Thioredoxin A Active-Site Mutants Form Mixed Disulfide Dimers That Resemble Enzyme-Substrate Reaction Intermediates

Journal of Molecular Biology

Volumn 379, Issue 3, 2008, Pages 520-534

  Kouwen, Thijs R H M ^a   Andréll, Juni ^b   Schrijver, Rianne ^a   Dubois, Jean Yves F ^a   Maher, Megan J ^b   Iwata, So ^b   Carpenter, Elisabeth P ^b   van Dijl, Jan Maarten ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Bacillus; dimer; disulfide; structure; thioredoxin

Indexed keywords

CYSTEINE; DIMER; DISULFIDE; HOMODIMER; THIOREDOXIN; THIOREDOXIN A;

AMINO TERMINAL SEQUENCE; ARTICLE; BACILLUS SUBTILIS; CONTROLLED STUDY; DIMERIZATION; ENZYME SUBSTRATE; GRAM POSITIVE BACTERIUM; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PURIFICATION; WILD TYPE; X RAY CRYSTALLOGRAPHY;

BACILLUS SUBTILIS; POSIBACTERIA;

EID: 43449123605     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.03.077     Document Type: Article

References (58)

1. Arner E.S. Holmgren A. Physiological functions of thioredoxin and thioredoxin reductase Eur. J. Biochem. 267 2000 6102 6109
2. Laurent T.C. Moore E.C. Richard P. Enzymatic synthesis of deoxyribonucleotides: IV. Isolation and characterization of thioredoxin, the hydrogen donor from Escherichia coli B J. Biol. Chem. 239 1964 3436 3444
3. Kern R. Malki A. Holmgren A. Richarme G. Chaperone properties of Escherichia coli thioredoxin and thioredoxin reductase Biochem. J. 371 2003 965 972
4. Powis G. Mustacich D. Coon A. The role of the redox protein thioredoxin in cell growth and cancer Free Radic. Biol. Med. 29 2000 312 322
5. Schurmann P. Redox signaling in the chloroplast: the ferredoxin/thioredoxin system Antioxid. Redox Signal. 5 2003 69 78
6. Kumar J.K. Tabor S. Richardson C.C. Proteomic analysis of thioredoxin-targeted proteins in Escherichia coli Proc. Natl Acad. Sci. USA 101 2004 3759 3764
7. Holmgren A. Thioredoxin: 6. The amino acid sequence of the protein from Escherichia coli B Eur. J. Biochem. 6 1968 475 484
8. Holmgren A. Thioredoxin Annu. Rev. Biochem. 54 1985 237 271
9. Kallis G.B. Holmgren A. Differential reactivity of the functional sulfhydryl groups of cysteine-32 and cysteine-35 present in the reduced form of thioredoxin from Escherichia coli J. Biol. Chem. 255 1980 10261 10265
10. Gilbert H.F. Molecular and cellular aspects of thiol–disulfide exchange Adv. Enzymol. Relat. Areas Mol. Biol. 63 1990 69 172
11. Holmgren A. Thioredoxin and glutaredoxin systems J. Biol. Chem. 264 1989 13963 13966
12. Li Y. Hu Y. Zhang X. Xu H. Lescop E. Xia B. Jin C. Conformational fluctuations coupled to the thiol–disulfide transfer between thioredoxin and arsenate reductase in Bacillus subtilis J. Biol. Chem. 282 2007 11078 11083
13. Weichsel A. Gasdaska J.R. Powis G. Montfort W.R. Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer Structure 4 1996 735 751
14. 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 NF kappa B Structure 3 1995 289 297
15. 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
16. Maeda K. Hagglund P. Finnie C. Svensson B. Henriksen A. Structural basis for target protein recognition by the protein disulfide reductase thioredoxin Structure 14 2006 1701 1710
17. Jeng M.F. Campbell A.P. Begley T. Holmgren A. Case D.A. Wright P.E. Dyson H.J. High-resolution solution structures of oxidized and reduced Escherichia coli thioredoxin Structure 2 1994 853 868
18. Katti S.K. LeMaster D.M. Eklund H. Crystal structure of thioredoxin from Escherichia coli at 1.68A resolution J. Mol. Biol. 212 1990 167 184
19. Lennon B.W. Williams C.H. Jr. Ludwig M.L. Twists in catalysis: alternating conformations of Escherichia coli thioredoxin reductase Science 289 2000 1190 1194
20. Dai S. Friemann R. Glauser D.A. Bourquin F. Manieri W. Schurmann P. Eklund H. Structural snapshots along the reaction pathway of ferredoxin–thioredoxin reductase Nature 448 2007 92 96
21. Doublie S. Tabor S. Long A.M. Richardson C.C. Ellenberger T. Crystal structure of a bacteriophage T7 DNA replication complex at 2.2A resolution Nature 391 1998 251 258
22. Kobayashi K. Ehrlich S.D. Albertini A. Amati G. Andersen K.K. Arnaud M. Essential Bacillus subtilis genes Proc. Natl Acad. Sci. USA 100 2003 4678 4683
23. Scharf C. Riethdorf S. Ernst H. Engelmann S. Volker U. Hecker M. Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis J. Bacteriol. 180 1998 1869 1877
24. Smits W.K. Dubois J.Y. Bron S. van Dijl J.M. Kuipers O.P. Tricksy business: transcriptome analysis reveals the involvement of thioredoxin A in redox homeostasis, oxidative stress, sulfur metabolism, and cellular differentiation in Bacillus subtilis J. Bacteriol. 187 2005 3921 3930
25. Holmgren A. Ohlsson I. Grankvist M.L. Thioredoxin from Escherichia coli . Radioimmunological and enzymatic determinations in wild type cells and mutants defective in phage T7 DNA replication J. Biol. Chem. 253 1978 430 436
26. Newton G.L. Arnold K. Price M.S. Sherrill C. Delcardayre S.B. Aharonowitz Y. Distribution of thiols in microorganisms: mycothiol is a major thiol in most actinomycetes J. Bacteriol. 178 1996 1990 1995
27. Prinz W.A. Aslund F. Holmgren A. Beckwith J. The role of the thioredoxin and glutaredoxin pathways in reducing protein disulfide bonds in the Escherichia coli cytoplasm J. Biol. Chem. 272 1997 15661 15667
28. Hisabori T. Hara S. Fujii T. Yamazaki D. Hosoya-Matsuda N. Motohashi K. Thioredoxin affinity chromatography: a useful method for further understanding the thioredoxin network J. Exp. Bot. 56 2005 1463 1468
29. Verdoucq L. Vignols F. Jacquot J.P. Chartier Y. Meyer Y. In vivo characterization of a thioredoxin H target protein defines a new peroxiredoxin family J. Biol. Chem. 274 1999 19714 19722
30. 15N NMR spectra of reduced and oxidized Escherichia coli thioredoxin FEBS Lett. 284 1991 178 183
31. 1H NMR of a C32S,C35S double mutant of Escherichia coli thioredoxin confirms its resemblance to the reduced wild-type protein FEBS Lett. 339 1994 11 17
32. Jeng M.F. Reymond M.T. Tennant L.L. Holmgren A. Dyson H.J. NMR characterization of a single-cysteine mutant of Escherichia coli thioredoxin and a covalent thioredoxin–peptide complex Eur. J. Biochem. 257 1998 299 308
33. Russel M. Model P. The role of thioredoxin in filamentous phage assembly. Construction, isolation, and characterization of mutant thioredoxins J. Biol. Chem. 261 1986 14997 15005
34. Kobayashi T. Kishigami S. Sone M. Inokuchi H. Mogi T. Ito K. Respiratory chain is required to maintain oxidized states of the DsbA–DsbB disulfide bond formation system in aerobically growing Escherichia coli cells Proc. Natl Acad. Sci. USA 94 1997 11857 11862
35. DeLano W.L. The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA, USA
36. Balmer Y. Koller A. del Val G. Manieri W. Schurmann P. Buchanan B.B. Proteomics gives insight into the regulatory function of chloroplast thioredoxins Proc. Natl Acad. Sci. USA 100 2003 370 375
37. Motohashi K. Kondoh A. Stumpp M.T. Hisabori T. Comprehensive survey of proteins targeted by chloroplast thioredoxin Proc. Natl Acad. Sci. USA 98 2001 11224 11229
38. a values of Escherichia coli thioredoxin Biochemistry 36 1997 14985 14991
39. Holmgren A. Thioredoxin structure and mechanism: conformational changes on oxidation of the active-site sulfhydryls to a disulfide Structure 3 1995 239 243
40. Dyson H.J. Jeng M.F. Tennant L.L. Slaby I. Lindell M. Cui D.S. Effects of buried charged groups on cysteine thiol ionization and reactivity in Escherichia coli thioredoxin: structural and functional characterization of mutants of Asp26 and Lys57 Biochemistry 36 1997 2622 2636
41. Jeng M.F. Holmgren A. Dyson H.J. Proton sharing between cysteine thiols in Escherichia coli thioredoxin: implications for the mechanism of protein disulfide reduction Biochemistry 34 1995 10101 10105
42. Ren X. Bjornstedt M. Shen B. Ericson M.L. Holmgren A. Mutagenesis of structural half-cystine residues in human thioredoxin and effects on the regulation of activity by selenodiglutathione Biochemistry 32 1993 9701 9708
43. Andersen J.F. Sanders D.A. Gasdaska J.R. Weichsel A. Powis G. Montfort W.R. Human thioredoxin homodimers: regulation by pH, role of aspartate 60, and crystal structure of the aspartate 60→ asparagine mutant Biochemistry 36 1997 13979 13988
44. Dyson H.J. Gippert G.P. Case D.A. Holmgren A. Wright P.E. Three-dimensional solution structure of the reduced form of Escherichia coli thioredoxin determined by nuclear magnetic resonance spectroscopy Biochemistry 29 1990 4129 4136
45. Holmgren A. Soderberg B.O. Eklund H. Branden C.I. Three-dimensional structure of Escherichia coli thioredoxin-S2 to 2.8A resolution Proc. Natl Acad. Sci. USA 72 1975 2305 2309
46. Holmgren A. Roberts G. Nuclear magnetic resonance studies of redox-induced conformational changes in thioredoxin from Escherichia coli FEBS Lett. 71 1976 261 265
47. Collet J.F. Peisach D. Bardwell J.C. Xu Z. The crystal structure of TrxA(CACA): insights into the formation of a [2Fe–2S] iron-sulfur cluster in an Escherichia coli thioredoxin mutant Protein Sci. 14 2005 1863 1869
48. Hochgrafe F. Mostertz J. Albrecht D. Hecker M. Fluorescence thiol modification assay: oxidatively modified proteins in Bacillus subtilis Mol. Microbiol. 58 2005 409 425
49. Sambrook J. Fritsch E.F. Maniatis T. Molecular Cloning: A Laboratory Manual 1989 Cold Spring Harbor Laboratory Press New York
50. Kunst F. Ogasawara N. Moszer I. Albertini A.M. Alloni G. Azevedo V. The complete genome sequence of the gram-positive bacterium Bacillus subtilis Nature 390 1997 249 256
51. Bron S. Venema G. Ultraviolet inactivation and excision-repair in Bacillus subtilis : I. Construction and characterization of a transformable eightfold auxotrophic strain and two ultraviolet-sensitive derivatives Mutat. Res. 15 1972 1 10
52. Murashima K. Chen C.L. Kosugi A. Tamaru Y. Doi R.H. Wong S.L. Heterologous production of Clostridium cellulovorans engB, using protease-deficient Bacillus subtilis , and preparation of active recombinant cellulosomes J. Bacteriol. 184 2002 76 81
53. Otwinowski Z. Minor W. Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. Part A 276 1997 307 326
54. Read R.J. Pushing the boundaries of molecular replacement with maximum likelihood Acta Crystallogr. Sect. D 57 2001 1373 1382
55. Vagin A.A. Steiner R.A. Lebedev A.A. Potterton L. McNicholas S. Long F. Murshudov G.N. REFMAC5 dictionary: organization of prior chemical knowledge and guidelines for its use Acta Crystallogr. Sect. D 60 2004 2184 2195
56. Perrakis A. Morris R. Lamzin V.S. Automated protein model building combined with iterative structure refinement Nat. Struct. Biol. 6 1999 458 463
57. Emsley P. Cowtan K. Coot: model-building tools for molecular graphics Acta Crystallogr. Sect. D 60 2004 2126 2132
58. Davis I.W. Leaver-Fay A. Chen V.B. Block J.N. Kapral G.J. Wang X. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35 2007 W375 W383