Biosynthesis of the polymannose lipopolysaccharide O-antigens from Escherichia coli serotypes O8 and O9a requires a unique combination of single- and multiple-active site mannosyltransferases

Journal of Biological Chemistry

Volumn 287, Issue 42, 2012, Pages 35078-35091

  Greenfield, Laura K ^a   Richards, Michele R ^b   Li, Jianjun ^c   Wakarchuk, Warren W ^c   Lowary, Todd L ^c,d   Whitfield, Chris ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

^c NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^d RYERSON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ASSEMBLY SYSTEMS; BACTERIAL POLYSACCHARIDES; COMPLEMENTATION; GLYCAN STRUCTURES; GLYCANS; IN-VITRO; IN-VIVO; LIPOPOLYSACCHARIDES; MANNOPYRANOSE; MODEL SYSTEM; O-ANTIGEN; PURIFIED ENZYME; SEROTYPES; TETRASACCHARIDES;

BIOCHEMISTRY; BIOSYNTHESIS; ENZYMES; ESCHERICHIA COLI;

ANTIGENS;

CARBOHYDRATE ANTIGEN; CARBOHYDRATE DERIVATIVE; MANNOPYRANOSE; MANNOSYLTRANSFERASE; O8 ANTIGEN; O9A ANTIGEN; PROTEIN WBDA; PROTEIN WBDB; PROTEIN WBDC; UNCLASSIFIED DRUG;

AMINO ACID TRANSPORT; ANTIGEN STRUCTURE; ARTICLE; CARBOHYDRATE SYNTHESIS; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; SEROTYPE;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MANNANS; MANNOSYLTRANSFERASES; O ANTIGENS; POLYISOPRENYL PHOSPHATES;

EID: 84867429653     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.401000     Document Type: Article

References (70)

1. Raetz, C. R., and Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu. Rev. Biochem. 71, 635-700 (Pubitemid 34800232)
2. Orskov, I., Orskov, F., Jann, B., and Jann, K. (1977) Serology, chemistry, and genetics of O- and K-antigens of Escherichia coli. Bacteriol. Rev. 41, 667-710 (Pubitemid 8194910)
3. Stenutz, R., Weintraub, A., and Widmalm, G. (2006) The structures of Escherichia coli O-polysaccharide antigens. FEMS Microbiol. Rev. 30, 382-403
4. Sperandeo, P., Dehò, G., and Polissi, A. (2009) The lipopolysaccharide transport system of Gram-negative bacteria. Biochim. Biophys. Acta 1791, 594-602
5. Fitzgerald-Chandler, D. K., and Jann, K. (1971) Studies of the biosynthesis of the O9 antigen from Escherichia coli O9:K30(A):H12. Eur. J. Biochem. 24, 222-231
6. Greenfield, L. K., and Whitfield, C. (2012) Synthesis of lipopolysaccharide O-antigens by ABC transporter-dependent pathways. Carbohydr. Res. 356, 12-24
7. Saeki, A., Kido, N., Sugiyama, T., Ohta, M., Iwashita, T., Uchiya, K., and Kato, N. (1993) Isolation of rfb gene clusters directing the synthesis of O-polysaccharides consisting of mannose homopolymers and serological analysis of lipopolysaccharides. Microbiol. Immunol. 37, 601-606 (Pubitemid 23288956)
8. Sugiyama, T., Kido, N., Kato, Y., Koide, N., Yoshida, T., and Yokochi, T. (1997) Evolutionary relationship among rfb gene clusters synthesizing mannose homopolymer as O-specific polysaccharides in Escherichia coli and Klebsiella. Gene 198, 111-113
9. Sugiyama, T., Kido, N., Kato, Y., Koide, N., Yoshida, T., and Yokochi, T. (1998) Generation of Escherichia coli O9a serotype, a subtype of E. coli O9, by transfer of the wb*gene cluster of Klebsiella O3 into E. coli via recombination. J. Bacteriol. 180, 2775-2778 (Pubitemid 28213282)
10. Kido, N., and Kobayashi, H. (2000) A single amino acid substitution in a mannosyltransferase, WbdA, converts the Escherichia coli O9 polysaccharide into O9a. Generation of a new O-serotype group. J. Bacteriol. 182, 2567-2573 (Pubitemid 30212917)
11. Vinogradov, E., Frirdich, E., MacLean, L. L., Perry, M. B., Petersen, B. O., Duus, J. Ø., and Whitfield, C. (2002) Structures of lipopolysaccharides from Klebsiella pneumoniae. Eluicidation of the structure of the linkage region between core and polysaccharide O chain and identification of the residues at the non-reducing termini of the O chains. J. Biol. Chem. 277, 25070-25081 (Pubitemid 34951812)
12. Clarke, B. R., Richards, M. R., Greenfield, L. K., Hou, D., Lowary, T. L., and Whitfield, C. (2011) In vitro reconstruction of the chain termination reaction in biosynthesis of the Escherichia coli O9a O-polysaccharide. The chain-length regulator, WbdD, catalyzes the addition of methyl phosphate to the non-reducing terminus of the growing glycan. J. Biol. Chem. 286, 41391-41401
13. Kubler-Kielb, J., Whitfield, C., Katzenellenbogen, E., and Vinogradov, E. (2012) Identification of the methyl phosphate substituent at the non-reducing terminal mannose residue of the O-specific polysaccharides of Klebsiella pneumoniae O3, Hafnia alvei PCM 1223, and Escherichia coli O9/O9a LPS. Carbohydr Res. 347, 186-188
14. Kido, N., Torgov, V. I., Sugiyama, T., Uchiya, K., Sugihara, H., Komatsu, T., Kato, N., and Jann, K. (1995) Expression of the O9 polysaccharide of Escherichia coli. Sequencing of the E. coli O9 rfb gene cluster, characterization of mannosyl transferases, and evidence for an ATP-binding cassette transport system. J. Bacteriol. 177, 2178-2187
15. Clarke, B. R., Cuthbertson, L., and Whitfield, C. (2004) Nonreducing terminal modifications determine the chain length of polymannose O-antigens of Escherichia coli and couple chain termination to polymer export via an ATP-binding cassette transporter. J. Biol. Chem. 279, 35709-35718 (Pubitemid 39100575)
16. Cuthbertson, L., Kimber, M. S., and Whitfield, C. (2007) Substrate binding by a bacterial ABC transporter involved in polysaccharide export. Proc. Natl. Acad. Sci. U.S.A. 104, 19529-19534
17. Kido, N., Morooka, N., Paeng, N., Ohtani, T., Kobayashi, H., Shibata, N., Okawa, Y., Suzuki, S., Sugiyama, T., and Yokochi, T. (1997) Production of monoclonal antibody discriminating serological difference in Escherichia coli O9 and O9a polysaccharides. Microbiol. Immunol. 41, 519-525 (Pubitemid 27318088)
18. Meier-Dieter, U., Starman, R., Barr, K., Mayer, H., and Rick, P. D. (1990) Biosynthesis of enterobacterial common antigen in Escherichia coli. Biochemical characterization of Tn10 insertion mutants defective in enterobacterial common antigen synthesis. J. Biol. Chem. 265, 13490-13497
19. Meier-Dieter, U., Barr, K., Starman, R., Hatch, L., and Rick, P. D. (1992) Nucleotide sequence of the Escherichia coli rfe gene involved in the synthesis of enterobacterial common antigen. Molecular cloning of the rfe-rff gene cluster. J. Biol. Chem. 267, 746-753
20. Miller, J. H. (1972) Experiments in Molecular Genetics, pp. 432-433, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
21. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd Ed., pA3, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY
22. Datsenko, K. A., and Wanner, B. L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U.S.A. 97, 6640-6645 (Pubitemid 30412767)
23. Guzman, L. M., Belin, D., Carson, M. J., and Beckwith, J. (1995) Tight regulation, modulation, and high level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177, 4121-4130
24. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D., and Bairoch, A. (2005) in The Proteomics Protocols Handbook (Walker, J. M., ed) pp. 571-607, Humana Press, Totowa, NJ
25. Ginsberg, C., Zhang, Y. H., Yuan, Y., and Walker, S. (2006) In vitro reconstitution of two essential steps in wall teichoic acid biosynthesis. ACS Chem. Biol. 1, 25-28
26. Kanegasaki, S., and Jann, K. (1979) Demonstration by membrane reconstitution of a butanol-soluble intermediate in the biosynthesis of the O9 antigen of Escherichia coli. Eur. J. Biochem. 95, 287-293 (Pubitemid 9234051)
27. Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., and Smith, F. (1956) Acolorimetric method for the determination of sugars substances. Nature 168, 167
28. Liu, C., Skogman, F., Cai, Y., and Lowary, T. L. (2007) Synthesis of the "primer-adaptor" trisaccharide moiety of Escherichia coli O8, O9, and O9a lipopolysaccharide. Carbohydr. Res. 342, 2818-2825 (Pubitemid 350119832)
29. Hou, D., Skogman, F., and Lowary, T. L. (2008) Synthesis of 8-azidooctyl glycoside derivatives of the O-chain repeating unit of Escherichia coli O9a lipopolysaccharide and a methylated analog. Carbohydr. Res. 343, 1778-1789
30. Wakarchuk, W. W., and Cunningham, A. M. (2003) Capillary electrophoresis as an assay method for monitoring glycosyltransferase activity. Methods Mol. Biol. 213, 263-274
31. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685
32. Hitchcock, P. J., and Brown, T. M. (1983) Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154, 269-277 (Pubitemid 13115445)
33. Tsai, C. M., and Frasch, C. E. (1982) A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119, 115-119 (Pubitemid 12142846)
34. Shatzman, A. R., Gross, M. S., and Rosenberg, M. (2001) Expression using vectors with phage λ regulatory sequences. Current Protocols in Molecular Biology 11, chapter 16 unit 16.3
35. Kido, N., Sugiyama, T., Yokochi, T., Kobayashi, H., and Okawa, Y. (1998) Synthesis of Escherichia coli O9a polysaccharide requires the participation of two domains of WbdA, a mannosyltransferase encoded within the wb*gene cluster. Mol. Microbiol. 27, 1213-1221 (Pubitemid 28137973)
36. Geremia, R. A., Petroni, E. A., Ielpi, L., and Henrissat, B. (1996) Towards a classification of glycosyltransferases based on amino acid sequence similarities. Prokaryotic α-mannosyltransferases. Biochem. J. 318, 133-138 (Pubitemid 26283636)
37. Campbell, J. A., Davies, G. J., Bulone, V., and Henrissat, B. (1997) A classification of nucleotide-diphospho-sugar glycosyltransferases based on amino acid sequence similarities. Biochem. J. 326, 929-939 (Pubitemid 27438071)
38. Coutinho, P. M., Deleury, E., Davies, G. J., and Henrissat, B. (2003) An evolving hierarchical family classification for glycosyltransferases. J. Mol. Biol. 328, 307-317 (Pubitemid 36407576)
39. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy). An expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
40. Parolis, L. A., Parolis, H., and Dutton, G. G. (1986) Structural studies of the O-antigen polysaccharide of Escherichia coli 09a. Carbohydr Res. 155, 272-276
41. Jansson, P. E., Stenutz, R., and Widmalm, G. (2006) Sequence determination of oligosaccharides and regular polysaccharides using NMR spectroscopy and a novel Web-based version of the computer program CASPER. Carbohydr. Res. 341, 1003-1010
42. Lundborg, M., and Widmalm, G. (2011) Structure analysis of glycans by NMR chemical shift prediction. Anal. Chem. 83, 1514-1517
43. Jansson, P. E., Lönngren, J., Widmalm, G., Leontein, K., Slettengren, K., Svenson, S. B., Wrangsell, G., Dell, A., and Tiller, P. R. (1985) Structural studies of the O-antigen polysaccharides of Klebsiella O5 and Escherichia coli O8. Carbohydr. Res. 145, 59-66
44. Cuthbertson, L., Kos, V., and Whitfield, C. (2010) ABC transporters involved in export of cell surface glycoconjugates. Microbiol. Mol. Biol. Rev. 74, 341-362
45. Martinez-Fleites, C., Proctor, M., Roberts, S., Bolam, D. N., Gilbert, H. J., and Davies, G. J. (2006) Insights into the synthesis of lipopolysaccharide and antibiotics through the structures of two retaining glycosyltransferases from family GT4. Chem. Biol. 13, 1143-1152 (Pubitemid 44750727)
46. Steiner, K., Hagelueken, G., Messner, P., Schäffer, C., and Naismith, J. H. (2010) Structural basis of substrate binding in WsaF, a rhamnosyltransferase from Geobacillus stearothermophilus. J. Mol. Biol. 397, 436-447
47. Guerin, M. E., Kordulakova, J., Schaeffer, F., Svetlikova, Z., Buschiazzo, A., Giganti, D., Gicquel, B., Mikusova, K., Jackson, M., and Alzari, P. M. (2007) Molecular recognition and interfacial catalysis by the essential phosphatidylinositol mannosyltransferase PimA from mycobacteria. J. Biol. Chem. 282, 20705-20714 (Pubitemid 47100006)
48. Glover, K. J., Weerapana, E., and Imperiali, B. (2005) In vitro assembly of the undecaprenylpyrophosphate-linked heptasaccharide for prokaryotic N-linked glycosylation. Proc. Natl. Acad. Sci. U.S.A. 102, 14255-14259 (Pubitemid 41429685)
49. Troutman, J. M., and Imperiali, B. (2009) Campylobacter jejuni PglH is a single active site processive polymerase that utilizes product inhibition to limit sequential glycosyl transfer reactions. Biochemistry 48, 2807-2816
50. Kremer, L., Dover, L. G., Morehouse, C., Hitchin, P., Everett, M., Morris, H. R., Dell, A., Brennan, P. J., McNeil, M. R., Flaherty, C., Duncan, K., and Besra, G. S. (2001) Galactan biosynthesis in Mycobacterium tuberculosis. Identification of a bifunctional UDP-galactofuranosyltransferase. J. Biol. Chem. 276, 26430-26440
51. Belánová, M., Dianisková, P., Brennan, P. J., Completo, G. C., Rose, N. L., Lowary, T. L., and Mikusová, K. (2008) Galactosyltransferases in mycobacterial cell wall synthesis. J. Bacteriol. 190, 1141-1145
52. Brozek, K. A., Hosaka, K., Robertson, A. D., and Raetz, C. R. (1989) Biosynthesis of lipopolysaccharide in Escherichia coli. Cytoplasmic enzymes that attach 3-deoxy-D-manno-octulosonic acid to lipid A. J. Biol. Chem. 264, 6956-6966 (Pubitemid 19114810)
53. O'Reilly, M. K., Zhang, G., and Imperiali, B. (2006) In vitro evidence for the dual function of Alg2 and Alg11. Essential mannosyltransferases in N-linked glycoprotein biosynthesis. Biochemistry 45, 9593-9603 (Pubitemid 44223263)
54. Absmanner, B., Schmeiser, V., Kämpf, M., and Lehle, L. (2010) Biochemical characterization, membrane association, and identification of amino acids essential for the function of Alg11 from Saccharomyces cerevisiae, an α1,2-mannosyltransferase catalyzing two sequential glycosylation steps in the formation of the lipid-linked core oligosaccharide. Biochem. J. 426, 205-217
55. Gilbert, M., Brisson, J. R., Karwaski, M. F., Michniewicz, J., Cunningham, A. M., Wu, Y., Young, N. M., and Wakarchuk, W. W. (2000) Biosynthesis of ganglioside mimics in Campylobacter jejuni OH4384. Identification of the glycosyltransferase genes, enzymatic synthesis of model compounds, and characterization of nanomole amounts by 600-mHz 1H and 13C NMR analysis. J. Biol. Chem. 275, 3896-3906 (Pubitemid 30094614)
56. Blixt, O., Vasiliu, D., Allin, K., Jacobsen, N., Warnock, D., Razi, N., Paulson, J. C., Bernatchez, S., Gilbert, M., and Wakarchuk, W. (2005) Chemoenzymatic synthesis of 2-azidoethyl-ganglio-oligosaccharides GD3, GT3, GM2, GD2, GT2, GM1, and GD1a. Carbohydr. Res. 340, 1963-1972
57. Cuthbertson, L., Powers, J., and Whitfield, C. (2005) The C-terminal domain of the nucleotide-binding domain protein Wzt determines substrate specificity in the ATP-binding cassette transporter for the lipopolysaccharide O-antigens in Escherichia coli serotypes O8 and O9a. J. Biol. Chem. 280, 30310-30319 (Pubitemid 41216211)
58. Clarke, B. R., Greenfield, L. K., Bouwman, C., and Whitfield, C. (2009) Coordination of polymerization, chain termination, and export in assembly of the Escherichia coli lipopolysaccharide O9a antigen in an ATP-binding cassette transporter-dependent pathway. J. Biol. Chem. 284, 30662-30672
59. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C., and Gonzales, N. R. (2011) CDD. A conserved domain database for the functional annotation of proteins. Nucleic Acids Res. 39, D225-D229
60. Perepelov, A. V., Li, D., Liu, B., Senchenkova, S. N., Guo, D., Shevelev, S. D., Shashkov, A. S., Guo, X., Feng, L., Knirel, Y. A., and Wang, L. (2009) Structural and genetic characterization of Escherichia coli O99 antigen. FEMS Immunol. Med. Microbiol. 57, 80-87
61. Feng, L., Senchenkova, S. N., Yang, J., Shashkov, A. S., Tao, J., Guo, H., Cheng, J., Ren, Y., Knirel, Y. A., Reeves, P. R., and Wang, L. (2004) Synthesis of the heteropolysaccharide O-antigen of Escherichia coli O52 requires an ABC transporter. Structural and genetic evidence. J. Bacteriol. 186, 4510-4519 (Pubitemid 38891014)
62. Schäffer, C., Wugeditsch, T., Kählig, H., Scheberl, A., Zayni, S., and Messner, P. (2002) The surface layer (S-layer) glycoprotein of Geobacillus stearothermophilus NRS 2004/3a. Analysis of its glycosylation. J. Biol. Chem. 277, 6230-6239 (Pubitemid 34968414)
63. Steiner, K., Novotny, R., Werz, D. B., Zarschler, K., Seeberger, P. H., Hofinger, A., Kosma, P., Schäffer, C., and Messner, P. (2008) Molecular basis of S-layer glycoprotein glycan biosynthesis in Geobacillus stearothermophilus. J. Biol. Chem. 283, 21120-21133
64. Arsenault, T. L., Hughes, D. W., MacLean, D. B., Szarek, W. A., Kropinski, A. M. B., and Lam, J. S. (1991) Structural studies on the polysaccharide portion of "A-band" lipopolysaccharide from a mutant (AK1401) of Pseudomonas aeruginosa strain PAO1. Can. J. Chem. 69, 1273-1280
65. Rocchetta, H. L., Burrows, L. L., Pacan, J. C., and Lam, J. S. (1998) Three rhamnosyltransferases responsible for assembly of the A-band D-rhamnan polysaccharide in Pseudomonas aeruginosa. A fourth transferase, WbpL, is required for the initiation of both A-band and B-band lipopolysaccharide synthesis. Mol. Microbiol. 28, 1103-1119 (Pubitemid 28293536)
66. Ninomiya, T., Sugiura, N., Tawada, A., Sugimoto, K., Watanabe, H., and Kimata, K. (2002) Molecular cloning and characterization of chondroitin polymerase from Escherichia coli strain K4. J. Biol. Chem. 277, 21567-21575 (Pubitemid 34952303)
67. Sobhany, M., Kakuta, Y., Sugiura, N., Kimata, K., and Negishi, M. (2008) The chondroitin polymerase K4CP and the molecular mechanism of selective bindings of donor substrates to two active sites. J. Biol. Chem. 283, 32328-32333
68. Griffiths, G., Cook, N. J., Gottfridson, E., Lind, T., Lidholt, K., and Roberts, I. S. (1998) Characterization of the glycosyltransferase enzyme from the Escherichia coli K5 capsule gene cluster and identification and characterization of the glucuronyl active site. J. Biol. Chem. 273, 11752-11757 (Pubitemid 28272079)
69. Hodson, N., Griffiths, G., Cook, N., Pourhossein, M., Gottfridson, E., Lind, T., Lidholt, K., and Roberts, I. S. (2000) Identification that KfiA, a protein essential for the biosynthesis of the Escherichia coli K5 capsular polysaccharide, is an α-UDP-GlcNAc glycosyltransferase. The formation of a membrane-associated K5 biosynthetic complex requires KfiA, KfiB, and KfiC. J. Biol. Chem. 275, 27311-27315
70. Sugiura, N., Baba, Y., Kawaguchi, Y., Iwatani, T., Suzuki, K., Kusakabe, T., Yamagishi, K., Kimata, K., Kakuta, Y., and Watanabe, H. (2010) Glucuronyltransferase activity of KfiC from Escherichia coli strain K5 requires association of KfiA. KfiC and KfiA are essential enzymes for production of K5 polysaccharide, N-acetylheparosan. J. Biol. Chem. 285, 1597-1606