Biosynthesis of UDP-GlcNAc(3NAc)A by WbpB, WbpE, and WbpD: Enzymes in the Wbp pathway responsible for O-antigen assembly in Pseudomonas aeruginosa PAO1

Biochemistry

Volumn 48, Issue 23, 2009, Pages 5446-5455

  Larkin, Angelyn ^a   Imperiali, Barbara ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID DERIVATIVE; BIOCHEMICAL CHARACTERIZATION; COUPLED REACTION; ENCODED PROTEINS; GLYCOSYL DONORS; HOST DEFENSE; IN-VITRO; LIPOPOLYSACCHARIDE; MANNURONIC ACIDS; NMR SPECTROSCOPY; O-ANTIGEN; OVER-EXPRESSION; P.AERUGINOSA; PSEUDOMONAS AERUGINOSA; RECYCLING PATHWAYS; REPEATING UNIT; RP-HPLC; SEROTYPE; SINGLE REACTION VESSEL;

ACIDS; ANTIGENS; BIOCHEMICAL ENGINEERING; BIOCHEMISTRY; BIOSYNTHESIS; CAPILLARY ELECTROPHORESIS; CATALYSTS; CLONING; ENZYMES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYSACCHARIDES; SUGAR (SUCROSE); SUGARS;

INTERNET PROTOCOLS;

AMINOTRANSFERASE; BACTERIAL ENZYME; GLUCOSAMINE DERIVATIVE; GLUCURONIC ACID; LIPOPOLYSACCHARIDE; MANNURONIC ACID; NICOTINAMIDE ADENINE DINUCLEOTIDE; O ANTIGEN; OXIDOREDUCTASE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE 2 ACETAMIDO 2 DEOXY 3 OXO 3 GLUCURONIC ACID; URIDINE DIPHOSPHATE 2,3 DIACETAMIDO 2,3 DIDEOXY DEXTRO GLUCURONIC ACID; URIDINE DIPHOSPHATE 2,3 DIACETAMIDO 2,3 DIDEOXY DEXTRO MANNURONIC ACID; URIDINE DIPHOSPHATE GLUCURONIC ACID; URIDINE DIPHOSPHATE N ACETYL DEXTRO GLUCOSAMINURONIC ACID; WBPA ENZYME; WBPB ENZYME; WBPD ENZYME; WBPE ENZYME; WBPI ENZYME;

ACETYLATION; ARTICLE; BACTERIAL STRAIN; BIOSYNTHESIS; CAPILLARY ELECTROPHORESIS; CHEMICAL STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME SYNTHESIS; IN VITRO STUDY; MOLECULAR CLONING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; ONE POT SYNTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; VIRULENCE;

BACTERIAL PROTEINS; CARBOHYDRATE SEQUENCE; ELECTROPHORESIS, CAPILLARY; LIPOPOLYSACCHARIDES; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; O ANTIGENS; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; URIDINE DIPHOSPHATE SUGARS; URONIC ACIDS;

PSEUDOMONAS AERUGINOSA;

EID: 67049154264     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi900186u     Document Type: Article

References (49)

1. Pier, G. B. (2007) Pseudomonas aeruginosa lipopolysaccharide: A major virulence factor, initiator of inflammation and target for effective immunity. Int. J. Med. Microbiol. 297, 277-295.
2. Neu, H. C. (1985) Infections due to gram-negative bacteria: An overview. Rev. Infect. Dis. 7, S778-S782.
3. Diaz, M. H., Shaver, C. M., King, J. D., Musunuri, S., Kazzaz, J. A., and Hauser, A. R. (2008) Pseudomonas aeruginosa induces localized immunosuppression during pneumonia. Infect. Immun. 76, 4414-4421.
4. Tang, H. B., DiMango, E., Bryan, R., Gambello, M., Iglewski, B. H., Goldberg, J. B., and Prince, A. (1996) Contribution of specific Pseudomonas aeruginosa virulence factors to pathogenesis of pneumonia in a neonatal mouse model of infection. Infect. Immun. 64, 37-43.
5. Son, M. S., Matthews, W. J. Jr., Kang, Y., Nguyen, D. T., and Hoang, T. T. (2007) In vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infect. Immun. 75, 5313-5324.
6. Hancock, R. E. (1998) Resistance mechanisms in Pseudomonas aeruginosa and other nonfermative gram-negative bacteria. Clin. Infect. Dis. 27, S93-S99.
7. Mesaros, N., Nordmann, P., Plesiat, P., Roussel-Delvallez, M., Van Eldere, J., Y., G., Van Laethem, Y., Jacobs, F., Lebecque, P., Malfroot, A., Tulkens, P. M., and Van Bambeke, F. (2007) Pseudomonas aeruginosa: resistance and therapeutic options at the turn of the new millennium. Clin. Microbiol. Infect. 13, 560-578.
8. Zaborina, O., Holbrook, C., Chen, Y., Long, J., Zaborin, A., Morozova, I., Fernandez, H., Wang, Y., Turner, J. R., and Alverdy, J. C. (2008) Structure-function aspects of PstS in multi-drug resistant Pseudomonas aeruginosa. PLoS Pathog. 4, e43. (Pubitemid 351340709)
9. Döring, G., and Pier, G. B. (2008) Vaccines and immunotherapy against Pseudomonas aeruginosa. Vaccine 26, 1011-1024.
10. Cryz, S. J. Jr., Pitt, T. L., Furer, E., and Germanier, R. (1984) Role of lipopolysaccharide in virulence of Pseudomonas aeruginosa. Infect. Immun. 44, 508-513.
11. Lam, M. Y., McGroarty, E. J., Kropinski, A. M., MacDonald, L. A., Pedersen, S. S., Hoiby, N., and Lam, J. S. (1989) Occurrence of a common lipopolysaccharide antigen in standard and clinical strains of Pseudomonas aeruginosa. J. Clin. Microbiol. 27, 962-967.
12. Rocchetta, H. L., Burrows, L. L., and Lam, J. S. (1999) Genetics of O-antigen biosynthesis in Pseudomonas aeruginosa. Microbiol. Mol. Biol. Rev. 63, 523-553.
13. Knirel, Y. A., Bystrova, O. V., Kocharova, N. A., Zahringer, U., and Pier, G. B. (2006) Conserved and variable structural features in the lipopolysaccharide of Pseudomonas aeruginosa. J. Endotoxin Res. 12, 324-336. (Pubitemid 47487888)
14. Knirel, Y. A., Vinogradov, E. V., Kocharova, N. A., Paramonov, N. K., Kochetkov, N. K., Dmitriev, B. A., Stanislavsky, E. S., and Lanyi, B. (1988) The structure of O-specific polysaccharides and serological classification of Pseudomonas aeruginosa. Acta Microbiol. Hung. 35, 3-24.
15. Bystrova, O. V., Knirel, Y. A., Lindner, B., Kocharova, N. A., Kondakova, A. N., Zahringer, U., and Pier, G. B. (2006) Structures of the core oligosaccharide and O-units in the R- and SR-type lipopolysaccharides of reference strains of Pseudomonas aeruginosa O-serogroups. FEMS Immunol. Med. Microbiol. 46, 85-99.
16. Arsenault, T. L., Hughes, D. W., MacLean, D. B., Szarek, W., Kropinkski, 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.
17. Dasgupta, T., deKievit, T. R., Masoud, H., Altman, E., Richards, J. C., Sadovskaya, I., Speert, D. P., and Lam, J. S. (1994) Characterization of lipopolysaccharide-deficient mutants of Pseudomonas aeruginosa derived from serotypes O3, O5, and O6. Infect. Immun. 62, 809-817.
18. Hancock, R. E., Mutharia, L. M., Chan, L., Darveau, R. P., Speert, D. P., and Pier, G. B. (1983) Pseudomonas aeruginosa isolates from patients with cystic fibrosis: a class of serum-sensitive, nontypable strains deficient in lipopolysaccharide O side chains. Infect. Immun. 42, 170-177.
19. Kochetkov, N. K., and Knirel, Y. A. (1994) Structure of lipopolysaccharides from gram-negative bacteria. III. Structure of O-specific polysaccharides. Biochemistry (Moscow) 59, 1325-1383.
20. Burrows, L. L., Charter, D. F., and Lam, J. S. (1996) Molecular characterization of the Pseudomonas aeruginosa serotype O5 (PAO1) B-band lipopolysaccharide gene cluster. Mol. Microbiol. 22, 481-495.
21. Wenzel, C. Q., Daniels, C., Keates, R. A. B., Brewer, D., and Lam, J. S. (2005) Evidence that WbpD is an N-acetyltransferase belonging to the hexapeptide acyltransferase superfamily and an important protein for O-antigen biosynthesis in Pseudomonas aeruginosa PAO1. Mol. Microbiol. 57, 1288-1303.
22. Miller, W. L., Wenzel, C. Q., Daniels, C., Larocque, S., Brisson, J.-R., and Lam, J. S. (2004) Biochemical characterization of WbpA, a UDP-N-acetyl-D-glucosamine 6-dehydrogenase involved in O-antigen biosynthesis in Pseudomonas aeruginosa PAO1. J. Biol. Chem. 279, 37551-37558.
23. Westman, E. L., McNally, D. J., Rejzek, M., Miller, W. L., Kannathasan, V. S., Preston, A., Maskell, D. J., Field, R. A., Brisson, J.-R., and Lam, J. S. (2007) Identification and biochemical characterization of two novel UDP-2,3-diacetamido-2,3-dideoxy-α-D-glucuronic acid 2-epimerases from respiratory pathogens. Biochem. J. 405, 123-130. (Pubitemid 46999932)
24. Westman, E. L., Preston, A., Field, R. A., and Lam, J. S. (2008) Biosynthesis of a rare di-N-acetylated sugar in the lipopolysaccharides of both Pseudomonas aeruginosa and Bordetella pertussis occurs via an identical scheme despite different gene clusters. J. Bacteriol. 190, 6060-6069.
25. Burrows, L. L., Pigeon, K. E., and Lam, J. S. (2000) Pseudomonas aeruginosa B-band lipopolysaccharide genes wbpA and wbpI and their Escherichia coli homologues wecC and wecB are not functionally interchangeable. FEMS Microbiol. Lett. 189, 135-141.
26. Rejzek, M., Mukhopadhyay, B., Wenzel, C. Q., Lam, J. S., and Field, R. A. (2007) Direct oxidation of sugar nucleotides to the corresponding uronic acids:TEMPO and platinum-based procedures. Carb. Res. 342, 460-466.
27. Stahl, E. (1969) Thin-Layer Chromatography: A Laboratory Handbook, 2nd ed., Springer-Verlag, New York..
28. Lanning, M. C., and Cohen, S. S. (1951) The detection and estimation of 2-ketohexonic acids. J. Biol. Chem. 189, 109-114.
29. Kalliri, E., Mulrooney, S. B., and Hausinger, R. P. (2008) Identification of Escherichia coli YgaF as an L-2-hydroxyglutarate oxidase. J. Bacteriol. 190, 3793-3798. (Pubitemid 351732857)
30. + is the physiological cofactor of ADP-L-glycero-D-mannoheptose 6-epimerase. J. Biol. Chem. 276, 27329-27334.
31. + in urocanase: Separation and characterization of fully active and inhibited forms of the enzyme. Eur. J. Biochem. 185, 615-619.
32. Obhi, R. K., and Creuzenet, C. (2005) Biochemical characterization of the Campylobacter jejuni Cj1294, a novel UDP-4-keto-6-deoxy-GlcNAc aminotransferase that generates UDP-4-amino-4,6-dideoxy-GalNAc. J. Biol. Chem. 280, 20902-20908.
33. Vijayakumar, S., Merkx-Jacques, A., Ratnayake, D. B., Gryski, I., Obhi, R. K., Houle, S., Dozois, C. M., and Creuzenet, C. (2006) Cj1121c, a novel UDP-4-keto-6-deoxy-GlcNAc C-4 aminotransferase essential for protein glycosylation and virulence in Campylobacter jejuni. J. Biol. Chem. 281, 27733-27743.
34. Schoenhofen, I. C., McNally, D. J., Vinogradov, E., Whitfield, D., Young, N. M., Dick, S., Wakarchuk, W. W., Brisson, J.-R., and Logan, S. M. (2006) Functional characterization of dehydratase/aminotransferase pairs from Helicobacter and Campylobacter: Enzymes distinguishing the pseudaminic acid and bacillosamine biosynthetic pathways. J. Biol. Chem. 281, 723-732.
35. Knirel, Y. A., and Kochetkov, N. K. (1987) 2,3-Diamino-2,3-dideoxyuronic and 5,7-diamino-3,5,7,9-tetradeoxynonulosonic acids: new components of bacterial polysaccharides. FEMS Microbiol. Rev. 46, 381-385.
36. Okuda, S., Murata, S., and Suzuki, N. (1986) Isolation and identification of uridine(5′)-diphospho(1)-2,3-diacetamido-2,3-dideoxy-alpha-D- glucopyranuronic acid from Pseudomonas aeruginosa P1-III. Biochem. J. 239, 733-738.
37. Voisin, S., Houliston, R. S., Kelly, J., Brisson, J.-R., Watson, D., Bardy, S. L., Jarrell, K. F., and Logan, S. M. (2005) Identification and characterization of the unique N-linked glycan common to the flagellins and S-layer glycoprotein of Methanococcus voltae. J. Biol. Chem. 280, 16586-16593.
38. Kelly, J., Logan, S. M., Jarrell, K. F., VanDyke, D. J., and Vinogradov, E. V. (2009) A novel N-linked flagellar glycan from Methanococcus maripalidus. Carb. Res. 344, 648-653.
39. Shaffer, C., Kahlig, H., Christian, R., Schulz, G., Zanyi, S., and Messner, P. (1999) The diacetamidodideoxyuronic-acid-containing glycan chain of Bacillus stearothermophilus NRS 2004/3a represents the secondary cell-wall polymer of wild-type B. stearothermophilus strains. Microbiol. 145, 1575-1583. (Pubitemid 29352001)
40. Allen, A., and Maskell, D. (1996) The identification, cloning and mutagenesis of a genetic locus required for lipopolysaccharide biosynthesis in Bordatella pertussis. Mol. Microbiol. 19, 37-52.
41. Caroff, M., Brisson, J.-R., Martin, A., and Karibian, D. (2000) Structure of the Bordetella pertussis 1414 endotoxin. FEBS Lett. 477, 8-14. (Pubitemid 30438849)
42. Sweet, C. R., Ribeiro, A. A., and Raetz, C. R. H. (2004) Oxidation and transamination of the 3″-position of UDP-N-acetylglucosamine by enzymes from Acidithiobacillus ferrooxidans: Role in the formation of lipid A molecules with four amide-linked acyl chains. J. Biol. Chem. 279, 25400-25410.
43. Zhao, G., and Winkler, M. E. (1996) A novel α-ketoglutarate reductase activity of the serA-encoded 3-phosphoglycerate dehydrogenase of Escherichia coli K-12 and its possible implications for human 2-hydroxyglutaric adicuria. J. Bacteriol. 178, 232-239. (Pubitemid 3021261)
44. Westman, E. L., McNally, D. J., Charchoglyan, A., Brewer, D., Field, R. A., and Lam, J. S. (2009) Characterization of WbpB, WbpE, and WbpD, and reconstitution of a pathway for the biosynthesis of UDP-2,3-diacetamido-2,3- dideoxy-D-mannuronic acid in Pseudomonas aeruginosa, J. Biol. Chem. [Online early access].
45. Raetz, C. R. H., and Roderick, S. L. (1995) A left-handed parallel β-helix in the structure of UDP-N-acetylglucosamine acyltransferase. Science 270, 997-1000.
46. Vuorio, R., Härkönen, T., Tolvanen, M., and Vaara, M. (1994) The novel hexapeptide motif found in the acyltransferases LpxA and LpxD of lipid A biosynthesis is conserved in various bacteria. FEBS Lett. 337, 289-292. (Pubitemid 24034789)
47. Olsen, L. R., Vetting, M. W., and Roderick, S. L. (2007) Structure of the E. coli bifunctional GlmU acetyltransferase active site with substrates and products. Protein Sci. 16, 1230-1235. (Pubitemid 46849231)
48. Olivier, N. B., and Imperiali, B. (2008) Crystal structure and catalytic mechanism of PglD from Campylobacter jejuni. J. Biol. Chem. 283, 27937-27946.
49. Olivier, N. B., Chen, M. M., Behr, J. R., and Imperiali, B. (2006) In vitro biosynthesis of UDP-N,N′-diacetylbacillosamine by enzymes of the Campylobacter jejuni general protein glycosylation system. Biochemistry 45, 13659-13669.