The PAPS-independent aryl sulfotransferase and the alternative disulfide bond formation system in pathogenic bacteria

Antioxidants and Redox Signaling

Volumn 13, Issue 8, 2010, Pages 1247-1259

  Malojčić, Goran ^a   Glockshuber, Rudi ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

1 NAPHTHOL; 1 NAPHTHYLSULFATE; 2 NAPHTHYLSULFATE; 4 ACETYLPHENYLSULFATE; 4 METHYLUMBELLIFERYLSULFATE; 4 NITROPHENYLSULFATE; 9 PHENANTHROL; ADENOSINE 3' PHOSPHATE 5' PHOSPHOSULFATE; ADRENALIN; AMOXICILLIN; ARYL SULFOTRANSFERASE; BETA LACTAM ANTIBIOTIC; CEFADROXIL; CEFOPERAZONE; ESTRADIOL; GALLIC ACID; PARACETAMOL; PHENOL DERIVATIVE; PICOSULFATE; PICOSULFATE SODIUM; RESORCINOL; TYRAMINE; TYROSINE DERIVATIVE; TYROSINE METHYL ESTER; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AZOTOBACTER VINELANDII; BACTERIAL INFECTION; BACTERIAL VIRULENCE; BACTERIUM; CAMPYLOBACTER CURVUS; CAMPYLOBACTER FETUS; CAMPYLOBACTER JEJUNI; CAMPYLOBACTER LARI; CATALYSIS; CHEMICAL STRUCTURE; CITROBACTER FREUNDII; DISULFIDE BOND; ENZYME REGULATION; ENZYME STRUCTURE; ESCHERICHIA COLI K 12; GENOMICS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROKARYOTE; REVIEW; SALMONELLA ENTERICA; STRUCTURAL HOMOLOGY; SULFATION; THREE DIMENSIONAL IMAGING; UPREGULATION; UROPATHOGENIC ESCHERICHIA COLI;

ARYLSULFOTRANSFERASE; BACTERIA; DISULFIDES; HUMANS; OXIDATION-REDUCTION; PHOSPHOADENOSINE PHOSPHOSULFATE; PROTEIN FOLDING;

BACTERIA (MICROORGANISMS); PROKARYOTA;

EID: 77956333061     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2010.3119     Document Type: Review

References (77)

1. Baek MC, Kim SK, Kim DH, Kim BK, and Choi EC. Cloning and sequencing of the Klebsiella K-36 astA gene, encoding an arylsulfate sulfotransferase. Microbiol Immunol 40: 531-537, 1996.
2. Bardwell JC. Building bridges: disulphide bond formation in the cell. Mol Microbiol 14: 199-205, 1994.
3. 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.
4. Bardwell JC, McGovern K, and Beckwith J. Identification of a protein required for disulfide bond formation in vivo. Cell 67: 581-589, 1991.
5. 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.
6. Bojarova P and Williams SJ. Sulfotransferases, sulfatases and formylglycine-generating enzymes: a sulfation fascination. Curr Opin Chem Biol 12: 573-581, 2008.
7. Bouwman CW, Kohli M, Killoran A, Touchie GA, Kadner RJ, and Martin NL. 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, 2003.
8. Cameron DR and Thatcher GRJ. Mechanisms of reaction of sulfate esters: a molecular orbital study of associative sul-furyl group transfer, intramolecular migration and pseu-dorotation. J Org Chem 61: 5986-5997, 1996.
9. Chai CL and Lowe G. The mechanism and stereochemical course of sulfuryl transfer catalysed by the aryl sulfo-transferase from Eubacterium A-44. Bioorg Chem 20: 181-188, 1992.
10. Chapman E, Best MD, Hanson SR, and Wong CH. Sulfo-transferases: structure, mechanism, biological activity, inhibition, and synthetic utility. Angew Chem Int Ed Engl 43: 3526-3548, 2004.
11. Chen VM, Ahamed J, Versteeg HH, Berndt MC, Ruf W, and Hogg PJ. Evidence for activation of tissue factor by an allo-steric disulfide bond. Biochemistry 45: 12020-12028, 2006.
12. Chen VM and Hogg PJ. Allosteric disulfide bonds in thrombosis and thrombolysis. J Thromb Haemost 4: 2533-2541, 2006.
13. Cook PF and Cleland WW. Enzyme Kinetics and Mechanism. London: Garland Science, 2007.
14. Devi VS, Sprecher CB, Hunziker P, Mittl PR, Bosshard HR, and Jelesarov I. Disulfide formation and stability of a cys-teine-rich repeat protein from Helicobacter pylori. Biochemistry 45: 1599-1607, 2006.
15. 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.
16. Doron-Faigenboim A, Stern A, Mayrose I, Bacharach E, and Pupko T. Selecton: a server for detecting evolutionary forces at a single amino-acid site. Bioinformatics 21: 2101-2103, 2005.
17. Fan SW, George RA, Haworth NL, Feng LL, Liu JY, and Wouters MA. Conformational changes in redox pairs of protein structures. Protein Sci 18: 1745-1765, 2009.
18. Gamage N, Barnett A, Hempel N, Duggleby RG, Windmill KF, Martin JL, and McManus ME. Human sulfotransferases and their role in chemical metabolism. Toxicol Sci 90: 5-22, 2006.
19. Gibson KE, Kobayashi H, and Walker GC. Molecular determinants of a symbiotic chronic infection. Annu Rev Genet 42: 413-441, 2008.
20. Godlewska R, Dzwonek A, Mikula M, Ostrowski J, Pawlowski M, Bujnicki JM, and Jagusztyn-Krynicka EK. Helicobacter pylori protein oxidation influences the colonization process. Int J Med Microbiol 296: 321-324, 2006.
21. Graafland T, Wagenaar A, Kirby AJ, and Engberts JBFN. Structure and reactivity in intramolecular catalysis. catalysis of sulfonamide hydrolysis by the neighboring carboxyl group. J Am Chem Soc 101: 6981-6991, 1979.
22. Grimshaw J, Stirnimann CU, Brozzo MS, Malojcic G, Grütter MG, Capitani G, and Glockshuber R. DsbL and DsbI form a specific dithiol oxidase system for periplasmic arylsulfate sulfotransferase in uropathogenic E. coli. J Mol Biol doi:10.1016=j.jmb.2008.05.031, 2008.
23. Haworth NL, Feng LL, and Wouters MA. High torsional energy disulfides: relationship between cross-strand dis-ulfides and right-handed staples. J Bioinformat Comput Biol 4: 155-168, 2006.
24. Haworth NL, Gready JE, George RA, and Wouters MA. Evaluating the stability of disulfide bridges in proteins: a torsional potential energy surface for diethyl disulfide. Mol Simulat 33: 475-485, 2007.
25. 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.
26. Hogg PJ. Contribution of allosteric disulfide bonds to regulation of hemostasis. J Thromb Haemost 7(suppl 1): 13-16, 2009.
27. 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.
28. Inaba K. Disulfide bond formation system in Escherichia coli. J Biochem 146: 591-597, 2009.
29. 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.
30. Jakoby WB and Ziegler DM. The enzymes of detoxication. J Biol Chem 265: 20715-20718, 1990.
31. Jawad Z and Paoli M. Novel sequences propel familiar folds. Structure 10: 447-454, 2002.
32. Kadokura H, Katzen F, and Beckwith J. Protein disulfide bond formation in prokaryotes. Annu Rev Biochem 72: 111-135, 2003.
33. Kang JW, Jeong YJ, Kwon AR, Yun HJ, Kim DH, and Choi EC. Cloning, sequence analysis, and characterization of the astA gene encoding an arylsulfate sulfotransferase from Ci-trobacter freundii. Arch Pharm Res 24: 316-322, 2001.
34. Kang JW, Kwon AR, Kim DH, and Choi EC. Cloning and sequencing of the astA gene encoding arylsulfate sulfo-transferase from Salmonella typhimurium. Biol Pharm Bull 24: 570-574, 2001.
35. Kim B, Hyun YJ, Lee KS, Kobashi K, and Kim DH. Cloning, expression and purification of arylsulfate sulfo-transferase from Eubacterium A-44. Biol Pharm Bull 30: 11-14, 2007.
36. Kim DH, Hyun SH, Shim SB, and Kobashi K. The role of intestinal bacteria in the transformation of sodium pico-sulfate. Jpn J Pharmacol 59: 1-5, 1992.
37. Kim DH, Kim HS, Imamura L, and Kobashi K. Kinetic studies on a sulfotransferase from Klebsiella K-36, a rat intestinal bacterium. Biol Pharm Bull 17: 543-545, 1994.
38. Kim DH, Kim HS, and Kobashi K. Purification and characterization of novel sulfotransferase obtained from Klebsiella K-36, an intestinal bacterium of rat. J Biochem 112: 456-460, 1992.
39. Kim DH and Kobashi K. Kinetic studies on a novel sulfo-transferase from Eubacterium A-44, a human intestinal bacterium. J Biochem 109: 45-48, 1991.
40. Kim DH and Kobashi K. The role of intestinal flora in metabolism of phenolic sulfate esters. Biochem Pharmacol 35: 3507-3510, 1986.
41. Kim DH, Konishi L, and Kobashi K. Purification, characterization and reaction mechanism of novel arylsulfo-transferase obtained from an anaerobic bacterium of human intestine. Biochim Biophys Acta 872: 33-41, 1986.
42. Kim DH, Yoon HK, Koizumi M, and Kobashi K. Sulfation of phenolic antibiotics by sulfotransferase obtained from a human intestinal bacterium. Chem Pharm Bull (Tokyo) 40: 1056-1057, 1992.
43. Kobashi K, Fukaya Y, Kim DH, Akao T, and Takebe S. A novel type of aryl sulfotransferase obtained from an anaerobic bacterium of human intestine. Arch Biochem Biophys 245: 537-539, 1986.
44. Kobashi K, Kim D-H, Morikawa T. A novel type of ar-ylsulfotransferase. J Protein Chem 6: 237-244, 1987.
45. Kwon AR, Oh TG, Kim DH, and Choi EC. Molecular cloning of the arylsulfate sulfotransferase gene and characterization of its product from Enterobacter amnigenus AR-37. Protein Expr Purif 17: 366-372, 1999.
46. Kwon AR, Yun HJ, and Choi EC. Kinetic mechanism and identification of the active site tyrosine residue in Enterobacter amnigenus arylsulfate sulfotransferase. Biochem Biophys Res Commun 285: 526-529, 2001.
47. Lasica AM and Jagusztyn-Krynicka EK. The role of Dsb proteins of gram-negative bacteria in the process of patho-genesis. FEMS Microbiol Rev 31: 626-636, 2007.
48. Lee NS, Kim BT, Kim DH, and Kobashi K. Purification and reaction mechanism of arylsulfate sulfotransferase from Haemophilus K-12, a mouse intestinal bacterium. J Biochem 118: 796-801, 1995.
49. Lide DR. CRC Handbook of Chemistry and Physics. Boca Raton, FL: Taylor & Francis Group, 2006=2007.
50. Lin D, Kim B, and Slauch JM. DsbL and DsbI contribute to periplasmic disulfide bond formation in Salmonella enterica serovar Typhimurium. Microbiology (Reading, England) 155: 4014-4024, 2009.
51. Lloyd AL, Rasko DA, and Mobley HL. Defining genomic islands and uropathogen-specific genes in uropathogenic Escherichia coli. J Bacteriol 189: 3532-3546, 2007.
52. Malojcic G. Structure and function of the wild-type trans-membrane oxidoreductase DsbB and the arylsulfate sulfo-transferase from uropathogenic Escherichia coli. PhD thesis: ETH Zurich, Zurich, Switzerland, 2008.
53. Malojcic G and Glockshuber R. Disulfide-bond formation and isomerization in prokaryotes. In: RSC Biomolecular Sciences, edited by Buchner J and Kiefhaber T. Weinheim: Royal Society of Chemistry, 2009, pp. 19-40.
54. Malojcic G, Owen RL, Grimshaw JP, Brozzo MS, Dreher-Teo H, and Glockshuber R. A structural and biochemical basis for PAPS-independent sulfuryl transfer by aryl sulfo-transferase from uropathogenic Escherichia coli. Proc Natl Acad Sci\USA 105: 19217-19222, 2008.
55. 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.
56. 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.
57. Mathew JA, Tan YP, Srinivasa Rao PS, Lim TM, and Leung KY. Edwardsiella tarda mutants defective in siderophore production, motility, serum resistance and catalase activity. Microbiol (Reading, England) 147: 449-457, 2001.
58. Mobley HL, Green DM, Trifillis AL, Johnson DE, Chippendale GR, Lockatell CV, Jones BD, and Warren JW. Pyelonephritogenic Escherichia coli and killing of cultured human renal proximal tubular epithelial cells: role of hemolysin in some strains. Infect Lmmun 58: 1281-1289, 1990.
59. Mougous JD, Green RE, Williams SJ, Brenner SE, and Ber-tozzi CR. Sulfotransferases and sulfatases in mycobacteria. Chem Biol 9: 767-776, 2002.
60. Mougous JD, Petzold CJ, Senaratne RH, Lee DH, Akey DL, Lin FL, Munchel SE, Pratt MR, Riley LW, Leary JA, Berger JM, and Bertozzi CR. Identification, function and structure of the mycobacterial sulfotransferase that initiates sulfolipid-1 biosynthesis. Nat Struct Mol Biol 11: 721-729, 2004.
61. Paoli M. Protein folds propelled by diversity. Prog Biophys Mol Biol 76: 103-130, 2001.
62. 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.
63. Pi N, Yu Y, Mougous JD, and Leary JA. Observation of a hybrid random ping-pong mechanism of catalysis for NodST: a mass spectrometry approach. Protein Sci 13: 903-912, 2004.
64. Raczko AM, Bujnicki JM, Pawlowski M, Godlewska R, Lewandowska M, and Jagusztyn-Krynicka EK. Characterization of new DsbB-like thiol-oxidoreductases of Campylo-bacter jejuni and Helicobacter pylori and classification of the DsbB family based on phylogenomic, structural and functional criteria. Microbiology (Reading, England) 151: 219-231, 2005.
65. Sambrook DW Jr. Molecular Cloning: A Laboratory Manual. New York: Cold Spring Harbor Press, 2001.
66. Schmidt B, Ho L, and Hogg PJ. Allosteric disulfide bonds. Biochemistry 45: 7429-7433, 2006.
67. Smith TF, Gaitatzes C, Saxena K, and Neer EJ. The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24: 181-185, 1999.
68. Teramoto T, Adachi R, Sakakibara Y, Liu MC, Suiko M, Kimura M, and Kakuta Y. On the similar spatial arrangement of active site residues in PAPS-dependent and phenolic sulfate-utilizing sulfotransferases. FEBS Lett 583: 3091-3094, 2009.
69. Teramoto T, Sakakibara Y, Liu MC, Suiko M, Kimura M, and Kakuta Y. Snapshot of a Michaelis complex in a sulfuryl transfer reaction: crystal structure of a mouse sulfotransfer-ase, mSULT1D1, complexed with donor substrate and accepter substrate. Biochem Biophys Res Commun 383: 83-87, 2009.
70. 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.
71. 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 oxi-doreductase NmDsbA3 from Neisseria meningitidis. J Biol Chem 283: 32452-32461, 2008.
72. Voet D and Voet JG. Biochemistry. New York: John Wiley and Sons, 2004.
73. Welch RA, Burland V, Plunkett G 3rd, Redford P, Roesch P, Rasko D, Buckles EL, Liou SR, Boutin A, Hackett J, Stroud D, Mayhew GF, Rose DJ, Zhou S, Schwartz DC, Perna NT, Mobley HL, Donnenberg MS, and Blattner FR. Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli. Proc Natl Acad Sci\USA 99: 17020-17024, 2002.
74. Wouters MA, George RA, and Haworth NL. "Forbidden" disulfides: their role as redox switches. Curr Protein Peptide Sci 8: 484-495, 2007.
75. Wouters MA, Lau KK, and Hogg PJ. Cross-strand dis-ulphides in cell entry proteins: poised to act. Bioessays 26: 73-79, 2004.
76. Wunderlich M and Glockshuber R. Redox properties of protein disulfide isomerase (DsbA) from Escherichia coli. Protein Sci 2: 717-726, 1993.
77. 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.