NMR structure of Escherichia coli glutaredoxin 3-glutathione mixed disulfide complex: Implications for the enzymatic mechanism

Journal of Molecular Biology

Volumn 286, Issue 2, 1999, Pages 541-552

  Nordstrand, Kerstin ^b   Åslund, Fredrik ^a   Holmgren, Arne ^a   Otting, Gottfried ^b   Berndt, Kurt D ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NONE

Author keywords

Glutaredoxin; Glutathione; NMR structure; Thiol disulfide oxidoreductase; Thioredoxin superfamily

Indexed keywords

GLUTATHIONE;

ARTICLE; BINDING SITE; CONTROLLED STUDY; ENZYME MECHANISM; ESCHERICHIA COLI; HYDROGEN BOND; LIGAND BINDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY;

EID: 0033582607     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2444     Document Type: Article

References (65)

1. 15N with sidechain Hβ resonances in larger proteins. J. Magn. Reson. 95:1991;636-641.
2. Åslund F., Ehn B., Miranda-Vizuete A., Pueyo C., Holmgren A. Two additional glutaredoxins exist in Escherichia coli: glutaredoxin 3 is a hydrogen donor for ribonucleotide reductase in a thioredoxin/glutaredoxin 1 double mutant. Proc. Natl Acad. Sci. USA. 91:1994;9813-9817.
3. 15N NMR assignments, and structural analysis. J. Biol. Chem. 271:1996;6736-6745.
4. Åslund F., Berndt K. D., Holmgren A. Redox potentials of glutaredoxins and other thiol-disulfide oxidoreductases of the thioredoxin superfamily determined by direct protein-protein redox equilibria. J. Biol. Chem. 272:1997;30780-30786.
5. Aue W. P., Bartholdi E., Ernst R. R. Two-dimensional spectroscopy. Application to nuclear magnetic resonance. J. Chem. Phys. 64:1976;2229-2246.
6. Bandyopadhyay S., Starke D. W., Mieyal J. J., Gronostajski R. M. Thioltransferase (glutaredoxin) reactivates the DNA-binding activity of oxidation-inactivated nuclear factor I. J. Biol. Chem. 273:1998;392-397.
7. Benesch R. E., Benesch R. The acid strength of the -SH group in cysteine and related compounds. J. Am. Chem. Soc. 77:1955;5877-5881.
8. Lexpression system and properties of a novel elongated form. Protein Expr. Purif. 2:1991;287-295.
9. Brändén C. I., Tooze J. Introduction to Protein Structure. 1991;Garland Publishing, Inc. New York.
10. 1H NMR spectra in proteins. J. Magn. Reson. 77:1988;166-169.
11. Bushweller J. H., Åslund F., Wüthrich K., Holmgren A. Structural and functional characterization of the mutant Escherichia coli glutaredoxin (C14S) and its mixed disulfide with glutathione. Biochemistry. 31:1992;9288-9293.
12. Bushweller J. H., Billeter M., Holmgren A., Wüthrich K. The nuclear magnetic resonance solution structure of the mixed disulfide between Escherichia coli glutaredoxin(C14S) and glutathione. J. Mol. Biol. 235:1994;1585-1597.
13. Chivers P. T., Raines R. T. General acid/base catalysis in the active site of Escherichia coli thioredoxin. Biochemistry. 36:1997;15810-15816.
14. Cotgreave I. A., Gerdes R. G. Recent trends in glutathione biochemistry - glutathione-protein interactions-a molecular link between oxidative stress and cell proliferation. Biochem. Biophys. Res. Commun. 242:1998;1-9.
15. Davis D. A., Newcomb F. M., Starke D. W., Ott D. E., Mieyal J. J., Yarchoan R. Thioltransferase (glutaredoxin) is detected within HIV-1 and can regulate the activity of glutathionylated HIV-1 protease in vitro. J. Biol. Chem. 272:1997;25935-25940.
16. Dirr H., Reinemer P., Huber R. X-ray crystal structures of cytosolic glutathione S-transferases. Implications for protein architecture, substrate recognition and catalytic function. Eur. J. Biochem. 220:1994;645-661.
17. Doublié S., Tabor S., Long A. M., Richardson C. C., Ellenberger T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature. 391:1998;251-258.
18. Dyson H. J., Jeng M. F., Tennant L. L., Slaby I., Lindell M., Cui D. S., Kuprin S., Holmgren A. 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. 36:1997;2622-2636.
19. Eklund H., Cambillau C., Sjöberg B. M., Holmgren A., Jörnvall H., Höög J. O., Brändén C. I. Conformational and functional similarities between glutaredoxin and thioredoxins. EMBO J. 3:1984;1443-1449.
20. Gilbert H. F. Redox control of enzyme activities by thiol/disulfide exchange. Methods Enzymol. 107:1984;330-351.
21. Gill S. C., von Hippel P. H. Calculation of protein extinction coefficients from amino acid sequence data. Anal. Biochem. 182:1989;319-326.
22. Gravina S. A., Mieyal J. J. Thioltransferase is a specific glutathionyl mixed disulfide oxidoreductase. Biochemistry. 32:1993;3368-3376.
23. Güntert P., Qian Y. Q., Otting G., Müller M., Gehring W., Wüthrich K. Structure determination of the Antp(C39-S) homeodomain from nuclear magnetic resonance data in solution using a novel strategy for the structure calculation with the programs DIANA, CALIBA, HABAS and GLOMSA. J. Mol. Biol. 217:1991;531-540.
24. Güntert P., Mumenthaler C., Wüthrich K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 273:1997;283-298.
25. Holmgren A. Hydrogen donor system for Escherichia coli ribonucleoside-diphosphate reductase dependent upon glutathione. Proc. Natl Acad. Sci. USA. 73:1976;2275-2279.
26. Holmgren A. Glutathione-dependent enzyme reactions of the phage T4 ribonucleotide reductase system. J. Biol. Chem. 253:1978;7424-7430.
27. Holmgren A. Glutathione-dependent synthesis of deoxyribonucleotides. Characterization of the enzymatic mechanism of Escherichia coli glutaredoxin. J. Biol. Chem. 254:1979a;3672-3678.
28. Holmgren A. Glutathione-dependent synthesis of deoxyribonucleotides. Purification and characterization of glutaredoxin fromEscherichia coli. J. Biol. Chem. 254:1979b;3664-3671.
29. Holmgren A. Thioredoxin. Annu. Rev. Biochem. 54:1985;237-271.
30. Holmgren A. Thioredoxin and glutaredoxin systems. J. Biol. Chem. 264:1989;13963-13966.
31. Holmgren A., Åslund F. Glutaredoxin. Methods Enzymol. 252:1995;283-292.
32. Höög J. O., Jörnvall H., Holmgren A., Carlquist M., Persson M. The primary structure of Escherichia coli glutaredoxin. Distant homology with thioredoxins in a superfamily of small proteins with a redox-active cystine disulfide/cysteine dithiol. Eur. J. Biochem. 136:1983;223-232.
33. Hutchinson E. G., Thornton J. M. PROMOTIF-a program to identify and analyze structural motifs in proteins. Protein Sci. 5:1996;212-220.
34. Kabsch W., Sander C. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers. 22:1983;2577-2637.
35. Katti S. K., Robbins A. H., Yang Y., Wells W. W. Crystal structure of thioltransferase at 2.2 Å resolution. Protein Sci. 4:1995;1998-2005.
36. Katz B. A. Structural and mechanistic determinants of affinity and specificity of ligands discovered or engineered by phage display. Annu. Rev. Biophys. Biomol. Struct. 26:1997;27-45.
37. Koradi R., Billeter M., Wüthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. Model. 14:1996;51-55.
38. Laskowski R. A., Rullmann J. A., MacArthur M. W., Kaptein R., Thornton J. M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR. 8:1996;477-486.
39. LeMaster D. M., Springer P. A., Unkefer C. J. The role of the buried aspartate of Escherichia coli thioredoxin in the activation of the mixed disulfide intermediate. J. Biol. Chem. 272:1997;29998-30001.
40. Lundström-Ljung J., Holmgren A. Glutaredoxin accelerates glutathione-dependent folding of reduced ribonuclease A together with protein disulfide-isomerase. J. Biol. Chem. 270:1995;7822-7828.
41. Martin J. L. Thioredoxin: a fold for all reasons. Structure. 3:1995;245-250.
42. McFarlan S. C., Terrell C. A., Hogenkamp H. P. The purification, characterization, and primary structure of a small redox protein from Methanobacterium thermoautotrophicum, an archaebacterium. J. Biol. Chem. 267:1992;10561-10569.
43. Milner-White E. J. Recurring loop motif in proteins that occurs in right-handed and left-handed forms. Its relationship with alpha-helices and beta-bulge loops. J. Mol. Biol. 199:1988;503-511.
44. Mueller L. P. E. COSY, a simple alternative to E. COSY. J. Magn. Reson. 72:1987;191-196.
45. Nikkola M., Gleason F. K., Saarinen M., Joelson T., Björnberg O., Eklund H. A putative glutathione-binding site in T4 glutaredoxin investigated by site-directed mutagenesis. J. Biol. Chem. 266:1991;16105-16112.
46. Otting G., Orbons L. P. M., Wüthrich K. Suppression of zero-quantum coherence in NOESY and soft-NOESY. J. Magn. Reson. 89:1990;423-430.
47. Padilla C. A., Martínez-Galisteo E., Bárcena J. A., Spyrou G., Holmgren A. Purification from placenta, amino acid sequence, structure comparisons and cDNA cloning of human glutaredoxin. Eur. J. Biochem. 227:1995;27-34.
48. Qin J., Clore G. M., Kennedy W. M., Huth J. R., Gronenborn A. M. Solution structure of human thioredoxin in a mixed disulfide intermediate complex with its target peptide from the transcription factor NFκB. Structure. 3:1995;289-297.
49. Qin J., Clore G. M., Kennedy W. P., Kuszewski J., Gronenborn A. M. The solution structure of human thioredoxin complexed with its target from Ref-1 reveals peptide chain reversal. Structure. 4:1996;613-620.
50. Rance M., Bodenhausen G., Wagner G., Wüthrich K., Ernst R. R. A systematic approach to the suppression of J cross-peaks in 2D exchange and 2D NOE spectroscopy. J. Magn. Reson. 62:1985;497-510.
51. Sinning I., Kleywegt G. J., Cowan S. W., Reinemer P., Dirr H. W., Huber R., Gilliland G. L., Armstrong R. N., Ji X., Board P. G., Olin B., Mannervik B., Jones T. A. Structure determination and refinement of human alpha class glutathione transferase A1-1, and a comparison with the Mu and Pi class enzymes. J. Mol. Biol. 232:1993;192-212.
52. Sjöberg B. M., Holmgren A. Studies on the structure of T4 thioredoxin. II. Amino acid sequence of the protein and comparison with thioredoxin fromEscherichia coli. J. Biol. Chem. 247:1972;8063-8068.
53. 1H N.M.R. assignments and determination of the three-dimensional structure of reducedEscherichia coli glutaredoxin. J. Mol. Biol. 221:1991;1311-1324.
54. Söderberg B. O., Sjöberg B. M., Sonnerstam U., Brändén C. I. Three-dimensional structure of thioredoxin induced by bacteriophage T4. Proc. Natl Acad. Sci. USA. 75:1978;5827-5830.
55. Srinivasan U., Mieyal P. A., Mieyal J. J. pH profiles indicative of rate-limiting nucleophilic displacement in thioltransferase catalysis. Biochemistry. 36:1997;3199-3206.
56. 15N NMR resonance assignments and secondary structure of human glutaredoxin in the fully reduced form. Protein Sci. 6:1997;383-390.
57. Sun C. H., Berardi M. J., Bushweller J. H. The NMR solution structure of human glutaredoxin in the fully reduced form. J. Mol. Biol. 280:1998;687-701.
58. Szajewski R. P., Whitesides G. M. Rate constants and equilibrium constants for thiol-disulfide interchange reactions involving oxidized glutathione. J. Am. Chem. Soc. 102:1980;2011-2026.
59. Szyperski T., Güntert P., Otting G., Wüthrich K. Determination of scalar coupling constants by inverse Fourier transformation of in-phase multiplets. J. Magn. Reson. 99:1992;552-560.
60. Talluri S., Wagner G. An optimized 3D NOESY-HSQC. J. Magn. Reson. sect. B. 112:1996;200-205.
61. Vlamis-Gardikas A., Åslund F., Spyrou G., Bergman T., Holmgren A. Cloning, overexpression, and characterization of glutaredoxin 2, an atypical glutaredoxin from Escherichia coli. J. Biol. Chem. 272:1997;11236-11243.
62. Widersten M., Björnestedt R., Mannervik B. Involvement of the carboxyl groups of glutathione in the catalytic mechanism of human glutathione transferase A1-1. Biochemistry. 35:1996;7731-7742.
63. Xia T. H., Bushweller J. H., Sodano P., Billeter M., Björnberg O., Holmgren A., Wüthrich K. NMR structure of oxidized Escherichia coli glutaredoxin: comparison with reduced E. coli glutaredoxin and functionally related proteins. Protein Sci. 1:1992;310-321.
64. Yang Y. F., Gan Z. R., Wells W. W. Cloning and sequencing the cDNA encoding pig liver thioltransferase. Gene. 83:1989;339-346.
65. 13C N.M.R. Int. J. Pept. Protein Res. 29:1987;638-646.