Characterization of two UDP-Gal: GalNAc-diphosphate-lipid β1,3-galactosyltransferases WbwC from Escherichia coli serotypes O104 and O5

Journal of Bacteriology

Volumn 196, Issue 17, 2014, Pages 3122-3133

  Wang, Shuo ^a   Czuchry, Diana ^a   Liu, Bin ^b   Vinnikova, Anna N ^a   Gao, Yin ^a   Vlahakis, Jason Z ^a   Szarek, Walter A ^a   Wang, Lei ^b   Feng, Lu ^b   Brockhausen, Inka ^a  

^a QUEEN S UNIVERSITY   (Canada)

^b NANKAI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALIPHATIC COMPOUND; ASPARTIC ACID; BACTERIAL ENZYME; CANCER ANTIBODY; CARBON; GALACTOSIDASE; GALACTOSYLTRANSFERASE; GLUCAN SYNTHASE; IMIDAZOLE DERIVATIVE; MANGANESE; O GLYCANASE; THOMSEN FRIEDENREICH ANTIBODY; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GALACTOSE N ACETYLGALACTOSAMINE DIPHOSPHATE LIPID BETA 1,3 GALACTOSYLTRANSFERASE WBWC ECO104; URIDINE DIPHOSPHATE GALACTOSE N ACETYLGALACTOSAMINE DIPHOSPHATE LIPID BETA 1,3 GALACTOSYLTRANSFERASE WBWC ECO5;

ARTICLE; CARBOHYDRATE SYNTHESIS; CATALYSIS; CONTROLLED STUDY; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ENTEROHEMORRHAGIC ESCHERICHIA COLI O104; ENTEROHEMORRHAGIC ESCHERICHIA COLI O5; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MUTAGENESIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN DOMAIN; SEQUENCE ANALYSIS;

AMINO ACID SEQUENCE; ENTEROHEMORRHAGIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GALACTOSYLTRANSFERASES; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; SEROTYPING;

EID: 84905453308     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.01698-14     Document Type: Article

References (53)

1. Ho TD, Waldor MK. 2007. Enterohemorrhagic Escherichia coli O157:H7 Gal mutants are sensitive to bacteriophage P1 and defective in intestinal colonization. Infect. Immun. 75:1661-1666. http://dx.doi.org/10.1128/IAI.01342-06.
2. Raetz CR, Whitfield C. 2002. Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71:635-700. http://dx.doi.org/10.1146/annurev.biochem.71.110601.135414.
3. Sheng H, Lim JY, Watkins MK, Minnich SA, Hovde CJ. 2008. Characterization of an Escherichia coli O157:H7 O-antigen deletion mutant and effect of the deletion on bacterial persistence in the mouse intestine and colonization at the bovine terminal rectal mucosa. Appl. Environ. Microbiol. 74:5015-5022. http://dx.doi.org/10.1128/AEM.00743-08.
4. Strauss J, Burnham NA, Camesano TA. 2009. Atomic force microscopy study of the role of LPS O-antigen on adhesion of E. coli. J. Mol. Recognit. 22:347-355. http://dx.doi.org/10.1002/jmr.955.
5. Zhang L, Radziejewska-Lebrecht J, Krajewska-Pietrasik D, Toivanen P, Skurnik M. 1997. Molecular and chemical characterization of the lipopolysaccharide O-antigen and its role in the virulence of Yersinia enterocolitica serotype O8. Mol. Microbiol. 23:63-76. http://dx.doi.org/10.1046/j.1365-2958.1997.1871558.x.
6. Reeves PR, Hobbs M, Valvano MA, Skurnik M, Whitfield C, Coplin D, Kido N, Klena J, Maskell D, Raetz CR. 1996. Bacterial polysaccharide synthesis and gene nomenclature. Trends Microbiol. 4:495-503. http://dx.doi.org/10.1016/S0966-842X(97)82912-5.
7. Shimizu T, Yamasaki S, Tsukamoto T, Takeda Y. 1999. Analysis of the genes responsible for the O-antigen synthesis in enterohaemorrhagic Escherichia coli O157. Microb. Pathog. 26:235-247. http://dx.doi.org/10.1006/mpat.1998.0253.
8. Reeves PR. 1994. Biosynthesis and assembly of lipopolysaccharide. New Comp. Biochem. 27:281-314. http://dx.doi.org/10.1016/S0167-7306(08) 60416-0.
9. Whitfield C. 1995. Biosynthesis of lipopolysaccharide O antigens. Trends Microbiol. 3:178-185. http://dx.doi.org/10.1016/S0966-842X(00)88917-9.
10. Qin J, Cui Y, Zhao X, Rohde H, Liang T, Wolters M, Li D, Belmar Campos C, Christner M, Song Y, Yang R. 2011. Identification of the Shiga toxin-producing Escherichia coli O104:H4 strain responsible for a food poisoning outbreak in Germany by PCR. J. Clin. Microbiol. 49: 3439-3440. http://dx.doi.org/10.1128/JCM.01312-11.
11. Creydt VP, Nuñez P, Boccoli J, Silberstein C, Zotta E, Goldstein J, Ibarra C. 2006. Role of the Shiga toxin in the hemolytic uremic syndrome. Medicina (B. Aires) 66(Suppl 3):S11-S15. (In Spanish.)
12. Frank C, Werber D, Cramer JP, Askar M, Faber M, an der Heiden M, Bernard H, Fruth A, Prager R, Spode A, Wadl M, Zoufaly A, Jordan S, Kemper MJ, Follin P, Müller L, King LA, Rosner B, Buchholz U, Stark K, Krause G, Investigation Team HUS. 2011. Epidemic profile of Shigatoxin- producing Escherichia coli O104:H4 outbreak in Germany. N. Engl. J. Med. 365:1771-1780. http://dx.doi.org/10.1056/NEJMoa1106483
13. Muniesa M, Hammerl JA, Hertwig S, Appel B, Brüssow H. 2012. Shiga toxin-producing Escherichia coli O104:H4: a new challenge for microbiology. Appl. Environ. Microbiol. 78:4065-4073. http://dx.doi.org/10.1128/AEM.00217-12.
14. Gamian A, Romanowska E, Ulrich J, Defaye J. 1992. The structure of the sialic acid-containing Escherichia coli O104 O-specific polysaccharide and its linkage to the core region in lipopolysaccharide. Carbohydr. Res. 236: 195-208. http://dx.doi.org/10.1016/0008-6215(92)85016-S.
15. Urbina F, Nordmark EL, Yang Z, Weintraub A, Scheutz F, Widmalm G. Structural elucidation of the O-antigenic polysaccharide from the enteroaggregative Escherichia coli strain 180/C3 and its immunochemical relationship with E. coli O5 and O65. Carbohydr. Res. 340:645-650. http://dx.doi.org/10.1016/j.carres.2005.01.001.
16. Brockhausen I, Gao Y. 2012. Structural glycobiology, p 177-214. In Yuriev E, Ramsland PA (ed), Structural glycobiology: applications in cancer research. CRC Press, Taylor & Francis Group, Boca Raton, FL.
17. Springer GF. 1997. Immunoreactive T and Tn epitopes in cancer diagnosis, prognosis, and immunotherapy. J. Mol. Med. 75:594-602. http://dx.doi.org/10.1007/s001090050144.
18. Wang L, Briggs CE, Rothemund D, Fratamico P, Luchansky JB, Reeves PR. 2001. Sequence of the E. coli O104 antigen gene cluster and identification of O104 specific genes. Gene 270:231-236. http://dx.doi.org/10.1016/S0378-1119(01)00471-1.
19. Rush JS, Alaimo C, Robbiani R, Wacker M, Waechter CJ. 2010. A novel epimerase that converts GlcNAc-P-P-undecaprenol to GalNAc-P-Pundecaprenol in Escherichia coli O157. J. Biol. Chem. 285:1671-1680. http://dx.doi.org/10.1074/jbc. M109.061630.
20. Freinkman E, Chng SS, Kahne D. 2011. The complex that inserts lipopolysaccharide into the bacterial outer membrane forms a two-protein plug-and-barrel. Proc. Natl. Acad. Sci. U. S. A. 108:2486-2491. http://dx.doi.org/10.1073/pnas.1015617108.
21. Wang L, Reeves PR. 1998. Organization of Escherichia coli O157 O antigen gene cluster and identification of its specific genes. Infect. Immun. 66:3545-3551.
22. Brockhausen I, Hu B, Liu B, Lau K, Szarek WA, Wang L, Feng L. 2008. Characterization of two beta-1,3-glucosyltransferases from Escherichia coli serotypes O56 and O152. J. Bacteriol. 190:4922-4932. http://dx.doi.org/10.1128/JB.00160-08.
23. Gao Y, Liu B, Strum S, Schutzbach JS, Druzhinina TN, Utkina NS, Torgov VI, Danilov L, Veselovsky VV, Vlahakis JZ, Szarek WA, Wang L, Brockhausen I. 2012. Biochemical characterization of WbdN, a beta1,3-glucosyltransferase involved in O-antigen synthesis in enterohemorrhagic Escherichia coli O157. Glycobiology 22:1092-1102. http://dx.doi.org/10.1093/glycob/cws081.
24. Riley JG, Menggad M, Montoya-Peleaz PJ, Szarek WA, Marolda CL, Valvano MA, Schutzbach JS, Brockhausen I. 2005. The wbbD gene of E. coli strain VW187 (O7:K1) encodes a UDP-Gal: GlcNAc{alpha}- pyrophosphate-R {beta}1,3-galactosyltransferase involved in the biosynthesis of O7-specific lipopolysaccharide. Glycobiology 15:605-613.
25. Xu C, Liu B, Hu B, Han Y, Feng L, Allingham JS, Szarek WA, Wang L, Brockhausen I. 2011. Biochemical characterization of UDP-Gal:GlcNAcpyrophosphate- lipid β-1,4-Galactosyltransferase WfeD, a new enzyme from Shigella boydii type 14 that catalyzes the second step in O-antigen repeating-unit synthesis. J. Bacteriol. 193:449-459. http://dx.doi.org/10.1128/JB.00737-10.
26. Montoya-Peleaz PJ, Riley JG, Szarek WA, Valvano MA, Schutzbach JS, Brockhausen I. 2005. Identification of a UDP-Gal:GlcNAc-R galactosyltransferase activity in Escherichia coli VW187. Bioorg. Med. Chem. Lett. 15:1205-1211. http://dx.doi.org/10.1016/j.bmcl.2004.11.077.
27. Vinnikova AN, Druzhinina TN, Danilov LL, Utkina NS, Torgov VI, Veselovsky VV, Wang S, Liu B, Wang L, Brockhausen I. 2013. Synthesis of a fluorescent acceptor substrate for glycosyltransferases involved in the assembly of O-antigens of enterohemorrhagic Escherichia coli O157 and O5. Carbohydr. Res. 366:17-24. http://dx.doi.org/10.1016/j.carres.2012.11.009.
28. Brockhausen I, Benn M, Bhat S, Marone S, Riley JG, Montoya-Peleaz P, Vlahakis JZ, Paulsen H, Schutzbach JS, Szarek WA. 2006. UDP-Gal: GlcNAc-R beta1,4-galactosyltransferase-a target enzyme for drug design. Acceptor specificity and inhibition of the enzyme. Glycoconj. J. 23: 525-541.
29. Gao Y, Lazar C, Szarek WA, Brockhausen I. 2010. Specificity of β1,4-galactosyltransferase inhibition by 2-naphthyl 2-butanamido-2-deoxy-1-thio-β-D-glucopyranoside. Glycoconj. J. 27:673-684. http://dx.doi.org/10.1007/s10719-010-9312-3.
30. Gao Y, Vinnikova A, Brockhausen I. 2013. Functional identification of bacterial glucosyltransferase WbdN. Glycosyltransferases: methods and protocols in method molecular biology. Humana Press, Springer Science and Business Media, New York, NY.
31. Gao Y, Vlahakis JZ, Szarek WA, Brockhausen I. 2013. Selective inhibition of glycosyltransferases by bivalent imidazolium salts. Bioorg. Med. Chem. 21:1305-1311. http://dx.doi.org/10.1016/j.bmc.2012.12.034.
32. Visscher I, Stuart MC, Engberts JB. 2006. The influence of phenyl and phenoxy modification in the hydrophobic tails of di-n-alkyl phosphate amphiphiles on aggregate morphology. Org. Biomol. Chem. 4:707-712. http://dx.doi.org/10.1039/b514285g.
33. Bernardes GJL, Kikkeri R, Maglinao M, Laurino P, Collot M, Hong SY, Lepenies B, Seeberger PH. 2010. Design, synthesis and biological evaluation of carbohydrate-functionalized cyclodextrins and liposomes for hepatocyte- specific targeting. Org. Biomol. Chem. 8:4987-4996. http://dx.doi.org/10.1039/c0ob00372g.
34. Nakabayashi S, Warren CD, Jeanloz RW. 1986. A new procedure for the preparation of oligosaccharide oxazolines. Carbohydr. Res. 150:C7-C10. http://dx.doi.org/10.1016/0008-6215(86)80028-3.
35. Fegan N, Barlow RS, Gobius KS. 2006. Escherichia coli O157 somatic antigen is present in an isolate of E. fergusonii. Curr. Microbiol. 52:482-486. http://dx.doi.org/10.1007/s00284-005-0447-6.
36. Cheng J, Wang Q, Wang W, Wang Y, Wang L, Feng L. 2006. Characterization of E. coli O24 and O56Oantigen gene clusters reveals a complex evolutionary history of the O24 gene cluster. Curr. Microbiol. 53:470-476. http://dx.doi.org/10.1007/s00284-006-0032-7.
37. Yi W, Perali RS, Eguchi H, Motari E, Woodward R, Wang PG. 2008. Characterization of a bacterial β-1,3-galactosyltransferase with application in the synthesis of tumor-associated T-antigen mimics. Biochemistry 47:1241-1248. http://dx.doi.org/10.1021/bi7020712.
38. Liu XW, Xia C, Li L, Guan WY, Pettit N, Zhang HC, Chen M, Wang PG. 2009. Characterization and synthetic application of a novel beta1,3-galactosyltransferase from Escherichia coli O55:H7. Bioorg. Med. Chem. 17:4910-4915. http://dx.doi.org/10.1016/j.bmc.2009.06.005.
39. Gao Y, Aryal RP, Ju T, Cummings Gahlay RDG, Jarvis DL, Matta KL, Vlahakis JZ, Szarek WA, Brockhausen I. 2013. Acceptor specificities and selective inhibition of recombinant human Gal- and GlcNAc-transferases that synthesize core structures 1, 2, 3 and 4 of O-glycans. Biochim. Biophys. Acta 1830:4274-4281. http://dx.doi.org/10.1016/j.bbagen.2013.04.001.
40. Breton C, Snajdrová L, Jeanneau C, Koca J, Imberty A. 2006. Structures and mechanisms of glycosyltransferases. Glycobiology 16:29R-37R. http://dx.doi.org/10.1093/glycob/cwj016.
41. Ünligil UM, Rini JM. 2000. Glycosyltransferase structure and mechanism. Curr. Opin. Struct. Biol. 10:510-517. http://dx.doi.org/10.1016/S0959-440X(00)00124-X.
42. Liu B, Knirel YA, Feng L, Perepelov AV, Senchenkova SN, Wang Q, Reeves PR, Wang L. 2008. Structure and genetics of Shigella O antigens. FEMS Microbiol. Rev. 32:627-653. http://dx.doi.org/10.1111/j.1574-6976.2008.00114.x.
43. Mann FM, Prisic S, Davenport EK, Determan MK, Coates RM, Peters RJ. 2010. A single residue switch for Mg(2+)-dependent inhibition characterizes plant class II diterpene cyclases from primary and secondary metabolism. J. Biol. Chem. 285:20558-20563. http://dx.doi.org/10.1074/jbc. M110.123307.
44. Peters RJ, Croteau RB. 2002. Abietadiene synthase catalysis: conserved residues involved in protonation-initiated cyclization of geranylgeranyl diphosphate to (+)-copalyl diphosphate. Biochemistry 41:1836-1842. http://dx.doi.org/10.1021/bi011879d.
45. Karsten U, Papsdorf G, Pauly A, Vojtesek B, Moll R, Lane EB, Clausen H, Stosiek P, Kasper M. 1993. Subtypes of non-transformed human mammary epithelial cells cultured in vitro: histo-blood group antigen H type 2 defines basal cell-derived cells. Differentiation 54:55-56. http://dx.doi.org/10.1111/j.1432-0436.1993.tb01588.x.
46. Brocke C, Kunz H. 2002. Synthesis of tumor-associated glycopeptide antigens. Bioorg. Med. Chem. 10:3085-3112. http://dx.doi.org/10.1016/S0968-0896(02)00135-9.
47. Bernatchez S, Gilbert M, Blanchard M-C, Karwaski M-F, Li J, DeFrees S, WakarchukWW.2007. Variants of the β1,3-galactosyltransferase CgtB from the bacterium Campylobacter jejuni have distinct acceptor specificities. Glycobiology 17:1333-1343. http://dx.doi.org/10.1093/glycob/cwm090.
48. Brockhausen I, Riley JG, Joynt M, Yang X, Szarek WA. 2008. Acceptor substrate specificity of UDP-Gal:GlcNAc-R β1,3-galactosyltransferase (WbbD) from Escherichia coli O7:K1. Glycoconj. J. 25:663-673. http://dx.doi.org/10.1007/s10719-008-9127-7.
49. Yi W, Yao Q, Zhang Y, Motari E, Lin S, Wang PG. 2006. The wbnH gene of Escherichia coli O86:H2 encodes an β-1,3-N-acetylgalactosaminyl transferase involved in the O-repeating unit biosynthesis. Biochem. Biophys. Res. Commun. 344:631-639. http://dx.doi.org/10.1016/j.bbrc.2006.03.181.
50. Brockhausen I, Larsson EA, Hindsgaul O. 2008. A very simple synthesis of GlcNAc-alpha-pyrophosphoryl-decanol: a substrate for the assay of a bacterial galactosyltransferase. Bioorg. Med. Chem. Lett. 18:804-807. http://dx.doi.org/10.1016/j.bmcl.2007.11.031.
51. Riley JG, Xu C, Brockhausen I. 2010. Synthesis of acceptor substrate analogs for the study of glycosyltransferases involved in the second step of the biosynthesis of O-antigen repeating units. Carbohydr. Res. 345:586-597. http://dx.doi.org/10.1016/j.carres.2009.12.022.
52. Samuel G, Reeves P. 2003. Biosynthesis of O-antigens: genes and pathways involved in nucleotide sugar precursor synthesis and O-antigen assembly. Carbohydr. Res. 338:2503-2519. http://dx.doi.org/10.1016/j.carres.2003.07.009.
53. Valvano MA. 2003. Export of O-specific lipopolysaccharide. Front. Biosci. 8:s452-s471. http://dx.doi.org/10.2741/1079.