOLMOL: a program for display and analysis of macromolecular structures, J. Mol. Graphics, 14, 51, 10.1016/0263-7855(96)00009-4