Comparative sequence, structure and redox analyses of Klebsiella pneumoniae DsbA show that anti-virulence target DsbA enzymes fall into distinct classes

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Kurth, Fabian ^a   Rimmer, Kieran ^b   Premkumar, Lakshmanane ^a   Mohanty, Biswaranjan ^b   Duprez, Wilko ^a   Halili, Maria A ^a   Shouldice, Stephen R ^a,c   Heras, Begoña ^a,d   Fairlie, David P ^a   Scanlon, Martin J ^a,b   Martin, Jennifer L ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b MONASH UNIVERSITY   (Australia)

^c JANSSEN RESEARCH FOUNDATION   (Belgium)

^d LA TROBE UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENETIC COMPLEMENTATION TEST; KLEBSIELLA PNEUMONIAE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; OXIDATION-REDUCTION; PROTEIN DISULFIDE-ISOMERASES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SALMONELLA TYPHIMURIUM; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; VIRULENCE FACTORS;

EID: 84893633855     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0080210     Document Type: Article

References (76)

1. Souli M, Galani I, Giamarellou H (2008) Emergence of extensively drug-resistant and pandrug-resistant Gram-negative bacilli in Europe. Euro Surveill 13(47): 19045. PubMed: 19021957.
2. Heras B, Shouldice SR, Totsika M, Scanlon MJ, Schembri MA et al. (2009) DSB proteins and bacterial pathogenicity. Nat Rev Microbiol 7: 215-225. doi:10.1038/nrmicro2087. PubMed: 19198617.
3. Bardwell JC, McGovern K, Beckwith J (1991) Identification of a protein required for disulfide bond formation in vivo. Cell 67: 581-589. doi:10.1016/0092-8674(91)90532-4. PubMed: 1934062. (Pubitemid 121001472)
4. Dutton RJ, Boyd D, Berkmen M, Beckwith J (2008) Bacterial species exhibit diversity in their mechanisms and capacity for protein disulfide bond formation. Proc Natl Acad Sci U S A 105: 11933-11938. doi:10.1073/pnas. 0804621105. PubMed: 18695247.
5. Miki T, Okada N, Kim Y, Abe A, Danbara H (2008) DsbA directs efficient expression of outer membrane secretin EscC of the enteropathogenic Escherichia coli type III secretion apparatus. Microb Pathog 44: 151-158. doi:10.1016/j.micpath.2007.09.001. PubMed: 17933489. (Pubitemid 350297680)
6. Wunderlich M, Glockshuber R (1993) Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli. Protein Sci 2: 717-726. doi:10.1002/pro.5560020503. PubMed: 8495194. (Pubitemid 23121086)
7. Zapun A, Bardwell JC, Creighton TE (1993) The reactive and destabilizing disulfide bond of DsbA, a protein required for protein disulfide bond formation in vivo. Biochemistry 32: 5083-5092. doi:10.1021/bi00070a016. PubMed: 8494885. (Pubitemid 23162074)
8. Martin JL, Bardwell JC, Kuriyan J (1993) Crystal structure of the DsbA protein required for disulphide bond formation in vivo. Nature 365: 464-468. doi:10.1038/365464a0. PubMed: 8413591. (Pubitemid 23311046)
9. Huber-Wunderlich M, Glockshuber R (1998) A single dipeptide sequence modulates the redox properties of a whole enzyme family. Fold Des 3: 161-171. doi:10.1016/S1359-0278(98)00024-8. PubMed: 9562546. (Pubitemid 28264393)
10. Kobayashi T, Kishigami S, Sone M, Inokuchi H, Mogi T et al. (1997) Respiratory chain is required to maintain oxidized states of the DsbADsbB disulfide bond formation system in aerobically growing Escherichia coli cells. Proc Natl Acad Sci U S A 94: 11857-11862. doi:10.1073/pnas.94.22.11857. PubMed: 9342327.
11. Ireland PM, McMahon RM, Marshall LE, Halili M, Furlong et al. (: Sep 202013) Disarming Burkholderia pseudomallei: Structural and functional characterisation of a disulfide oxidoreductase (DsbA) required for virulence in vivo. Antioxid Redox Signal: Sep 20 Epub.
12. Totsika M, Heras B, Wurpel DJ, Schembri MA (2009) Characterization of two homologous disulfide bond systems involved in virulence factor biogenesis in uropathogenic Escherichia coli CFT073. J Bacteriol 191: 3901-3908. doi:10.1128/JB.00143-09. PubMed: 19376849.
13. Heras B, Kurz M, Jarrott R, Shouldice SR, Frei P et al. (2008) Staphylococcus aureus DsbA does not have a destabilizing disulfide. A new paradigm for bacterial oxidative folding. J Biol Chem 283: 4261-4271. PubMed: 18077463.
14. Shouldice SR, Heras B, Walden PM, Totsika M, Schembri MA et al. (2011) Structure and function of DsbA, a key bacterial oxidative folding catalyst. Antioxid Redox Signal 14: 1729-1760. doi:10.1089/ars.2010.3344. PubMed: 21241169.
15. Vivian JP, Scoullar J, Rimmer K, Bushell SR, Beddoe T et al. (2009) Structure and function of the oxidoreductase DsbA1 from Neisseria meningitidis. J Mol Biol 394: 931-943. doi:10.1016/j.jmb.2009.09.065. PubMed: 19815019.
16. Shouldice SR, Heras B, Jarrott R, Sharma P, Scanlon MJ et al. (2010) Characterization of the DsbA oxidative folding catalyst from Pseudomonas aeruginosa reveals a highly oxidizing protein that binds small molecules. Antioxid Redox Signal 12: 921-931. doi:10.1089/ars.2009.2736. PubMed: 19788398.
17. Hu SH, Peek JA, Rattigan E, Taylor RK, Martin JL (1997) Structure of TcpG, the DsbA protein folding catalyst from Vibrio cholerae. J Mol Biol 268: 137-146. doi:10.1006/jmbi.1997.0940. PubMed: 9149147. (Pubitemid 27192684)
18. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234. doi:10.1016/j.pep.2005.01.016. PubMed: 15915565.
19. Bader M, Muse W, Zander T, Bardwell J (1998) Reconstitution of a protein disulfide catalytic system. J Biol Chem 273: 10302-10307. doi:10.1074/jbc.273. 17.10302. PubMed: 9553083. (Pubitemid 28227634)
20. Holmgren A (1979) Thioredoxin catalyzes the reduction of insulin disulfides by dithiothreitol and dihydrolipoamide. J Biol Chem 254: 9627-9632. PubMed: 385588.
21. Nelson JW, Creighton TE (1994) Reactivity and ionization of the active site cysteine residues of DsbA, a protein required for disulfide bond formation in vivo. Biochemistry 33: 5974-5983. doi:10.1021/bi00185a039. PubMed: 8180227. (Pubitemid 24184604)
22. Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82: 70-77. doi:10.1016/0003-9861(59)90090-6. PubMed: 13650640.
23. Kurz M, Iturbe-Ormaetxe I, Jarrott R, Shouldice SR, Wouters MA et al. (2009) Structural and functional characterization of the oxidoreductase alpha-DsbA1 from Wolbachia pipientis. Antioxid Redox Signal 11: 1485-1500. doi:10.1089/ars.2008.2420. PubMed: 19265485.
24. McPhillips TM, McPhillips SE, Chiu HJ, Cohen AE, Deacon AM et al. (2002) Blu-Ice and the Distributed Control System: software for data acquisition and instrument control at macromolecular crystallography beamlines. J Synchrotron Radiat 9: 401-406. doi:10.1107/S0909049502015170. PubMed: 12409628.
25. Battye TG, Kontogiannis L, Johnson O, Powell HR, Leslie AG (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallogr D Biol Crystallogr 67: 271-281. doi:10.1107/S0907444910048675. PubMed: 21460445.
26. Kabsch W (2010) Xds. Acta Crystallogr D Biol Crystallogr 66: 125-132. doi:10.1107/S0907444909047337. PubMed: 20124692.
27. Evans P (2006) Scaling and assessment of data quality. Acta Crystallogr D Biol Crystallogr 62: 72-82. doi:10.1107/S0108767306098564. PubMed: 16369096.
28. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40: 658-674. doi:10.1107/S0021889807021206. PubMed: 19461840. (Pubitemid 47080256)
29. Emsley P, Lohkamp B, Scott WG, Cowtan K (2010) Features and development of Coot. Acta Crystallogr D Biol Crystallogr 66: 486-501. doi:10.1107/ S0907444910007493. PubMed: 20383002.
30. Adams PD, Afonine PV, Bunkóczi G, Chen VB, Davis IW et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66: 213-221. doi:10.1107/ S0907444909052925. PubMed: 20124702.
31. Chen VB, Arendall WB 3rd, Headd JJ, Keedy DA, Immormino RM et al. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21. doi:10.1107/S1744309109042018. PubMed: 20057044.
32. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA (2001) Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98: 10037-10041. doi:10.1073/pnas.181342398. PubMed: 11517324. (Pubitemid 32802969)
33. Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y et al. (2006) CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res 34: W116-W118. doi:10.1093/nar/gkl601. PubMed: 16844972. (Pubitemid 44529746)
34. Li Z, Ye Y, Godzik A (2006) Flexible Structural Neighborhood - a database of protein structural similarities and alignments. Nucleic Acids Res 34: D277-D280. doi:10.1093/nar/gkj124. PubMed: 16381864.
35. Fiorito F, Herrmann T, Damberger FF, Wuthrich K (2008) Autom Automated amino acid side-chain NMR assignment of proteins using (13)C- and (15)N-resolved 3D [ (1)H, (1)H]-NOESY. J Biomol NMR 42: 23-33
36. Mohanty B, Serrano P, Pedrini B, Jaudzems K, Geralt M et al. (2010) Comparison of NMR and crystal structures for the proteins TM1112 and TM1367. Acta Crystallogr Sect F Struct Biol Cryst Commun 66: 1381-1392. doi:10.1107/S1744309110020956. PubMed: 20944235.
37. Güntert P (2004) Automated NMR structure calculation with CYANA. Methods Mol Biol 278: 353-378. PubMed: 15318003.
38. Koradi R, Billeter M, Wüthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14: 29-55. 8744573.
39. Inaba K, Murakami S, Suzuki M, Nakagawa A, Yamashita E et al. (2006) Crystal structure of the DsbB-DsbA complex reveals a mechanism of disulfide bond generation. Cell 127: 789-801. doi:10.1016/j.cell.2006.10.034. PubMed: 17110337. (Pubitemid 44716258)
40. Malojciæ G, Owen RL, Grimshaw JP, Glockshuber R (2008) Preparation and structure of the charge-transfer intermediate of the transmembrane redox catalyst DsbB. FEBS Lett 582: 3301-3307. doi:10.1016/j.febslet.2008.07.063. PubMed: 18775700.
41. UniProt Consortium (2012) Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 40: D71-D75. doi:10.1093/nar/ gkr981. PubMed: 22102590.
42. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. doi:10.1093/bioinformatics/btm404. PubMed: 17846036. (Pubitemid 350162903)
43. Heras B, Totsika M, Jarrott R, Shouldice SR, Guncar G et al. (2010) Structural and functional characterization of three DsbA paralogues from Salmonella enterica serovar typhimurium. J Biol Chem 285: 18423-18432. doi:10.1074/jbc.M110.101360. PubMed: 20233716.
44. Bouwman CW, Kohli M, Killoran A, Touchie GA, Kadner RJ et al. (2003) Characterization of SrgA, a Salmonella enterica serovar Typhimurium virulence plasmid-encoded paralogue of the disulfide oxidoreductase DsbA, essential for biogenesis of plasmid-encoded fimbriae. J Bacteriol 185: 991-1000. doi:10.1128/JB.185.3.991-1000.2003. PubMed: 12533475. (Pubitemid 36139458)
45. Hiniker A, Bardwell JC (2004) In vivo substrate specificity of periplasmic disulfide oxidoreductases. J Biol Chem 279: 12967-12973. PubMed: 14726535. (Pubitemid 38445872)
46. Inaba K, Ito K (2008) Structure and mechanisms of the DsbB-DsbA disulfide bond generation machine. Biochim Biophys Acta 1783: 520-529. doi:10.1016/j.bbamcr.2007.11.006. PubMed: 18082634.
47. Paxman JJ, Borg NA, Horne J, Thompson PE, Chin Y et al. (2009) 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. doi:10.1074/jbc.M109.011502. PubMed: 19389711.
48. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D et al. (2009) Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis 48: 1-12. doi:10.1086/591855. PubMed: 19035777.
49. Keynan Y, Rubinstein E (2007) The changing face of Klebsiella pneumoniae infections in the community. Int J Antimicrob Agents 30: 385-389. doi:10.1016/j.ijantimicag.2007.06.019. PubMed: 17716872. (Pubitemid 47498960)
50. Dailey FE, Berg HC (1993) Mutants in disulfide bond formation that disrupt flagellar assembly in Escherichia coli. Proc Natl Acad Sci U S A 90: 1043-1047. doi:10.1073/pnas.90.3.1043. PubMed: 8503954. (Pubitemid 23053947)
51. Lafaye C, Iwema T, Carpentier P, Jullian-Binard C, Kroll JS et al. (2009) Biochemical and structural study of the homologues of the thiol-disulfide oxidoreductase DsbA in Neisseria meningitidis. J Mol Biol 392: 952-966. doi:10.1016/j.jmb.2009.07.056. PubMed: 19631659.
52. Hillson DA, Lambert N, Freedman RB (1984) Formation and isomerization of disulfide bonds in proteins: protein disulfide-isomerase. Methods Enzymol 107: 281-294. doi:10.1016/0076-6879(84)07018-X. PubMed: 6503714.
53. Premkumar L, Heras B, Duprez W, Walden P, Halili M et al. (2013) Rv2969c, essential for optimal growth in Mycobacterium tuberculosis, is a DsbA-like enzyme that interacts with VKOR-derived peptides and has atypical features of DsbA-like disulfide oxidases. Acta Crystallogr D Biol Crystallogr 69: 1981-1994. doi:10.1107/S0907444913017800. PubMed: 24100317.
54. Walden PM, Heras B, Chen KE, Halili MA, Rimmer K et al. (2012) The 1.2 Å resolution crystal structure of TcpG, the Vibrio cholerae DsbA disulfide-forming protein required for pilus and cholera-toxin production. Acta Crystallogr D Biol Crystallogr 68: 1290-1302. doi:10.1107/S0907444912026388. PubMed: 22993083.
55. Guddat LW, Bardwell JC, Zander T, Martin JL (1997) The uncharged surface features surrounding the active site of Escherichia coli DsbA are conserved and are implicated in peptide binding. Protein Sci 6: 1148-1156. doi:10.1002/pro.5560060603. PubMed: 9194175. (Pubitemid 27260149)
56. Horne J, d'Auvergne EJ, Coles M, Velkov T, Chin Y et al. (2007) Probing the flexibility of the DsbA oxidoreductase from Vibrio cholerae - a 15N - 1H heteronuclear NMR relaxation analysis of oxidized and reduced forms of DsbA. J Mol Biol 371: 703-716. doi:10.1016/j.jmb.2007.05.067. PubMed: 17585933. (Pubitemid 47087822)
57. Guddat LW, Bardwell JC, Glockshuber R, Huber-Wunderlich M, Zander T et al. (1997) Structural analysis of three His32 mutants of DsbA: support for an electrostatic role of His32 in DsbA stability. Protein Sci 6: 1893-1900. doi:10.1002/pro.5560060910. PubMed: 9300489. (Pubitemid 27391270)
58. Schirra HJ, Renner C, Czisch M, Huber-Wunderlich M, Holak TA et al. (1998) Structure of reduced DsbA from Escherichia coli in solution. Biochemistry 37: 6263-6276. doi:10.1021/bi980136y. PubMed: 9572841. (Pubitemid 28213644)
59. Guddat LW, Bardwell JC, Martin JL (1998) Crystal structures of reduced and oxidized DsbA: investigation of domain motion and thiolate stabilization. Structure 6: 757-767. doi:10.1016/S0969-2126(98)00077-X. PubMed: 9655827. (Pubitemid 28301209)
60. Ho J, Tambyah PA, Paterson DL (2010) Multiresistant Gram-negative infections: a global perspective. Curr Opin Infect Dis 23: 546-553. doi:10.1097/QCO.0b013e32833f0d3e. PubMed: 20802331.
61. Clatworthy AE, Pierson E, Hung DT (2007) Targeting virulence: a new paradigm for antimicrobial therapy. Nat Chem Biol 3: 541-548. doi:10.1038/nchembio.2007.24. PubMed: 17710100. (Pubitemid 47294400)
62. Rasko DA, Sperandio V (2010) Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9: 117-128. doi:10.1038/nrd3013. PubMed: 20081869.
63. Alksne LE, Projan SJ (2000) Bacterial virulence as a target for antimicrobial chemotherapy. Curr Opin Biotechnol 11: 625-636. doi:10.1016/S0958-1669(00)00155-5. PubMed: 11102800.
64. Lee YM, Almqvist F, Hultgren SJ (2003) Targeting virulence for antimicrobial chemotherapy. Curr Opin Pharmacol 3: 513-519. doi:10.1016/j.coph. 2003.04.001. PubMed: 14559097. (Pubitemid 37221132)
65. Barczak AK, Hung DT (2009) Productive steps toward an antimicrobial targeting virulence. Curr Opin Microbiol 12: 490-496. doi:10.1016/j.mib.2009.06. 012. PubMed: 19631578.
66. Pinkner JS, Remaut H, Buelens F, Miller E, Aberg V et al. (2006) Rationally designed small compounds inhibit pilus biogenesis in uropathogenic bacteria. Proc Natl Acad Sci U S A 103: 17897-17902. doi:10.1073/pnas. 0606795103. PubMed: 17098869. (Pubitemid 44852257)
67. Felise HB, Nguyen HV, Pfuetzner RA, Barry KC, Jackson SR et al. (2008) An inhibitor of gram-negative bacterial virulence protein secretion. Cell Host Microbe 4: 325-336. doi:10.1016/j.chom.2008.08.001. PubMed: 18854237.
68. Jacob-Dubuisson F, Pinkner J, Xu Z, Striker R, Padmanhaban A et al. (1994) PapD chaperone function in pilus biogenesis depends on oxidant and chaperone-like activities of DsbA. Proc Natl Acad Sci U S A 91: 11552-11556. doi:10.1073/pnas.91.24.11552. PubMed: 7972100. (Pubitemid 24356382)
69. Miki T, Okada N, Danbara H (2004) Two periplasmic disulfide 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. doi:10.1074/jbc.M402760200. PubMed: 15169785. (Pubitemid 39318093)
70. Lin D, Rao CV, Slauch JM (2008) 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. doi:10.1128/JB.01323-07. PubMed: 17951383.
71. Jackson MW, Plano GV (1999) DsbA is required for stable expression of outer membrane protein YscC and for efficient Yop secretion in Yersinia pestis. J Bacteriol 181: 5126-5130. PubMed: 10438793. (Pubitemid 29383552)
72. Zav'yalov VP, Chernovskaya TV, Chapman DA, Karlyshev AV, MacIntyre S et al. (1997) Influence of the conserved disulphide bond, exposed to the putative binding pocket, on the structure and function of the immunoglobulin-like molecular chaperone Caf1M of Yersinia pestis. Biochem J 324 (2): 571-578. PubMed: 9182720. (Pubitemid 27268004)
73. Zhang HZ, Donnenberg MS (1996) DsbA is required for stability of the type IV pilin of enteropathogenic escherichia coli. Mol Microbiol 21: 787-797. doi:10.1046/j.1365-2958.1996.431403.x. PubMed: 8878041.
74. Sauvonnet N, Pugsley AP (1998) The requirement for DsbA in pullulanase secretion is independent of disulphide bond formation in the enzyme. Mol Microbiol 27: 661-667. doi:10.1046/j.1365-2958.1998.00722.x. PubMed: 9489677. (Pubitemid 28045747)
75. Pugsley AP, Bayan N, Sauvonnet N (2001) Disulfide bond formation in secreton component PulK provides a possible explanation for the role of DsbA in pullulanase secretion. J Bacteriol 183: 1312-1319. doi:10.1128/JB.183.4.1312- 1319.2001. PubMed: 11157944. (Pubitemid 32107727)
76. Inaba K, Murakami S, Nakagawa A, Iida H, Kinjo M et al. (2009) Dynamic nature of disulphide bond formation catalysts revealed by crystal structures of DsbB. EMBO J 28: 779-791. doi:10.1038/emboj.2009.21. PubMed: 19214188.