Structure and function of DsbA, a key bacterial oxidative folding catalyst

Antioxidants and Redox Signaling

Volumn 14, Issue 9, 2011, Pages 1729-1760

  Shouldice, Stephen R ^a   Heras, Begoña ^a   Walden, Patricia M ^a   Totsika, Makrina ^a   Schembri, Mark A ^a   Martin, Jennifer L ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; BACTERIAL PROTEIN; BACTERIAL TOXIN; CHAPERONE; DISULFIDE; DITHIOL DERIVATIVE; DSBA PROTEIN; DSBB PROTEIN; INTIMIN; THIOREDOXIN; UNCLASSIFIED DRUG;

BACTERIAL INFECTION; BACTERIAL VIRULENCE; CATALYST; CRYSTAL STRUCTURE; DISULFIDE BOND; ENDOPLASMIC RETICULUM; ESCHERICHIA COLI; FIMBRIA; FLAGELLUM; GAMMAPROTEOBACTERIA; GRAM POSITIVE BACTERIUM; ISOMERIZATION; LIGAND BINDING; MITOCHONDRION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; TYPE III SECRETION SYSTEM;

BACTERIAL PROTEINS; ESCHERICHIA COLI PROTEINS; PROTEIN DISULFIDE-ISOMERASES; PROTEIN STRUCTURE, SECONDARY; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; ESCHERICHIA COLI K12;

EID: 79953784595     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2010.3344     Document Type: Review

References (234)

1. Agudo D, Mendoza MT, Castanares C, Nombela C, and Rotger R. A proteomic approach to study Salmonella typhi periplasmic proteins altered by a lack of the DsbA thiol: Disulfide isomerase. Proteomics 4: 355-363, 2004. (Pubitemid 38235252)
2. Anfinsen CB and Haber E. Studies on the reduction and reformation of protein disulfide bonds. J Biol Chem 236: 1361-1363, 1961.
3. Arner ES. Selenoproteins. What unique properties can arise with selenocysteine in place of cysteine? Exp Cell Res 316: 1296-1303, 2010.
4. Arredondo SA, Chen TF, Riggs AF, Gilbert HF, and Georgiou G. Role of dimerization in the catalytic properties of the Escherichia coli disulfide isomerase DsbC. J Biol Chem 284: 23972-23979, 2009.
5. Aslund F, Berndt KD, and 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: 30780-30786, 1997. (Pubitemid 27527515)
6. Bader M, Muse W, Ballou DP, Gassner C, and Bardwell JC. Oxidative protein folding is driven by the electron transport system. Cell 98: 217-227, 1999. (Pubitemid 29344909)
7. Bader MW, Hiniker A, Regeimbal J, Goldstone D, Haebel PW, Riemer J, Metcalf P, and Bardwell JC. Turning a dis-ulfide isomerase into an oxidase: DsbC mutants that imitate DsbA. EMBO J 20: 1555-1562, 2001. (Pubitemid 32299393)
8. Bader MW, Xie T, Yu CA, and Bardwell JCA. Disulfide bonds are generated by quinone reduction. J Biol Chem 275: 26082-26088, 2000.
9. Balch WE, Morimoto RI, Dillin A, and Kelly JW. Adapting proteostasis for disease intervention. Science 319: 916-919, 2008. (Pubitemid 351263754)
10. Banci L, Bertini I, Cefaro C, Ciofi-Baffoni S, Gallo A, Martinelli M, Sideris DP, Katrakili N, and Tokatlidis K. MIA40 is an oxidoreductase that catalyzes oxidative protein folding in mitochondria. Nat Struct Mol Biol 16: 198-206, 2009.
11. Bardwell JC, Lee JO, Jander G, Martin N, Belin D, and Beckwith J. A pathway for disulfide bond formation in vivo. Proc Natl Acad Sci USA 90: 1038-1042, 1993. (Pubitemid 23053946)
12. Bardwell JC, McGovern K, and Beckwith J. Identification of a protein required for disulfide bond formation in vivo. Cell 67: 581-589, 1991. (Pubitemid 121001472)
13. Barnhart MM, Pinkner JS, Soto GE, Sauer FG, Langermann S, Waksman G, Frieden C, and Hultgren SJ. PapD-like chaperones provide the missing information for folding of pilin proteins. Proc Natl Acad Sci USA 97: 7709-7714, 2000. (Pubitemid 30460712)
14. Basharov MA. Protein folding. J Cell Mol Med 7: 223-237, 2003. (Pubitemid 37372042)
15. Beck MR, DeKoster GT, Hambly DM, Gross ML, Cistola DP, and Goldman WE. Structural features responsible for the biological stability of Histoplasma's virulence factor CBP. Biochemistry 47: 4427-4438, 2008. (Pubitemid 351522092)
16. Beld J, Woycechowsky KJ, and Hilvert D. Small-molecule diselenides catalyze oxidative protein folding in vivo. ACS Chem Biol 5: 177-182, 2010.
17. Berkmen M, Boyd D, and Beckwith J. The nonconsecutive disulfide bond of Escherichia coli phytase (AppA) renders it dependent on the protein-disulfide isomerase, DsbC. J Biol Chem 280: 11387-11394, 2005. (Pubitemid 40418447)
18. Bessette PH, Cotto JJ, Gilbert HF, and Georgiou G. In vivo and in vitro function of the Escherichia coli periplasmic cysteine oxidoreductase DsbG. J Biol Chem 274: 7784-7792, 1999.
19. Bihlmaier K, Mesecke N, Terziyska N, Bien M, Hell K, and Herrmann JM. The disulfide relay system of mitochondria is connected to the respiratory chain. J Cell Biol 179: 389-395, 2007. (Pubitemid 350074784)
20. Bitter W. Secretins of Pseudomonas aeruginosa: Large holes in the outer membrane. Arch Microbiol 179: 307-314, 2003. (Pubitemid 36578029)
21. Blank J, Kupke T, Lowe E, Barth P, Freedman RB, and Ruddock LW. The influence of His94 and Pro149 in modulating the activity of V. cholerae DsbA. Antioxid Redox Signal 5: 359-366, 2003. (Pubitemid 37087394)
22. Bodelon G, Marin E, and Fernandez LA. Role of peri-plasmic chaperones and BamA (YaeT=Omp85) in folding and secretion of intimin from enteropathogenic Escherichia coli strains. J Bacteriol 191: 5169-5179, 2009.
23. Bond CS. TopDraw: A sketchpad for protein structure topology cartoons. Bioinformatics 19: 311-312, 2003. (Pubitemid 36181928)
24. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, and Bartlett J. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 48: 1-12, 2009.
25. Braun P, Ockhuijsen C, Eppens E, Koster M, Bitter W, and Tommassen J. Maturation of Pseudomonas aeruginosa elas-tase. Formation of the disulfide bonds. J Biol Chem 276: 26030-26035, 2001.
26. Bringer MA, Rolhion N, Glasser AL, and Darfeuille-Mi-chaud A. The oxidoreductase DsbA plays a key role in the ability of the Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 to resist macrophage killing. J Bacteriol 189: 4860-4871, 2007. (Pubitemid 47025598)
27. Burall LS, Harro JM, Li X, Lockatell CV, Himpsl SD, Hebel JR, Johnson DE, and Mobley HL. Proteus mirabilis genes that contribute to pathogenesis of urinary tract infection: Identification of 25 signature-tagged mutants attenuated at least 100-fold. Infect Immun 72: 2922-2938, 2004. (Pubitemid 38542423)
28. Carvalho AT, Fernandes PA, Swart M, Van Stralen JN, Bickelhaupt FM, and Ramos MJ. Role of the variable active site residues in the function of thioredoxin family oxido-reductases. J Comput Chem 30: 710-724, 2009.
29. Chacinska A, Pfannschmidt S, Wiedemann N, Kozjak V, Sanjuan Szklarz LK, Schulze-Specking A, Truscott KN, Guiard B, Meisinger C, and Pfanner N. Essential role of Mia40 in import and assembly of mitochondrial inter-membrane space proteins. EMBO J 23: 3735-3746, 2004. (Pubitemid 39389705)
30. Charbonnier JB, Belin P, Moutiez M, Stura EA, and Quemeneur E. On the role of the cis-proline residue in the active site of DsbA. Protein Sci 8: 96-105, 1999. (Pubitemid 29035523)
31. Chen J, Song JL, Zhang S, Wang Y, Cui DF, and Wang CC. Chaperone activity of DsbC. J Biol Chem 274: 19601-19605, 1999.
32. Cho SH, Porat A, Ye J, and Beckwith J. Redox-active cysteines of a membrane electron transporter DsbD show dual compartment accessibility. EMBO J 26: 3509-3520, 2007. (Pubitemid 47236882)
33. Collet JF and Messens J. Structure, function, and mechanism of thioredoxin proteins. Antioxid Redox Signal 13: 1205-1216, 2010.
34. Cornelis GR. The type III secretion injectisome. Nat Rev Microbiol 4: 811-825, 2006. (Pubitemid 44593948)
35. Coulthurst SJ, Lilley KS, Hedley PE, Liu H, Toth IK, and Salmond GP. DsbA plays a critical and multifaceted role in the production of secreted virulence factors by the phyto-pathogen Erwinia carotovora subsp. atroseptica. J Biol Chem 283: 23739-23753, 2008.
36. Couprie J, Vinci F, Dugave C, Quemeneur E, and Moutiez M. Investigation of the DsbA mechanism through the synthesis and analysis of an irreversible enzyme-ligand complex. Biochemistry 39: 6732-6742, 2000. (Pubitemid 30354006)
37. Crow A, Lewin A, Hecht O, Carlsson Moller M, Moore GR, Hederstedt L, and Le Brun NE. Crystal structure and biophysical properties of Bacillus subtilis BdbD. An oxidizing thiol:disulfide oxidoreductase containing a novel metal site. J Biol Chem 284: 23719-23733, 2009.
38. Cumming RC, Andon NL, Haynes PA, Park M, Fischer WH, and Schubert D. Protein disulfide bond formation in the cytoplasm during oxidative stress. J Biol Chem 279: 21749-21758, 2004. (Pubitemid 38679361)
39. Dabir DV, Leverich EP, Kim SK, Tsai FD, Hirasawa M, Knaff DB, and Koehler CM. A role for cytochrome c and cytochrome c peroxidase in electron shuttling from Erv1. EMBO J 26: 4801-4811, 2007. (Pubitemid 350191306)
40. Dacheux D, Epaulard O, de Groot A, Guery B, Leberre R, Attree I, Polack B, and Toussaint B. Activation of the Pseudomonas aeruginosa type III secretion system requires an intact pyruvate dehydrogenase aceAB operon. Infect Immun 70: 3973-3977, 2002. (Pubitemid 34666044)
41. Dailey FE and Berg HC. Mutants in disulfide bond formation that disrupt flagellar assembly in Escherichia coli. Proc Natl Acad Sci USA 90: 1043-1047, 1993. (Pubitemid 23053947)
42. Daniels R, Mellroth P, Bernsel A, Neiers F, Normark S, von Heijne G, and Henriques-Normark B. Disulfide bond formation and cysteine exclusion in gram-positive bacteria. J Biol Chem 285: 3300-3309, 2010.
43. Debarbieux L and Beckwith J. Electron avenue: Pathways of disulfide bond formation and isomerization. Cell 99: 117-119, 1999. (Pubitemid 29491777)
44. Deponte M and Hell K. Disulphide bond formation in the intermembrane space of mitochondria. J Biochem 146: 599-608, 2009.
45. Depuydt M, Leonard SE, Vertommen D, Denoncin K, Morsomme P, Wahni K, Messens J, Carroll KS, and Collet JF. A periplasmic reducing system protects single cysteine residues from oxidation. Science 326: 1109-1111, 2009.
46. Dillet V, Dyson HJ, and Bashford D. Calculations of electrostatic interactions and pKas in the active site of Escher-ichia coli thioredoxin. Biochemistry 37: 10298-10306, 1998. (Pubitemid 28366387)
47. Dobson CM. Protein folding and misfolding. Nature 426: 884-890, 2003. (Pubitemid 38056880)
48. Dorenbos R, Stein T, Kabel J, Bruand C, Bolhuis A, Bron S, Quax WJ, and Van Dijl JM. Thiol-disulfide oxidoreductases are essential for the production of the lantibiotic sublancin 168. J Biol Chem 277: 16682-16688, 2002. (Pubitemid 34967687)
49. Dutton RJ, Boyd D, Berkmen M, and Beckwith J. Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc Natl Acad Sci USA 105: 11933-11938, 2008.
50. Dutton RJ, Wayman A, Wei JR, Rubin EJ, Beckwith J, and Boyd D. Inhibition of bacterial disulfide bond formation by the anticoagulant warfarin. Proc Natl Acad Sci USA 107: 297-301, 2010.
51. Eklund H, Cambillau C, Sjoberg BM, Holmgren A, Jornvall H, Hoog JO, and Branden CI. Conformational and functional similarities between glutaredoxin and thioredoxins. EMBO J 3: 1443-1449, 1984.
52. Eklund H, Ingelman M, Soderberg BO, Uhlin T, Nordlund P, Nikkola M, Sonnerstam U, Joelson T, and Petratos K. Structure of oxidized bacteriophage T4 glutaredoxin (thioredoxin). Refinement of native and mutant proteins. J Mol Biol 228: 596-618, 1992. (Pubitemid 23007578)
53. Ellis LB, Saurugger P, and Woodward C. Identification of the three-dimensional thioredoxin motif: Related structure in the ORF3 protein of the Staphylococcus aureus mer op-eron. Biochemistry 31: 4882-4891, 1992.
54. Emsley P, Lohkamp B, Scott WG, and Cowtan K. Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501, 2010.
55. Endo T, Yamano K, and Kawano S. Structural basis for the disulfide relay system in the mitochondrial intermembrane space. Antioxid Redox Signal 13: 1359-1373, 2010.
56. Fernandes PA and Ramos MJ. Theoretical insights into the mechanism for thiol=disulfide exchange. Chemistry 10: 257-266, 2004.
57. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, Holm L, Sonnhammer EL, Eddy SR, and Bateman A. The Pfam protein families database. Nucleic Acids Res 38: D211-222, 2010.
58. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, Kerlavage AR, Bult CJ, Tomb JF, Dougherty BA, Merrick JM, et al. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496-512, 1995.
59. Fontaine L and Hols P. The inhibitory spectrum of ther-mophilin 9 from Streptococcus thermophilus LMD-9 depends on the production of multiple peptides and the activity of BlpG(St), a thiol-disulfide oxidase. Appl Environ Microbiol 74: 1102-1110, 2008. (Pubitemid 351287081)
60. Frand AR and Kaiser CA. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol Cell 1: 161-170, 1998. (Pubitemid 128378657)
61. Frand AR and Kaiser CA. Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol Cell 4: 469-477, 1999. (Pubitemid 29531127)
62. Frand AR and Kaiser CA. Two pairs of conserved cysteines are required for the oxidative activity of Ero1p in protein disulfide bond formation in the endoplasmic reticulum. Mol Biol Cell 11: 2833-2843, 2000. (Pubitemid 32107068)
63. Frankel G, Phillips AD, Rosenshine I, Dougan G, Kaper JB, and Knutton S. Enteropathogenic and enterohaemorrhagic Escherichia coli: More subversive elements. Mol Microbiol 30: 911-921, 1998. (Pubitemid 28550116)
64. Frech C, Wunderlich M, Glockshuber R, and Schmid FX. Preferential binding of an unfolded protein to DsbA. EMBO J 15: 392-398, 1996. (Pubitemid 26029217)
65. Fuchs S, De Lorenzo F, and Anfinsen CB. Studies on the mechanism of the enzymic catalysis of disulfide interchange in proteins. J Biol Chem 242: 398-402, 1967.
66. Fujita M, Mihara H, Goto S, Esaki N, and Kanehisa M. Mining prokaryotic genomes for unknown amino acids: A stop-codon-based approach. BMC Bioinformatics 8: 225, 2007.
67. Galan JE and Wolf-Watz H. Protein delivery into eu-karyotic cells by type III secretion machines. Nature 444: 567-573, 2006. (Pubitemid 44864429)
68. Garmendia J, Frankel G, and Crepin VF. Enteropathogenic and enterohemorrhagic Escherichia coli infections: Translocation, translocation, translocation. Infect Immun 73: 2573-2585, 2005. (Pubitemid 40570322)
69. Georgescu RE, Li JH, Goldberg ME, Tasayco ML, and Chaffotte AF. Proline isomerization-independent accumulation of an early intermediate and heterogeneity of the folding pathways of a mixed alpha=beta protein, Escherichia coli thioredoxin. Biochemistry 37: 10286-10297, 1998. (Pubitemid 28366386)
70. Goldberger RF, Epstein CJ, and Anfinsen CB. Acceleration of reactivation of reduced bovine pancreatic ribonuclease by a microsomal system from rat liver. J Biol Chem 238: 628-635, 1963.
71. Grauschopf U, Fritz A, and Glockshuber R. Mechanism of the electron transfer catalyst DsbB from Escherichia coli. EMBO J 22: 3503-3513, 2003. (Pubitemid 36898328)
72. Grauschopf U, Winther JR, Korber P, Zander T, Dallinger P, and Bardwell JC. Why is DsbA such an oxidizing dis-ulfide catalyst? Cell 83: 947-955, 1995. (Pubitemid 26006536)
73. Grimshaw JP, Stirnimann CU, Brozzo MS, Malojcic G, Grutter MG, Capitani G, and Glockshuber R. DsbL and DsbI form a specific dithiol oxidase system for periplasmic arylsulfate sulfotransferase in uropathogenic Escherichia coli. J Mol Biol 380: 667-680, 2008.
74. Gross E, Kastner DB, Kaiser CA, and Fass D. Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell. Cell 117: 601-610, 2004. (Pubitemid 38692526)
75. Gross E, Sevier CS, Heldman N, Vitu E, Bentzur M, Kaiser CA, Thorpe C, and Fass D. Generating disulfides enzy-matically: Reaction products and electron acceptors of the endoplasmic reticulum thiol oxidase Ero1p. Proc Natl Acad Sci USA 103: 299-304, 2006. (Pubitemid 43122395)
76. Gross E, Sevier CS, Vala A, Kaiser CA, and Fass D. A new FAD-binding fold and intersubunit disulfide shuttle in the thiol oxidase Erv2p. Nat Struct Biol 9: 61-67, 2002. (Pubitemid 34049182)
77. Gruber CW, Cemazar M, Heras B, Martin JL, and Craik DJ. Protein disulfide isomerase: The structure of oxidative folding. Trends Biochem Sci 31: 455-464, 2006. (Pubitemid 44108657)
78. Guddat LW, Bardwell JC, Glockshuber R, Huber-Wunderlich M, Zander T, and Martin JL. Structural analysis of three His32 mutants of DsbA: Support for an electrostatic role of His32 in DsbA stability. Protein Sci 6: 1893-1900, 1997. (Pubitemid 27391270)
79. Guddat LW, Bardwell JC, and Martin JL. Crystal structures of reduced and oxidized DsbA: Investigation of domain motion and thiolate stabilization. Structure 6: 757-767, 1998. (Pubitemid 28301209)
80. Guddat LW, Bardwell JC, Zander T, and Martin JL. The uncharged surface features surrounding the active site of Escherichia coli DsbA are conserved and are implicated in peptide binding. Protein Sci 6: 1148-1156, 1997. (Pubitemid 27260149)
81. Guilhot C, Jander G, Martin NL, and Beckwith J. Evidence that the pathway of disulfide bond formation in Escherichia coli involves interactions between the cysteines of DsbB and DsbA. Proc Natl Acad Sci USA 92: 9895-9899, 1995.
82. Haebel PW, Goldstone D, Katzen F, Beckwith J, and Met-calf P. The disulfide bond isomerase DsbC is activated by an immunoglobulin-fold thiol oxidoreductase: Crystal structure of the DsbC-DsbDalpha complex. EMBO J 21: 4774-4784, 2002.
83. Hartl FU and Hayer-Hartl M. Molecular chaperones in the cytosol: Ffrom nascent chain to folded protein. Science 295: 1852-1858, 2002. (Pubitemid 34214115)
84. Hatahet F and Ruddock LW. Protein disulfide isomerase: A critical evaluation of its function in disulfide bond formation. Antiox Redox Signal 11: 2807-2850, 2009.
85. Hawkins HC and Freedman RB. The reactivities and ioniza-tion properties of the active-site dithiol groups of mammalian protein disulphide-isomerase. Biochem J 275: 335-339, 1991.
86. Hayashi S, Abe M, Kimoto M, Furukawa S, and Nakazawa T. The dsbA-dsbB disulfide bond formation system of Bur-kholderia cepacia is involved in the production of protease and alkaline phosphatase, motility, metal resistance, and multi-drug resistance. Microbiol Immunol 44: 41-50, 2000. (Pubitemid 30073697)
87. Hell K. The Erv1-Mia40 disulfide relay system in the in-termembrane space of mitochondria. Biochim Biophys Acta 1783: 601-609, 2008.
88. Hennecke J, Spleiss C, and Glockshuber R. Influence of acidic residues and the kink in the active-site helix on the properties of the disulfide oxidoreductase DsbA. J Biol Chem 272: 189-195, 1997. (Pubitemid 27021143)
89. Heras B, Edeling MA, Schirra HJ, Raina S, and Martin JL. Crystal structures of the DsbG disulfide isomerase reveal an unstable disulfide. Proc Natl Acad Sci USA 101: 8876-8881, 2004. (Pubitemid 38781579)
90. Heras B, Kurz M, Jarrott R, Shouldice SR, Frei P, Robin G, Cemazar M, Thony-Meyer L, Glockshuber R, and Martin JL. Staphylococcus aureus DsbA does not have a destabilizing disulfide. A new paradigm for bacterial oxidative folding. J Biol Chem 283: 4261-4271, 2008.
91. Heras B, Kurz M, Shouldice SR, and Martin JL. The name's bond . . . . . disulfide bond. Curr Opin Struct Biol 17: 691-698, 2007.
92. Heras B, Shouldice SR, Totsika M, Scanlon MJ, Schembri MA, and Martin JL. DSB proteins and bacterial pathoge-nicity. Nat Rev Microbiol 7: 215-225, 2009.
93. Heras B, Totsika M, Jarrott R, Shouldice SR, Guncar G, Achard ME, Wells TJ, Argente MP, McEwan AG, and Schembri MA. Structural and functional characterization of three DsbA paralogues from Salmonella enterica serovar Typhimurium. J Biol Chem 285: 18423-18432, 2010.
94. Hilgenboecker K, Hammerstein P, Schlattmann P, Tel-schow A, and Werren JH. How many species are infected with Wolbachia?-A statistical analysis of current data. FEMS Microbiol Lett 281: 215-220, 2008. (Pubitemid 351422951)
95. Hiniker A and Bardwell JC. In vivo substrate specificity of periplasmic disulfide oxidoreductases. J Biol Chem 279: 12967-12973, 2004. (Pubitemid 38445872)
96. Hiniker A and Bardwell JCA. In vivo substrate specificity of periplasmic disulfide oxidoreductases. J Biol Chem 279: 12967-12973, 2004. (Pubitemid 38445872)
97. Holm L, Kaariainen S, Rosenstrom P, and Schenkel A. Searching protein structure databases with DaliLite v.3. Bioinformatics 24: 2780-2781, 2008. (Pubitemid 352722625)
98. Holmgren A, Soderberg BO, Eklund H, and Branden CI. Three-dimensional structure of Escherichia coli thioredoxin-S2 to 2.8A resolution. Proc Natl Acad Sci USA 72: 2305-2309, 1975.
99. Hu SH, Peek JA, Rattigan E, Taylor RK, and Martin JL. Structure of TcpG, the DsbA protein folding catalyst from Vibrio cholerae. J Mol Biol 268: 137-146, 1997. (Pubitemid 27192684)
100. Huber-Wunderlich M and Glockshuber R. A single dipep-tide sequence modulates the redox properties of a whole enzyme family. Fold Des 3: 161-171, 1998. (Pubitemid 28264393)
101. Hultgren SJ, Abraham S, Caparon M, Falk P, St Geme JW, 3rd, and Normark S. Pilus and nonpilus bacterial adhesins: Assembly and function in cell recognition. Cell 73: 887-901, 1993. (Pubitemid 23165606)
102. Hultgren SJ, Normark S, and Abraham SN. Chaperone-assisted assembly and molecular architecture of adhesive pili. Annu Rev Microbiol 45: 383-415, 1991. (Pubitemid 21903797)
103. Hung DL, Knight SD, Woods RM, Pinkner JS, and Hultg-ren SJ. Molecular basis of two subfamilies of immuno-globulin-like chaperones. EMBO J 15: 3792-3805, 1996. (Pubitemid 26289789)
104. Hutchinson EG and Thornton JM. PROMOTIF-A program to identify and analyze structural motifs in proteins. Protein Sci 5: 212-220, 1996. (Pubitemid 26054277)
105. Hutt DM, Powers ET, and Balch WE. The proteostasis boundary in misfolding diseases of membrane traffic. FEBS Lett 583: 2639-2646, 2009.
106. Inaba K. Disulfide bond formation system in Escherichia coli. J Biochem 146: 591597, 2009.
107. Inaba K, Murakami S, Nakagawa A, Iida H, Kinjo M, Ito K, and Suzuki M. Dynamic nature of disulphide bond formation catalysts revealed by crystal structures of DsbB. EMBO J 28: 779-791, 2009.
108. Inaba K, Murakami S, Suzuki M, Nakagawa A, Yamashita E, Okada K, and Ito K. Crystal structure of the DsbB-DsbA complex reveals a mechanism of disulfide bond generation. Cell 127: 789-801, 2006. (Pubitemid 44716258)
109. Ireland DC, Colgrave ML, and Craik DJ. A novel suite of cyclotides from Viola odorata: Sequence variation and the implications for structure, function and stability. Biochem J 400: 1-12, 2006. (Pubitemid 44763814)
110. Ito K. Editing disulphide bonds: Error correction using re-dox currencies. Mol Microbiol 75: 1-5, 2010.
111. Jackson MW and Plano GV. DsbA is required for stable expression of outer membrane protein YscC and for efficient Yop secretion in Yersinia pestis. J Bacteriol 181: 5126-5130, 1999. (Pubitemid 29383552)
112. Jacob-Dubuisson F, Pinkner J, Xu Z, Striker R, Padman-haban A, and Hultgren SJ. PapD chaperone function in pilus biogenesis depends on oxidant and chaperone-like activities of DsbA. Proc Natl Acad Sci USA 91: 11552-11556, 1994. (Pubitemid 24356382)
113. Jacquot JP, Eklund H, Rouhier N, and Schurmann P. Structural and evolutionary aspects of thioredoxin reduc-tases in photosynthetic organisms. Trends Plant Sci 14: 336-343, 2009.
114. Jander G, Martin NL, and Beckwith J. Two cysteines in each periplasmic domain of the membrane protein DsbB are required for its function in protein disulfide bond formation. EMBO J 13: 5121-5127, 1994. (Pubitemid 24341093)
115. Jessop CE, Watkins RH, Simmons JJ, Tasab M, and Bulleid NJ. Protein disulphide isomerase family members show distinct substrate specificity: P5 is targeted to BiP client proteins. J Cell Sci 122: 4287-4295, 2009.
116. Jeyaprakash A and Hoy MA. Long PCR improves Wolbachia DNA amplification: wsp sequences found in 76% of sixty-three arthropod species. Insect Mol Biol 9: 393-405, 2000.
117. Jiang L, Liu Q, and Ni J. In silico identification of the sea squirt selenoproteome. BMC Genomics 11: 289, 2010.
118. Kadokura H and Beckwith J. Four cysteines of the membrane protein DsbB act in concert to oxidize its substrate DsbA. EMBO J 21: 2354-2363, 2002. (Pubitemid 34546708)
119. Kadokura H and Beckwith J. Detecting folding intermediates of a protein as it passes through the bacterial translocation channel. Cell 138: 1164-1173, 2009.
120. Kadokura H, Beckwith J. Mechanisms of oxidative protein folding in the bacterial cell envelope. Antioxid Redox Signal 13: 1231-1246, 2010.
121. Kadokura H, Nichols L, 2nd, and Beckwith J. Mutational alterations of the key cis proline residue that cause accumulation of enzymatic reaction intermediates of DsbA, a member of the thioredoxin superfamily. J Bacteriol 187: 1519-1522, 2005. (Pubitemid 40299477)
122. Kadokura H, Tian H, Zander T, Bardwell JC, and Beckwith J. Snapshots of DsbA in action: Detection of proteins in the process of oxidative folding. Science 303: 534-537, 2004. (Pubitemid 38120853)
123. Kamitani S, Akiyama Y, and Ito K. Identification and characterization of an Escherichia coli gene required for the formation of correctly folded alkaline phosphatase, a peri-plasmic enzyme. EMBO J 11: 57-62, 1992.
124. Karala AR, Lappi AK, and Ruddock LW. Modulation of an active-site cysteine pK(a) allows PDI to act as a catalyst of both disulfide bond formation and isomerization. J Mol Biol 396: 883-892, 2010.
125. Katti SK, LeMaster DM, and Eklund H. Crystal structure of thioredoxin from Escherichia coli at 1.68 A resolution. J Mol Biol 212: 167-184, 1990.
126. Katzen F and Beckwith J. Transmembrane electron transfer by the membrane protein DsbD occurs via a disulfide bond cascade. Cell 103: 769-779, 2000.
127. Katzen F and Beckwith J. Role and location of the unusual redox-active cysteines in the hydrophobic domain of the transmembrane electron transporter DsbD. Proc Natl Acad Sci USA 100: 10471-10476, 2003. (Pubitemid 37071902)
128. Kawano S, Yamano K, Naoe M, Momose T, Terao K, Nishikawa S, Watanabe N, and Endo T. Structural basis of yeast Tim40=Mia40 as an oxidative translocator in the mi-tochondrial intermembrane space. Proc Natl Acad Sci USA 106: 14403-14407, 2009.
129. Kelley RF and Richards FM. Replacement of proline-76 with alanine eliminates the slowest kinetic phase in thior-edoxin folding. Biochemistry 26: 6765-6774, 1987.
130. Kishigami S, Kanaya E, Kikuchi M, and Ito K. DsbA-DsbB interaction through their active site cysteines. Evidence from an odd cysteine mutant of DsbA. J Biol Chem 270: 17072-17074, 1995.
131. Kobayashi T and Ito K. Respiratory chain strongly oxidizes the CXXC motif of DsbB in the Escherichia coli disulfide bond formation pathway. EMBO J 18: 1192-1198, 1999. (Pubitemid 29110304)
132. Kouwen TR, van der Goot A, Dorenbos R, Winter T, Antelmann H, Plaisier MC, Quax WJ, van Dijl JM, and Dubois JY. Thiol-disulphide oxidoreductase modules in the low-GC Gram-positive bacteria. Mol Microbiol 64: 984-999, 2007. (Pubitemid 46743961)
133. Krissinel E and Henrick K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr D Biol Crystallogr 60: 2256-2268, 2004. (Pubitemid 41742778)
134. Kurz M, Iturbe-Ormaetxe I, Jarrott R, Cowieson N, Robin G, Jones A, King GJ, Frei P, Glockshuber R, O'Neill SL, Heras B, and Martin JL. Cloning, expression, purification and characterization of a DsbA-like protein from Wolbachia pipientis. Protein Expr Purif 59: 266-273, 2008.
135. Kurz M, Iturbe-Ormaetxe I, Jarrott R, Shouldice SR, Wouters MA, Frei P, Glockshuber R, O'Neill SL, Heras B, and Martin JL. Structural and functional characterization of the oxidoreductase alpha-DsbA1 from Wolbachia pipientis. Antioxid Redox Signal 11: 1485-1500, 2009.
136. Ladner JE, Parsons JF, Rife CL, Gilliland GL, and Armstrong RN. Parallel evolutionary pathways for glutathione trans-ferases: Structure and mechanism of the mitochondrial class kappa enzyme rGSTK1-1. Biochemistry 43: 352-361, 2004. (Pubitemid 38082557)
137. Lafaye C, Iwema T, Carpentier P, Jullian-Binard C, Kroll JS, Collet JF, and Serre L. Biochemical and structural study of the homologues of the thiol-disulfide oxidoreductase DsbA in Neisseria meningitidis. J Mol Biol 392: 952-966, 2009.
138. Laskowski RA. PDBsum new things. Nucleic Acids Res 37: D355-359, 2009.
139. Lee SH, Butler SM, and Camilli A. Selection for in vivo regulators of bacterial virulence. Proc Natl Acad Sci USA 98: 6889-6894, 2001. (Pubitemid 32538312)
140. Leichert LI and Jakob U. Global methods to monitor the thiol-disulfide state of proteins in vivo. Antioxid Redox Signal 8: 763-772, 2006. (Pubitemid 44036495)
141. Li J, Xia Z, and Ding J. Thioredoxin-like domain of human kappa class glutathione transferase reveals sequence ho-mology and structure similarity to the theta class enzyme. Protein Sci 14: 2361-2369, 2005. (Pubitemid 41252805)
142. Li W, Schulman S, Dutton RJ, Boyd D, Beckwith J, and Rapoport TA. Structure of a bacterial homologue of vitamin K epoxide reductase. Nature 463: 507-512, 2010.
143. Lin D, Rao CV, and Slauch JM. The Salmonella SPI1 type three secretion system responds to periplasmic disulfide bond status via the flagellar apparatus and the RcsCDB system. J Bacteriol 190: 87-97, 2008.
144. Lisowsky T. Dual function of a new nuclear gene for oxi-dative phosphorylation and vegetative growth in yeast. Mol Gen Genet 232: 58-64, 1992.
145. Longen S, Bien M, Bihlmaier K, Kloeppel C, Kauff F, Hammermeister M, Westermann B, Herrmann JM, and Riemer J. Systematic analysis of the twin cx(9)c protein family. J Mol Biol 393: 356-368, 2009.
146. Mac TT, von Hacht A, Hung KC, Dutton RJ, Boyd D, Bardwell JC, and Ulmer TS. Insight into disulfide bond catalysis in Chlamydia from the structure and function of DsbH, a novel oxidoreductase. J Biol Chem 283: 824-832, 2008.
147. Maeda K, Hagglund P, Finnie C, Svensson B, and Hen-riksen A. Structural basis for target protein recognition by the protein disulfide reductase thioredoxin. Structure 14: 1701-1710, 2006. (Pubitemid 46127457)
148. Magnet S, Bellais S, Dubost L, Fourgeaud M, Mainardi JL, Petit-Frere S, Marie A, Mengin-Lecreulx D, Arthur M, and Gutmann L. Identification of the L,D-transpeptidases responsible for attachment of the Braun lipoprotein to Es-cherichia coli peptidoglycan. J Bacteriol 189: 3927-3931, 2007. (Pubitemid 46740192)
149. Malojcic G, Owen RL, Grimshaw JP, and Glockshuber R. Preparation and structure of the charge-transfer intermediate of the transmembrane redox catalyst DsbB. FEBS Lett 582: 3301-3307, 2008.
150. Martin JL. Thioredoxin-A fold for all reasons. Structure 3: 245-250, 1995.
151. Martin JL, Bardwell JC, and Kuriyan J. Crystal structure of the DsbA protein required for disulphide bond formation in vivo. Nature 365: 464-468, 1993. (Pubitemid 23311046)
152. Martin JL, Waksman G, Bardwell JC, Beckwith J, and Kuriyan J. Crystallization of DsbA, an Escherichia coli protein required for disulphide bond formation in vivo. J Mol Biol 230: 1097-1100, 1993. (Pubitemid 23159951)
153. McCarthy AA, Haebel PW, Torronen A, Rybin V, Baker EN, and Metcalf P. Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nature Struct Biol 7: 196-199, 2000. (Pubitemid 30140763)
154. Meima R, Eschevins C, Fillinger S, Bolhuis A, Hamoen LW, Dorenbos R, Quax WJ, van Dijl JM, Provvedi R, Chen I, Dubnau D, and Bron S. The bdbDC operon of Bacillus subtilis encodes thiol-disulfide oxidoreductases required for competence development. J Biol Chem 277: 6994-7001, 2002. (Pubitemid 34953086)
155. Menard R, Sansonetti PJ, and Parsot C. Nonpolar muta-genesis of the ipa genes defines IpaB, IpaC, and IpaD as effectors of Shigella flexneri entry into epithelial cells. J Bacteriol 175: 5899-5906, 1993. (Pubitemid 23277438)
156. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W, Hell K, and Herrmann JM. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121: 1059-1069, 2005. (Pubitemid 40884396)
157. Miki T, Okada N, and Danbara H. Two periplasmic dis-ulfide oxidoreductases, DsbA and SrgA, target outer membrane protein SpiA, a component of the Salmonella pathogenicity island 2 Type III secretion system. J Biol Chem 279: 34631-34642, 2004. (Pubitemid 39318093)
158. Miki T, Okada N, Kim Y, Abe A, and Danbara H. DsbA directs efficient expression of outer membrane secretin EscC of the enteropathogenic Escherichia coli type III secretion apparatus. Microb Pathogen 44: 151-158, 2008. (Pubitemid 350297680)
159. Missiakas D, Georgopoulos C, and Raina S. Identification and
160. Mossner E, Huber-Wunderlich M, and Glockshuber R. Characterization of Escherichia coli thioredoxin variants mimicking the active-sites of other thiol=disulfide oxido-reductases. Protein Sci 7: 1233-1244, 1998. (Pubitemid 28237057)
161. Moutiez M, Burova TV, Haertle T, and Quemeneur E. On the non-respect of the thermodynamic cycle by DsbA variants. Protein Sci 8: 106-112, 1999. (Pubitemid 29035524)
162. Murzin AG, Brenner SE, Hubbard T, and Chothia C. SCOP: A structural classification of proteins database for the investigation of sequences and structures. J Mol Biol 247: 536-540, 1995.
163. Nelson JW and Creighton TE. Reactivity and ionization of the active site cysteine residues of DsbA, a protein required for disulfide bond formation in vivo. Biochemistry 33: 5974-5983, 1994. (Pubitemid 24184604)
164. Nuccio SP and Baumler AJ. Evolution of the chaper-one=usher assembly pathway: fimbrial classification goes Greek. Microbiol Mol Biol Rev 71: 551-575, 2007. (Pubitemid 350309177)
165. Parish D, Benach J, Liu G, Singarapu KK, Xiao R, Acton T, Su M, Bansal S, Prestegard JH, Hunt J, Montelione GT, and Szyperski T. Protein chaperones Q8ZP25-SALTY from Salmonella typhimurium and HYAE-ECOLI from Escherichia coli exhibit thioredoxin-like structures despite lack of canonical thioredoxin active site sequence motif. J Struct Funct Genomics 9: 41-49, 2008.
166. Park SY, Heo YJ, Choi YS, Deziel E, and Cho YH. Conserved virulence factors of Pseudomonas aeruginosa are required for killing Bacillus subtilis. J Microbiol 43: 443-450, 2005. (Pubitemid 41666884)
167. Paxman JJ, Borg NA, Horne J, Thompson PE, Chin Y, Sharma P, Simpson JS, Wielens J, Piek S, Kahler CM, Sa-kellaris H, Pearce M, Bottomley SP, Rossjohn J, and Scanlon MJ. The structure of the bacterial oxidoreductase enzyme DsbA in complex with a peptide reveals a basis for substrate specificity in the catalytic cycle of DsbA enzymes. J Biol Chem 284: 17835-17845, 2009.
168. Payne DJ. Microbiology. Desperately seeking new antibiotics. Science 321: 1644-1645, 2008.
169. Peek JA and Taylor RK. Characterization of a periplasmic thiol:disulfide interchange protein required for the functional maturation of secreted virulence factors of Vibrio cholerae. Proc Natl Acad Sci USA 89: 6210-6214, 1992.
170. Pelicic V. Type IV pili: E pluribus unum? Mol Microbiol 68: 827-837, 2008. (Pubitemid 351596335)
171. Piatek R, Bruzdziak P, Wojciechowski M, Zalewska-Piatek B, and Kur J. The noncanonical disulfide bond as the important stabilizing element of the immunoglobulin fold of the Dr fimbrial DraE subunit. Biochemistry 49: 1460-1468, 2010.
172. Pollard MG, Travers KJ, and Weissman JS. Ero1p: A novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol Cell 1: 171-182, 1998. (Pubitemid 128378658)
173. Pugsley AP, Bayan N, and Sauvonnet N. Disulfide bond formation in secreton component PulK provides a possible explanation for the role of DsbA in pullulanase secretion. J Bacteriol 183: 1312-1319, 2001. (Pubitemid 32107727)
174. Py B, Loiseau L, and Barras F. An inner membrane platform in the type II secretion machinery of Gram-negative bacteria. EMBO Rep 2: 244-248, 2001. (Pubitemid 32273305)
175. Quan S, Schneider I, Pan J, Von Hacht A, and Bardwell JC. The CXXC motif is more than a redox rheostat. J Biol Chem 282: 28823-28833, 2007. (Pubitemid 47606028)
176. Rasko DA and Sperandio V. Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9: 117-128, 2010.
177. Regeimbal J and Bardwell JCA. DsbB catalyzes disulfide bond formation de novo. J Biol Chem 277: 32706-32713, 2002. (Pubitemid 34984777)
178. Remaut H, Tang C, Henderson NS, Pinkner JS, Wang T, Hultgren SJ, Thanassi DG, Waksman G, and Li H. Fiber formation across the bacterial outer membrane by the chaperone=usher pathway. Cell 133: 640-652, 2008. (Pubitemid 351636304)
179. Ren G, Stephan D, Xu Z, Zheng Y, Tang D, Harrison RS, Kurz M, Jarrott R, Shouldice SR, Hiniker A, Martin JL, Heras B, and Bardwell JC. Properties of the thioredoxin fold superfamily are modulated by a single amino acid residue. J Biol Chem 284: 10150-10159, 2009.
180. Riemer J, Bulleid N, and Herrmann JM. Disulfide formation in the ER and mitochondria: Two solutions to a common process. Science 324: 1284-1287, 2009.
181. Rietsch A, Bessette P, Georgiou G, and Beckwith J. Reduction of the periplasmic disulfide bond isomerase, DsbC, occurs by passage of electrons from cytoplasmic thior-edoxin. J Bacteriol 179: 6602-6608, 1997. (Pubitemid 27465291)
182. Rinaldi FC, Meza AN, and Guimaraes BG. Structural and biochemical characterization of Xylella fastidiosa DsbA family members: New insights into the enzyme-substrate interaction. Biochemistry 48: 3508-3518, 2009.
183. Rozhkova A, Stirnimann CU, Frei P, Grauschopf U, Bru-nisholz R, Grutter MG, Capitani G, and Glockshuber R. Structural basis and kinetics of inter- and intramolecular disulfide exchange in the redox catalyst DsbD. EMBO J 23: 1709-1719, 2004. (Pubitemid 38649634)
184. Sauer FG, Remaut H, Hultgren SJ, and Waksman G. Fiber assembly by the chaperone-usher pathway. Biochim Biophys Acta 1694: 259-267, 2004. (Pubitemid 39535073)
185. Sauvonnet N and Pugsley AP. The requirement for DsbA in pullulanase secretion is independent of disulphide bond formation in the enzyme. Mol Microbiol 27: 661-667, 1998. (Pubitemid 28045747)
186. Schwaller M, Wilkinson B, and Gilbert HF. Reduction-reoxidation cycles contribute to catalysis of disulfide isomerization by protein-disulfide isomerase. J Biol Chem 278: 7154-7159, 2003. (Pubitemid 36800714)
187. Sevier CS, Kadokura H, Tam VC, Beckwith J, Fass D, and Kaiser CA. The prokaryotic enzyme DsbB may share key structural features with eukaryotic disulfide bond forming oxidoreductases. Protein Sci 14: 1630-1642, 2005. (Pubitemid 41007924)
188. Sevier CS and Kaiser CA. Conservation and diversity of the cellular disulfide bond formation pathways. Antioxid Redox Signal 8: 797-811, 2006. (Pubitemid 44036498)
189. Shao F, Bader MW, Jakob U, and Bardwell JC. DsbG, a protein disulfide isomerase with chaperone activity. J Biol Chem 275: 13349-13352, 2000. (Pubitemid 30257393)
190. Shevchik VE, Bortoli-German I, Robert-Baudouy J, Ro-binet S, Barras F, and Condemine G. Differential effect of dsbA and dsbC mutations on extracellular enzyme secretion in Erwinia chrysanthemi. Mol Microbiol 16: 745-753, 1995.
191. Shouldice SR, Cho SH, Boyd D, Heras B, Eser M, Beckwith J, Riggs P, Martin JL, and Berkmen M. In vivo oxidative protein folding can be facilitated by oxidation-reduction cycling. Mol Microbiol 75: 13-28, 2010.
192. Shouldice SR, Heras B, Jarrott R, Sharma P, Scanlon MJ, and Martin J. Characterisation of the DsbA oxidative folding catalyst from Pseudomonas aerugionsa reveals a highly oxidizing protein that binds small molecules. Anti-oxid Redox Signal 12: 921-931, 2010.
193. Sideris DP and Tokatlidis K. Oxidative protein folding in the mitochondrial intermembrane space. Antioxid Redox Signal 13: 1189-1204, 2010.
194. Sinha S, Langford PR,and Kroll JS. Functional diversity of three different DsbA proteins from Neisseria meningitidis. Microbiology 150: 2993-3000, 2004. (Pubitemid 39317800)
195. Soto GE and Hultgren SJ. Bacterial adhesins: Common themes and variations in architecture and assembly. J Bac-teriol 181: 1059-1071, 1999. (Pubitemid 29119542)
196. Stenson TH and Weiss AA. DsbA and DsbC are required for secretion of pertussis toxin by Bordetella pertussis. Infect Immun 70: 2297-2303, 2002. (Pubitemid 34408368)
197. Stojanovski D, Milenkovic D, Muller JM, Gabriel K, Schulze- Specking A, Baker MJ, Ryan MT, Guiard B, Pfanner N, and Chacinska A. Mitochondrial protein import: precursor oxidation in a ternary complex with disulfide carrier and sulf-hydryl oxidase. J Cell Biol 183: 195-202, 2008.
198. Stojanovski D, Muller JM, Milenkovic D, Guiard B, Pfanner N, and Chacinska A. The MIA system for protein import into the mitochondrial intermembrane space. Biochim Bio-phys Acta 1783: 610-617, 2008. (Pubitemid 351458554)
199. Su D, Berndt C, Fomenko DE, Holmgren A, and Gladyshev VN. A conserved cis-proline precludes metal binding by the active site thiolates in members of the thioredoxin family of proteins. Biochemistry 46: 6903-6910, 2007. (Pubitemid 46906419)
200. Tapley TL, Eichner T, Gleiter S, Ballou DP,and Bardwell JC. Kinetic characterization of the disulfide bond-forming enzyme DsbB. J Biol Chem 282: 10263-10271, 2007. (Pubitemid 47093415)
201. Terziyska N, Lutz T, Kozany C, Mokranjac D, Mesecke N, Neupert W, Herrmann JM, and Hell K. Mia40, a novel factor for protein import into the intermembrane space of mitochondria is able to bind metal ions. FEBS Lett 579: 179-184, 2005. (Pubitemid 40023393)
202. Thakur KG, Praveena T, and Gopal B. Structural and biochemical bases for the redox sensitivity of Mycobacterium tuberculosis RslA. J Mol Biol 397: 1199-1208, 2010.
203. Tinsley CR, Voulhoux R, Beretti JL, Tommassen J, and Nassif X. Three homologues, including two membrane-bound proteins, of the disulfide oxidoreductase DsbA in Neisseria meningitidis: Effects on bacterial growth and biogenesis of functional type IV pili. J Biol Chem 279: 27078-27087, 2004. (Pubitemid 38812544)
204. Tomb JF. A periplasmic protein disulfide oxidoreductase is required for transformation of Haemophilus influenzae Rd. Proc Natl Acad Sci USA 89: 10252-10256, 1992.
205. Totsika M, Heras B, Wurpel DJ, and Schembri MA. Characterization of two homologous disulfide bond systems involved in virulence factor biogenesis in uropathogenic Escherichia coli CFT073. J Bacteriol 191: 3901-3908, 2009.
206. Turcot I, Ponnampalam TV, Bouwman CW, and Martin NL. Isolation and characterization of a chromosomally encoded disulphide oxidoreductase from Salmonella enterica serovar Typhimurium. Can J Microbiol 47: 711-721, 2001. (Pubitemid 33033456)
207. Tutar L and Tutar Y. Heat shock proteins; An overview. Curr Pharm Biotechnol 11: 216-222, 2010.
208. Urban A, Leipelt M, Eggert T, and Jaeger KE. DsbA and DsbC affect extracellular enzyme formation in Pseudomonas aeruginosa. J Bacteriol 183: 587-596, 2001. (Pubitemid 32048117)
209. Vertommen D, Depuydt M, Pan J, Leverrier P, Knoops L, Szikora JP, Messens J, Bardwell JC, and Collet JF. The dis-ulphide isomerase DsbC cooperates with the oxidase DsbA in a DsbD-independent manner. Mol Microbiol 67: 336-349, 2008. (Pubitemid 350295830)
210. Vincent-Sealy LV, Thomas JD, Commander P, and Sal-mond GP. Erwinia carotovora DsbA mutants: Eevidence for a periplasmic-stress signal transduction system affecting transcription of genes encoding secreted proteins. Microbiology 145: 1945-1958, 1999. (Pubitemid 29396925)
211. Vivian JP, Scoullar J, Rimmer K, Bushell SR, Beddoe T, Wilce MC, Byres E, Boyle TP, Doak B, Simpson JS, Graham B, Heras B, Kahler CM, Rossjohn J, and Scanlon MJ. Structure and function of the oxidoreductase DsbA1 from Neisseria meningitidis. J Mol Biol 394: 931-943, 2009.
212. Vivian JP, Scoullar J, Robertson AL, Bottomley SP, Horne J, Chin Y, Wielens J, Thompson PE, Velkov T, Piek S, Byres E, Beddoe T, Wilce MC, Kahler CM, Rossjohn J, and Scanlon MJ. Structural and biochemical characterization of the ox-idoreductase NmDsbA3 from Neisseria meningitidis. J Biol Chem 283: 32452-32461, 2008.
213. Vlamis-Gardikas A. The multiple functions of the thiol-based electron flow pathways of Escherichia coli: Eternal concepts revisited. Biochim Biophys Acta 1780: 1170-1200, 2008.
214. Vogt SL, Nevesinjac AZ, Humphries RM, Donnenberg MS, Armstrong GD, and Raivio TL. The Cpx envelope stress response both facilitates and inhibits elaboration of the enteropathogenic Escherichia coli bundle-forming pilus. Mol Microbiol 76: 1095-1110, 2010.
215. Waksman G and Hultgren SJ. Structural biology of the chaperone-usher pathway of pilus biogenesis. Nat Rev Mi-crobiol 7: 765-774, 2009.
216. Wang S, Trumble WR, Liao H, Wesson CR, Dunker AK, Kang CH. Crystal structure of calsequestrin from rabbit skeletal muscle sarcoplasmic reticulum. Nat Struct Biol 5: 476-483, 1998. (Pubitemid 28265031)
217. Waschutza G, Li V, Schafer T, Schomburg D, Villmann C, Zakaria H, and Otto B. Engineered disulfide bonds in re-combinant human interferon-gamma: The impact of the N-terminal helix A and the AB-loop on protein stability. Protein Eng 9: 905-912, 1996. (Pubitemid 26366516)
218. Watarai M, Tobe T, Yoshikawa M, and Sasakawa C. Dis-ulfide oxidoreductase activity of Shigella flexneri is required for release of Ipa proteins and invasion of epithelial cells. Proc Natl Acad Sci USA 92: 4927-4931, 1995.
219. Wetzel R, Perry LJ, Baase WA, and Becktel WJ. Disulfide bonds and thermal stability in T4 lysozyme. Proc Natl Acad Sci USA 85: 401-405, 1988.
220. Worden AZ, Lee JH, Mock T, Rouze P, Simmons MP, Aerts AL, Allen AE, Cuvelier ML, Derelle E, Everett MV, Foulon E, Grimwood J, Gundlach H, Henrissat B, Napoli C, McDonald SM, Parker MS, Rombauts S, Salamov A, Von Dassow P, Badger JH, Coutinho PM, Demir E, Dubchak I, Gentemann C, Eikrem W, Gready JE, John U, Lanier W, Lindquist EA, Lucas S, Mayer KF, Moreau H, Not F, Otillar R, Panaud O, Pangilinan J, Paulsen I, Piegu B, Poliakov A, Robbens S, Schmutz J, Toulza E, Wyss T, Zelensky A, Zhou K, Armbrust EV, Bhattacharya D, Goodenough UW, Van de Peer Y, and Grigoriev IV. Green evolution and dynamic adaptations revealed by genomes of the marine picoeu-karyotes Micromonas. Science 324: 268-272, 2009.
221. Wu CK, Dailey TA, Dailey HA, Wang BC, and Rose JP. The crystal structure of augmenter of liver regeneration: A mammalian FAD-dependent sulfhydryl oxidase. Protein Sci 12: 1109-1118, 2003. (Pubitemid 36505444)
222. Wülfing C and Rappuoli R. Efficient production of heat-labile enterotoxin mutant proteins by overexpression of dsbA in a degP-deficient Escherichia coli strain. Arch Mi-crobiol 167: 280-283, 1997. (Pubitemid 27166219)
223. Wunderlich M and Glockshuber R. Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli. Protein Sci 2: 717-726, 1993. (Pubitemid 23121086)
224. Xia TH, Bushweller JH, Sodano P, Billeter M, Bjornberg O, Holmgren A, and Wuthrich K. NMR structure of oxidized Escherichia coli glutaredoxin: Comparison with reduced E. coli glutaredoxin and functionally related proteins. Protein Sci 1: 310-321, 1992. (Pubitemid 23007297)
225. Yen TY, Pal S, and de la Maza LM. Characterization of the disulfide bonds and free cysteine residues of the Chlamydia trachomatis mouse pneumonitis major outer membrane protein. Biochemistry 44: 6250-6256, 2005. (Pubitemid 40570718)
226. Young JC, Agashe VR, Siegers K, and Hartl FU. Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5: 781-791, 2004. (Pubitemid 39336272)
227. Yu J. Inactivation of DsbA, but not DsbC and DsbD, affects the intracellular survival and virulence of Shigella flexneri. Infect Immun 66: 3909-3917, 1998. (Pubitemid 28347854)
228. Yu J, Webb H, and Hirst TR. A homologue of the Escher-ichia coli DsbA protein involved in disulphide bond formation is required for enterotoxin biogenesis in Vibrio cholerae. Mol Microbiol 6: 1949-1958, 1992.
229. Zapun A, Bardwell JC, and Creighton TE. The reactive and destabilizing disulfide bond of DsbA, a protein required for protein disulfide bond formation in vivo. Biochemistry 32: 5083-5092, 1993. (Pubitemid 23162074)
230. Zhang HZ and Donnenberg MS. DsbA is required for stability of the type IV pilin of enteropathogenic Escherichia coli. Mol Microbiol 21: 787-797, 1996. (Pubitemid 26281526)
231. Zhang Y, Fomenko DE, and Gladyshev VN. The microbial selenoproteome of the Sargasso Sea. Genome Biol 6: R37, 2005.
232. Zhang Y and Gladyshev VN. High content of proteins containing 21st and 22nd amino acids, selenocysteine and pyrrolysine, in a symbiotic delta proteobacterium of gutless worm Olavius algarvensis. Nucleic Acids Res 35: 4952-4963, 2007. (Pubitemid 47394182)
233. Zhang Y, Romero H, Salinas G, and Gladyshev VN. Dynamic evolution of selenocysteine utilization in bacteria: A balance between selenoprotein loss and evolution of sele-nocysteine from redox active cysteine residues. Genome Biol 7: R94, 2006.
234. Zhou Y, Cierpicki T, Jimenez RH, Lukasik SM, Ellena JF, Cafiso DS, Kadokura H, Beckwith J, and Bushweller JH. NMR solution structure of the integral membrane enzyme DsbB: Functional insights into DsbB-catalyzed disulfide bond formation. Mol Cell 31: 896-908, 2008.