Functional analysis of the large periplasmic loop of the Escherichia coli K-12 WaaL O-antigen ligase

Molecular Microbiology

Volumn 70, Issue 6, 2008, Pages 1424-1440

  Pérez, José M ^a   McGarry, Megan A ^a   Marolda, Cristina L ^a   Valvano, Miguel A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; HISTIDINE; LIGASE; LIPID A; LYSINE; MEMBRANE ANTIGEN; MEMBRANE ENZYME; MUTANT PROTEIN; O ANTIGEN; OLIGOSACCHARIDE; PYROPHOSPHATE; UNCLASSIFIED DRUG; UNDECAPRENYL DIPHOSPHATE; WAAL O ANTIGEN LIGASE;

ALPHA HELIX; AMINO ACID SEQUENCE; ANTIGEN EXPRESSION; ARTICLE; CATALYSIS; CELL FUNCTION; CONTROLLED STUDY; CYTOPLASM; ESCHERICHIA COLI K 12; GENE MUTATION; LIGATION; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

AMINO ACID SEQUENCE; ARGININE; CONSERVED SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GREEN FLUORESCENT PROTEINS; LIGASES; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PERIPLASM; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT;

ESCHERICHIA COLI K12;

EID: 56749158132     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2008.06490.x     Document Type: Article

References (59)

1. Abeyrathne, P. Lam, J. (2007) WaaL of Pseudomonas aeruginosa utilizes ATP in in vitro ligation of O antigen onto lipid A-core. Mol Microbiol 65 : 1345 1359.
2. Abeyrathne, P., Daniels, C., Poon, K.K., Matewish, M.J. Lam, J. (2005) Functional characterization of WaaL, a ligase associated with linking O-antigen polysaccharide to the core of Pseudomonas aeruginosa lipopolysaccharide. J Bacteriol 187 : 3002 3012.
3. Amer, A.O. Valvano, M.A. (2000) The N-terminal region of the Escherichia coli WecA (Rfe) protein containing three predicted transmembrane helices is required for function but not for membrane insertion. J Bacteriol 182 : 498 503.
4. Benoit, S., Abaibou, H. Mandrand-Berthelot, M.A. (1998) Topological analysis of the aerobic membrane-bound formate dehydrogenase of Escherichia coli. J Bacteriol 180 : 6625 6634.
5. Broadhurst, R.W., Nietlispach, D., Wheatcroft, M.P., Leadlay, P.F. Weissman, K.J. (2003) The structure of docking domains in modular polyketide synthases. Chem Biol 10 : 723 731.
6. Dai, K., Xu, Y. Lutkenhaus, J. (1996) Topological characterization of the essential Escherichia coli cell division protein FtsN. J Bacteriol 178 : 1328 1334.
7. Daley, D.O., Rapp, M., Granseth, E., Melen, K., Drew, D. von Heijne, G. (2005) Global topology analysis of the Escherichia coli inner membrane proteome. Science 308 : 1321 1323.
8. Datsenko, K.A. Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97 : 6640 6645.
9. Doerrler, W.T. Raetz, C.R.H. (2002) ATPase activity of the MsbA lipid flippase of Escherichia coli. J Biol Chem 277 : 36697 36705.
10. Doerrler, W.T., Reedy, M.C. Raetz, C.R.H. (2001) An Escherichia coli mutant defective in lipid export. J Biol Chem 276 : 11461 11464.
11. Drew, D., Sjöstrand, D., Nilsson, J., Urbig, T., Chin, C.-N., de Gier, J.-W. von Heijne, G. (2002) Rapid topology mapping of Escherichia coli inner-membrane proteins by prediction and PhoA/GFP fusion analysis. Proc Natl Acad Sci USA 99 : 2690 2695.
12. Feilmeier, B.J., Iseminger, G., Schroeder, D., Webber, H. Phillips, G.J. (2000) Green fluorescent protein functions as a reporter for protein localization in Escherichia coli. J Bacteriol 182 : 4068 4076.
13. Feldman, M.F., Marolda, C.L., Monteiro, M.A., Perry, M.B., Parodi, A.J. Valvano, M.A. (1999) The activity of a putative polyisoprenol-linked sugar translocase (Wzx) involved in Escherichia coli O antigen assembly is independent of the chemical structure of the O repeat. J Biol Chem 274 : 35129 35138.
14. Feldman, M.F., Wacker, M., Hernandez, M., Hitchen, P.G., Marolda, C.L., Kowarik, M., et al. (2005) Engineering N-linked protein glycosylation with diverse O antigen lipopolysaccharide structures in Escherichia coli. Proc Natl Acad Sci USA 102 : 3016 3021.
15. Graille, M., Meyer, P., Leulliot, N., Sorel, I., Janin, J., Van Tilbeurgh, H. Quevillon-Cheruel, S. (2005) Crystal structure of the S. cerevisiae d-ribose-5-phosphate isomerase: comparison with the archaeal and bacterial enzymes. Biochimie 87 : 763 769.
16. Haardt, M. Bremer, E. (1996) Use of phoA and lacZ fusions to study the membrane topology of ProW, a component of the osmoregulated ProU transport system of Escherichia coli. J Bacteriol 178 : 5370 5381.
17. Heinrichs, D.E., Monteiro, M.A., Perry, M.B. Whitfield, C. (1998a) The assembly system for the lipopolysaccharide R2 core-type of Escherichia coli is a hybrid of those found in Escherichia coli K-12 and Salmonella enterica. Structure and function of the R2 WaaK and WaaL homologs. J Biol Chem 273 : 8849 8859.
18. Heinrichs, D.E., Yethon, J.A., Amor, P.A. Whitfield, C. (1998b) The assembly system for the outer core portion of R1- and R4-type lipopolysaccharides of Escherichia coli. The R1 core-specific α-glucosyltransferase provides a novel attachment site for O-polysaccharides. J Biol Chem 273 : 29497 29505.
19. Heinrichs, D.E., Yethon, J.A. Whitfield, C. (1998c) Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol Microbiol 30 : 221 232.
20. Hung, L.H., Ngan, S.C., Liu, T. Samudrala, R. (2005) protinfo: new algorithms for enhanced protein structure predictions. Nucleic Acids Res 33 : W77 W80.
21. Hung, L., Ngan, S. Samudrala, R. (2007) De novo protein structure prediction. In Computational Methods for Protein Structure Prediction and Modeling. Xu, Y., Xu, D. Liang, J. (eds). New York : Springer, pp. 43 64.
22. Joiner, K.A. (1988) Complement evasion by bacteria and parasites. Annu Rev Microbiol 42 : 201 230.
23. Kamio, Y. Nikaido, H. (1976) Outer membrane of Salmonella typhimurium: accessibility of phospholipid head groups to phospholipase c and cyanogen bromide activated dextran in the external medium. Biochemistry 15 : 2561 2570.
24. Kaniuk, N.A., Vinogradov, E. Whitfield, C. (2004) Investigation of the structural requirements in the lipopolysaccharide core acceptor for ligation of O antigens in the genus Salmonella: WaaL 'ligase' is not the sole determinant of acceptor specificity. J Biol Chem 279 : 36470 36480.
25. Karplus, K., Karchin, R., Draper, J., Casper, J., Mandel-Gutfreund, Y., Diekhans, M. Hughey, R. (2003) Combining local-structure, fold-recognition, and new fold methods for protein structure prediction. Proteins 53 (Suppl. 6 491 496.
26. Kashino, Y. (2003) Separation methods in the analysis of protein membrane complexes. J Chromatogr B Anal Technol Biomed Life Sci 797 : 191 216.
27. Keenleyside, W.J. Whitfield, C. (1996) A novel pathway for O-polysaccharide biosynthesis in Salmonella enterica serovar Borreze. J Biol Chem 271 : 28581 28592.
28. L'vov, V.L., Shashkov, A.S., Dimitriev, B.A., Kochetkov, N.K., Jann, B. Jann, K. (1984) Structural studies of the O-specific side chain of the lipopolysaccharide from Escherichia coli O:7. Carbohydr Res 126 : 249 259.
29. Lee, D., Zheng, J., She, Y. Jia, Z. (2008) Structure of Escherichia coli tyrosine kinase Etk reveals a novel activation mechanism. EMBO J 27 : 1758 1766.
30. Lehrer, J., Vigeant, K.A., Tatar, L.D. Valvano, M.A. (2007) Functional characterization and membrane topology of Escherichia coli WecA, a sugar-phosphate transferase initiating the biosynthesis of enterobacterial common antigen and O antigen lipopolysaccharide. J Bacteriol 189 : 2618 2628.
31. Liu, D. Reeves, P.R. (1994) Escherichia coli K12 regains its O antigen. Microbiology 140 : 49 57.
32. McGrath, B.C. Osborn, M.J. (1991) Localization of the terminal steps of O-antigen synthesis in Salmonella typhimurium. J Bacteriol 173 : 649 654.
33. Marolda, C.L., Vicarioli, J. Valvano, M.A. (2004) Wzx proteins involved in O antigen biosynthesis function in association with the first sugar of the O-specific lipopolysaccharide subunit. Microbiology 150 : 4095 4105.
34. Marolda, C.L., Lahiry, P., Vinés, E., Saldías, S. Valvano, M.A. (2006) Micromethods for the characterization of lipid A-core and O-antigen lipopolysaccharide. Methods Mol Biol 347 : 237 252.
35. Mulford, C.A. Osborn, M.J. (1983) An intermediate step in translocation of lipopolysaccharide to the outer membrane of Salmonella typhimurium. Proc Natl Acad Sci USA 80 : 1159 1163.
36. Nesper, J., Kraiss, A., Schild, S., Blass, J., Klose, K.E., Bockemuhl, J. Reidl, J. (2002) Comparative and genetic analyses of the putative Vibrio cholerae lipopolysaccharide core oligosaccharide biosynthesis (wav) gene cluster. Infect Immun 70 : 2419 2433.
37. Neuhard, J. Thomassen, E. (1976) Altered deoxyribonucleic pools in P2 eductants of Escherichia coli K-12 due to deletion of the dcd gene. J Bacteriol 126 : 999 1001.
38. Nikaido, H. (2003) Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67 : 593 656.
39. Nilsson, J., Persson, B. von Heijne, G. (2000) Consensus predictions of membrane protein topology. FEBS Lett 486 : 267 269.
40. Parsons, L.M., Grishaev, A. Bax, A. (2008) The periplasmic domain of TolR from Haemophilus influenzae forms a dimer with a large hydrophobic groove: NMR solution structure and comparison to SAXS data. Biochemistry 47 : 3131 3142.
41. Pluschke, G. Achtman, M. (1984) Degree of antibody-independent activation of the classical complement pathway by K1 Escherichia coli differs with O antigen type and correlates with virulence of meningitis in newborns. Infect Immun 43 : 684 692.
42. Pugsley, A.P. (1993) The complete general secretory pathway in gram-negative bacteria. Microbiol Rev 57 : 50 108.
43. Qutyan, M., Paliotti, M. Castric, P. (2007) PilO of Pseudomonas aeruginosa 1244: subcellular location and domain assignment. Mol Microbiol 66 : 1444 1458.
44. Raetz, C.R.H. Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71 : 635 700.
45. Raetz, C.R., Reynolds, C.M., Trent, M.S. Bishop, R.E. (2007) Lipid A modification systems in gram-negative bacteria. Annu Rev Biochem 76 : 295 329.
46. Raza, H., Weinander, R., Ekstrom, L. Morgenstern, R. (1996) Membrane topology of recombinant rat liver microsomal glutathione transferase expressed in E. coli. Biochem Biophys Res Commun 228 : 165 170.
47. Saldías, M.S., Patel, K., Marolda, C.L., Bittner, M., Contreras, I. Valvano, M.A. (2008) Distinct functional domains of the Salmonella enterica WbaP transferase that is involved in the initiation reaction for synthesis of the O antigen subunit. Microbiology 154 : 440 453.
48. Samudrala, R. Levitt, M. (2002) A comprehensive analysis of 40 blind protein structure predictions. BMC Struct Biol 2 : 3.
49. Schild, S., Lamprecht, A.K. Reidl, J. (2005) Molecular and functional characterization of O antigen transfer in Vibrio cholerae. J Biol Chem 280 : 25936 25947.
50. Sonnhammer, E.L.L., von Heijne, G. Krogh, A. (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. In Proceedings of Sixth International Conference on Intelligent Systems for Molecular Biology. Glasgow, J., Littlejohn, T., Major, F., Lathrop, R., Sankoff, D. Sensen, C. (eds). Menlo Park, CA : AAAI Press, pp. 175 182.
51. Stevenson, G., Neal, B., Liu, D., Hobbs, M., Packer, N.H., Batley, M., et al. (1994) Structure of the O antigen of Escherichia coli K-12 and the sequence of its rfb cluster. J Bacteriol 176 : 4144 4156.
52. Tocilj, A., Munger, C., Proteau, A., Morona, R., Purins, L., Ajamian, E., et al. (2008) Bacterial polysaccharide co-polymerases share a common framework for control of polymer length. Nat Struct Mol Biol 15 : 130 138.
53. Valdivia, R.H., Hromockyj, A.E., Monack, D., Ramakrishnan, L. Falkow, S. (1996) Applications for green fluorescent protein (GFP) in the study of host-pathogen interactions. Gene 173 : 47 52.
54. Valvano, M.A. (2003) Export of O-specific lipopolysaccharide. Front Biosci 8 : s452 s471.
55. Valvano, M.A. Crosa, J.H. (1989) Molecular cloning and expression in Escherichia coli K-12 of chromosomal genes determining the O7 lipopolysaccharide antigen of a human invasive strain of E. coli O7:K1. Infect Immun 57 : 937 943.
56. Vinés, E., Marolda, C.L., Balachandran, A. Valvano, M.A. (2005) Defective O antigen polymerization in tolA and pal mutants of Escherichia coli in response to extracytoplasmic stress. J Bacteriol 187 : 3359 3368.
57. Walker, J.E., Saraste, M., Runswick, M.J. Gay, N.J. (1982) Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1 : 945 951.
58. Yamaguchi, H., Kato, H., Hata, Y., Nishioka, T., Kimura, A., Oda, J. Katsube, Y. (1993) Three-dimensional structure of the glutathione synthetase from Escherichia coli B at 2.0 A resolution. J Mol Biol 229 : 1083 1100.
59. Zhang, R.C.E., Andersson, A., Savchenko, T., Skarina, E., Evdokimova, S., et al. (2003) Structure of Escherichia coli ribose-5-phosphate isomerase: a ubiquitous enzyme of the pentose phosphate pathway and the Calvin cycle. Structure 11 : 31 42.