Structure of WbdD: A bifunctional kinase and methyltransferase that regulates the chain length of the O antigen in Escherichia coli O9a

Molecular Microbiology

Volumn 86, Issue 3, 2012, Pages 730-742

  Hagelueken, Gregor ^a   Huang, Hexian ^a   Clarke, Bradley R ^b   Lebl, Tomas ^a   Whitfield, Chris ^b   Naismith, James H ^a  

^a UNIVERSITY OF ST ANDREWS   (United Kingdom)

^b UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ENZYME; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; O ANTIGEN; UNCLASSIFIED DRUG; WBDD PROTEIN;

ARTICLE; BACTERIAL STRAIN; BINDING SITE; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; METHYLTRANSFERASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; O ANTIGENS; POLYSACCHARIDES, BACTERIAL; PROTEIN KINASES; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA;

EID: 84868098716     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12014     Document Type: Article

References (45)

1. Adams, P., Grosse-Kunstleve, R., Hung, L., Ioerger, T., McCoy, A., Moriarty, N., etal. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr D Biol Crystallogr 58: 1948-1954.
2. Cakici, O., Sikorski, M., Stepkowski, T., Bujacz, G., and Jaskolski, M. (2010) Crystal structures of NodS N-methyltransferase from Bradyrhizobium japonicum in ligand-free form and as SAH complex. J Mol Biol 404: 874-889.
3. Canagarajah, B., Khokhlatchev, A., Cobb, M., and Goldsmith, E. (1997) Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90: 859-869.
4. Chen, V.B., Arendall, W.B., Headd, J.J., Keedy, D.A., Immormino, R.M., Kapral, G.J., etal. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21.
5. 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.
6. 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.
7. 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.
8. 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.
9. Cuthbertson, L., Kimber, M.S., and Whitfield, C. (2007) Substrate binding by a bacterial ABC transporter involved in polysaccharide export. Proc Natl Acad Sci USA 104: 19529-19534.
10. Cuthbertson, L., Kos, V., and Whitfield, C. (2010) ABC transporters involved in export of cell surface glycoconjugates. Microbiol Mol Biol Rev 74: 341-362.
11. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60: 2126-2132.
12. Endicott, J.A., Noble, M.E.M., and Johnson, L.N. (2012) The structural basis for control of eukaryotic protein kinases. Annu Rev Biochem 81: 587-613.
13. Greenfield, L.K., Richards, M.R., Li, J., Wakarchuk, W.W., Lowary, T.L., and Whitfield, C. (2012) Biosynthesis of the polymannose lipopolysaccharide O antigens from Escherichia coli serotypes O8 and O9a requires a unique combination of single- and multi-active site mannosyltransferases. J Biol Chem doi:10.1074/jbc.M112.401000.
14. Hagelueken, G., Huang, H., Clarke, B., Harlos, K., Whitfield, C., and Naismith, J.H. (2012) Crystallization, dehydration and experimental phasing of WbdD, a bi-functional kinase and methyltransferase from Escherichia coli O9a. Acta Crystallogr D Biol Crystallogr [WWW document]. URL http://journals.iucr.org/d/services/forthcoming.html.
15. Hitchcock, P.J., and Brown, T.M. (1983) Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154: 269-277.
16. Holm, L., and Rosenström, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res 38: W545-W549.
17. Hon, W.C., McKay, G.A., Thompson, P.R., Sweet, R.M., Yang, D.S., Wright, G.D., and Berghuis, A.M. (1997) Structure of an enzyme required for aminoglycoside antibiotic resistance reveals homology to eukaryotic protein kinases. Cell 89: 887-895.
18. Jacobs, M., Hayakawa, K., Swenson, L., Bellon, S., Fleming, M., Taslimi, P., and Doran, J. (2006) The structure of dimeric ROCK I reveals the mechanism for ligand selectivity. J Biol Chem 281: 260-268.
19. Joiner, K.A. (1988) Complement evasion by bacteria and parasites. Annu Rev Microbiol 42: 201-230.
20. Kannan, N., Taylor, S.S., Zhai, Y., Venter, J.C., and Manning, G. (2007) Structural and functional diversity of the microbial kinome. PLoS Biol 5: e17.
21. 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.
22. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
23. Liu, H., and Naismith, J.H. (2008) An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol. BMC Biotechnol 8: 91.
24. McCoy, A.J., Grosse-Kunstleve, R.W., Adams, P.D., Winn, M.D., Storoni, L.C., and Read, R.J. (2007) Phasercrystallographic software. J Appl Crystallogr 40: 658-674.
25. Murshudov, G.N., Vagin, A.A., and Dodson, E.J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53: 240-255.
26. Newman, J., Egan, D., Walter, T.S., Meged, R., Berry, I., Ben Jelloul, M., etal. (2005) Towards rationalization of crystallization screening for small- to medium-sized academic laboratories: the PACT/JCSG+ strategy. Acta Crystallogr D Biol Crystallogr 61: 1426-1431.
27. Oke, M., Carter, L.G., Johnson, K.A., Liu, H., McMahon, S.A., Yan, X., etal. (2010) The Scottish structural proteomics facility: targets, methods and outputs. J Struct Funct Genomics 11: 167-180.
28. Raetz, C.R.H., and Whitfield, C. (2002) Lipopolysaccharide endotoxins. Annu Rev Biochem 71: 635-700.
29. Riento, K., and Ridley, A.J. (2003) Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol 4: 446-456.
30. Schubert, H., Blumenthal, R., and Cheng, X. (2003) Many paths to methyltransfer: a chronicle of convergence. Trends Biochem Sci 28: 329-335.
31. Sebastian, J., and Asensio, C. (1972) Purification and properties of the mannokinase from Escherichia coli. Arch Biochem Biophys 151: 227-233.
32. Singh, S., McCoy, J.G., Zhang, C., Bingman, C.A., Phillips, G.N., and Thorson, J.S. (2008) Structure and mechanism of the rebeccamycin sugar 4'-O-methyltransferase RebM. J Biol Chem 283: 22628-22636.
33. Stenutz, R., Weintraub, A., and Widmalm, G. (2006) The structures of Escherichia coli O-polysaccharide antigens. FEMS Microbiol Rev 30: 382-403.
34. Sugiyama, T., Kido, N., Komatsu, T., Ohta, M., Jann, K., Jann, B., etal. (1994) Genetic analysis of Escherichia coli 09 rfb: identification and DNA sequence of phosphomannomutase and GDP-mannose pyrophosphorylase genes. Microbiology 140: 59-71.
35. Tsai, C.M., and Frasch, C.E. (1982) A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal Biochem 119: 115-119.
36. Tu, D., Li, Y., Song, H.K., Toms, A.V., Gould, C.J., Ficarro, S.B., etal. (2011) Crystal structure of a coiled-coil domain from human ROCK I. PLoS ONE 6: e18080.
37. 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.
38. White, K.A., Lin, S., Cotter, R.J., and Raetz, C.R. (1999) A Haemophilus influenzae gene that encodes a membrane bound 3-deoxy-D-manno-octulosonic acid (Kdo) kinase. Possible involvement of kdo phosphorylation in bacterial virulence. J Biol Chem 274: 31391-31400.
39. Winter, G. (2010) xia2: an expert system for macromolecular crystallography data reduction. J Appl Crystallogr 43: 186-190.
40. Xu, W., Harrison, S.C., and Eck, M.J. (1997) Three-dimensional structure of the tyrosine kinase c-Src. Nature 385: 595-602.
41. Yamaguchi, H., and Hendrickson, W.A. (1996) Structural basis for activation of human lymphocyte kinase Lck upon tyrosine phosphorylation. Nature 384: 484-489.
42. Young, T.A., Delagoutte, B., Endrizzi, J.A., Falick, A.M., and Alber, T. (2003) Structure of Mycobacterium tuberculosis PknB supports a universal activation mechanism for Ser/Thr protein kinases. Nat Struct Biol 10: 168-174.
43. Zheng, J., Knighton, D., Eyck Ten, L., Karlsson, R., Xuong, N., Taylor, S.S., and Sowadski, J.M. (1993a) Crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with magnesium-ATP and peptide inhibitor. Biochemistry 32: 2154-2161.
44. Zheng, J., Trafny, E.A., Knighton, D.R., Xuong, N.H., Taylor, S.S., Eyck Ten, L.F., and Sowadski, J.M. (1993b) 2.2 A refined crystal structure of the catalytic subunit of cAMP-dependent protein kinase complexed with MnATP and a peptide inhibitor. Acta Crystallogr D Biol Crystallogr 49: 362-365.
45. Zheng, J., He, C., Singh, V.K., Martin, N.L., and Jia, Z. (2007) Crystal structure of a novel prokaryotic Ser/Thr kinase and its implication in the Cpx stress response pathway. Mol Microbiol 63: 1360-1371.