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

Molecular Microbiology

Volumn 57, Issue 5, 2005, Pages 1288-1303

  Wenzel, Cory Q ^a   Daniels, Craig ^a,b   Keates, Robert A B ^a   Brewer, Dyanne ^a   Lam, Joseph S ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; HEXAPEPTIDE; HISTIDINE; HISTIDINE TAGGED FUSION PROTEIN; HYBRID PROTEIN; O ANTIGEN; PROTEIN WBPD; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE; URIDINE DIPHOSPHATE 2 ACETAMIDO 3 AMINO 2,3 DIDEOXYGLUCURONIC ACID 3 ACETYLTRANSFERASE; URIDINE DIPHOSPHATE 2,3 DIACETAMIDO 2,3 DIDEOXYMANNURONIC ACID; URIDINE DIPHOSPHATE SUGAR;

ARTICLE; BORDETELLA; CATALYSIS; CHROMOSOME ANALYSIS; CIRCULAR DICHROISM; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ANALYSIS; GENE OVEREXPRESSION; GENE STRUCTURE; GENETIC COMPLEMENTATION; KNOCKOUT GENE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRECIPITATION; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN SYNTHESIS; PROTEIN TERTIARY STRUCTURE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS AERUGINOSA PAO1; SERODIAGNOSIS;

ACETYL COENZYME A; ACETYLTRANSFERASES; AMINO ACID SEQUENCE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; O ANTIGENS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; STRUCTURE-ACTIVITY RELATIONSHIP; URONIC ACIDS;

BORDETELLA; PSEUDOMONAS AERUGINOSA;

EID: 23844492151     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04767.x     Document Type: Article

References (49)

1. Allen, A., and Maskell, D. (1996) The identification, cloning and mutagenesis of a genetic locus required for lipopolysaccharide biosynthesis in Bordetella pertussis. Mol Microbiol 19: 37-52.
2. Beaman, T.W., Binder, D.A., Blanchard, J.S., and Roderick, S.L. (1997) Three-dimensional structure of tetrahydrodipicolinate N-succinyltransferase. Biochemistry 36: 489-494.
3. Beaman, T.W., Sugantino, M., and Roderick, S.L. (1998a) Structure of the hexapeptide xenobiotic acetyltransferase from Pseudomonas aeruginosa. Biochemistry 37: 6689-6696.
4. Beaman, T.W., Blanchard, J.S., and Roderick, S.L. (1998b) The conformational change and active site structure of tetrahydrodipicolinate N-succinyltransferase. Biochemistry 37: 10363-10369.
5. Burnette, W.N. (1981) 'Western blotting': electrophoretic transfer of proteins from sodium dodecyl sulfate-polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem 112: 195-203.
6. Burrows, LL, 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.
7. Denk, D., and Bock, A. (1987) 1-Cysteine biosynthesis in Escherichia coli: nucleotide sequence and expression of the serine acetyltransferase (cysE) gene from the wild-type and a cysteine-excreting mutant. J Gen Microbiol 133: 515-525.
8. Farinha, M.A., and Kropinski, A.M. (1990) High efficiency electroporation of Pseudomonas aeruginosa using frozen cell suspensions. FEMS Microbiol Lett 58: 221-225.
9. Fomsgaard, A., Freudenberg, M.A., and Galanos, C. (1990) Modification of the silver staining technique to detect lipopolysaccharide in polyacrylamide gels. J Clin Microbiol 28: 2627-2631.
10. Gehring, A.M., Lees, W.J., Mindiola, D.J., Walsh, C.T., and Brown, E.D. (1996) Acetyltransfer precedes uridylyltransfer in the formation of UDP-N-acetylglucosamine in separable active sites of the bifunctional GlmU protein of Escherichia coli. Biochemistry 35: 579-585.
11. Goldberg, J.B., and Ohman, D.E. (1984) Cloning and expression in Pseudomonas aeruginosa of a gene involved in the production of alginate. J Bacteriol 158: 1115-1121.
12. Greenfield, N.J. (1996) Methods to estimate the conformation of proteins and polypeptides from circular dichroism data. Anal Biochem 235: 1-10.
13. Hancock, R.E., and Carey, A.M. (1979) Outer memberane of Pseudomonas aeruginosa: heat-2-mercaptoethanol-modifiable proteins. J Bacteriol 140: 902-910.
14. Hitchcock, P.J., and Brown, T.M. (1983) Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154: 269-277.
15. Hoang, T.T., Karkhoff-Schweizer, R.R., Kutchma, A.J., and Schweizer, H.P. (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212: 77-86.
16. Jones, D.T. (1999) Protein secondary structure prediction based on position-specific scoring matrices. J Mol Biol 292: 195-202.
17. Kelley, L.A., MacCallum, R.M., and Sternberg, M.J. (2000) Enhanced genome annotation using structural profiles in the program 3D-PSSM. J Mol Biol 299: 499-520.
18. de Kievit, T.R., and Lam, J.S. (1997) Isolation and characterization of two genes, waaC (rfaC) and waaF (rfaF), involved in Pseudomonas aeruginosa serotype O5 inner-core biosynthesis. J Bacteriol 179: 3451-3457.
19. Knirel, Y.A., and Kochetkov, N.K. (1994) The structure of lipopolysaccharides of Gram-negative bacteria. III. The structure of O-antigens: a review. Biochemistry (Moscow) 59: 1325-1383.
20. Kostrewa, D., D'Arcy, A., Takacs, B., and Kamber, M. (2001) Crystal structures of Streptococcus pneumoniae N-acetylglucosamine-1-phosphate uridyltransferase, GlmU, in apo form at 2.33 A resolution and in complex with UDP-N-acetylglucosamine and Mg(2+) at 1.96 A resolution. J Mol Biol 305: 279-289.
21. Lam, J.S., Lam, M.Y., MacDonald, L.A., and Hancock, R.E. (1987) Visualization of Pseudomonas aeruginosa O antigens by using a protein A-dextran-colloidal gold conjugate with both immunoglobulin G and immunoglobulin M monoclonal antibodies. J Bacteriol 169: 3531-3538.
22. Lo Leggio, L., Dal Degan, F., Poulsen, P., Andersen, S.M., and Larsen, S. (2003) The structure and specificity of Escherichia coli maltose acetyltransferase give new insight into the LacA family of acyltransferases. Biochemistry 42: 5225-5235.
23. Ma, S., Selvaraj, U., Ohman, D.E., Quarless, R., Hassett, D.J., and Wozniak, D.J. (1998) Phosphorylation-independent activity of the response regulators AlgB and AlgR in promoting alginate biosynthesis in mucoid Pseudomonas aeruginosa. J Bacteriol 180: 956-968.
24. McGuffin, L.J., Bryson, K., and Jones, D.T. (2000) The PSIPRED protein structure prediction server. Bioinformatics 16: 404-405.
25. Marchler-Bauer, A., Anderson, J.B., DeWeese-Scott, C., Fedorova, N.D., Geer, L.Y., He, S., et al. (2003) CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res 31: 383-387.
26. Mengin-Lecreulx, D., and van Heijenoort, J. (1994) Copurification of glucosamine-1-phosphate acetyltransferase and N-acetylglucosamine-1-phosphate uridyltransferase activities of Escherichia coli: characterization of the glmU gene product as a bifunctional enzyme catalyzing two subsequent steps in the pathway for UDP-N-acetylglucosamine synthesis. J Bacteriol 176: 5788-5795.
27. 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.
28. Olsen, L.R., and Roderick, S.L. (2001) Structure of the Escherichia coli GlmU pyrophosphorylase and acetyltransferase active sites. Biochemistry 40: 1913-1921.
29. Pfoestl, A., Hofinger, A., Kosma, P., and Messner, P. (2003) Biosynthesis of dTDP-3-acetamido-3,6-dideoxy-alpha-D-galactose in Aneurinibacillus thermoaerophilus L420-91T. J Biol Chem 278: 26410-26417.
30. Pier, G.B. (2000) Role of the cystic fibrosis transmembrane conductance regulator in innate immunity to Pseudomonas aeruginosa infections. Proc Natl Acad Sci USA 97: 8822-8828.
31. Raetz, C.R.H. (1996). Bacterial lipopolysaccharides: a remarkable family of bioactive macroamphphiles. In Escherichia coli and Salmonella: Cellular and Molecular Biology. Neidhardt, F.C., Curtis, R.C.I., Ingram, J.L., et al. (eds). Washington, DC: ASM Press, pp. 1035-1063.
32. Raetz, C.R., and Roderick, S.L. (1995) A left-handed parallel beta helix in the structure of UDP-N-acetylglucosamine acyltransferase. Science 270: 997-1000.
33. Raymond, C.K., Sims, E.H., Kas, A., Spencer, D.H., Kutyavin, T.V., Ivey, R.G., et al. (2002) Genetic variation at the O-antigen biosynthetic locus in Pseudomonas aeruginosa. J Bacteriol 184: 3614-3622.
34. 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.
35. Schnaitman, C.A., and Klena, J.D. (1993) Genetics of lipopolysaccharide biosynthesis in enteric bacteria. Microbiol Rev 57: 655-682.
36. Schweizer, H.P., and Hoang, T.T. (1995) An improved system for gene replacement and xylE fusion analysis in Pseudomonas aeruginosa. Gene 158: 15-22.
37. Simms, S.A., Voige, W.H., and Gilvarg, C. (1984) Purification and characterization of succinyl-CoA: tetrahydrodipicolinate N-succinyltransferase from Escherichia coli. J Biol Chem 259: 2734-2741.
38. Simon, R., Priefer, U., and Puhler, A. (1983) A broad-host-range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Bio/ Technology 1: 784-791.
39. Sreerama, N., and Woody, R.W. (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism. Anal Biochem 209: 32-44.
40. Sreerama, N., and Woody, R.W. (1994a) Poly(pro)II helices in globular proteins: identification and circular dichroic analysis. Biochemistry 33: 10022-10025.
41. Sreerama, N., and Woody, R.W. (1994b) Protein secondary structure from circular dichroism spectroscopy. Combining variable selection principle and cluster analysis with neural network, ridge regression and self-consistent methods. J Mol Biol 242: 497-507.
42. Stover, C.K., Pham, X.Q., Erwin, A.L., Mizoguchi, S.D., Warrener, P., Hickey, M.J., et al. (2000) Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406: 959-964.
43. Sugantino, M., and Roderick, S.L. (2002) Crystal structure of Vat(D): an acetyltransferase that inactivates streptogramin group A antibiotics. Biochemistry 41: 2209-2216.
44. Sulzenbacher, G., Gal, L., Peneff, C., Fassy, F., and Bourne, Y. (2001) Crystal structure of Streptococcus pneumoniae N-acetylglucosamine-1-phosphate uridyltransferase bound to acetyl-coenzyme A reveals a novel active site architecture. J Biol Chem 276: 11844-11851.
45. Vaara, M. (1992) Eight bacterial proteins, including UDP-N- acetylglucosamine acyltransferase (LpxA) and three other transferases of Escherichia coli, consist of a six-residue periodicity theme. FEMS Microbiol Lett 76: 249-254.
46. Vuorio, R., Harkonen, 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.
47. Wang, W., and Malcolm, B.A. (1999) Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange Site-Directed Mutagenesis. Biotechniques 26: 680-682.
48. Wang, X.G., Olsen, L.R., and Roderick, S.L. (2002) Structure of the lac operon galactoside acetyltransferase. Structure (Camb) 10: 581-588.
49. West, S.E., Schweizer, H.P., Dall, C., Sample, A.K., and Runyen-Janecky, L.J. (1994) Construction of improved Escherichia-Pseudomonas shuttle vectors derived from pUC18/19 and sequence of the region required for their replication in Pseudomonas aeruginosa. Gene 11: 81-86.