Characterization of the dehydratase WcbK and the reductase WcaG involved in GDP-6-deoxy-manno-heptose biosynthesis in Campylobacter jejuni

Biochemical Journal

Volumn 439, Issue 2, 2011, Pages 235-248

  Mccallum, Matthew ^a   Shaw, Gary S ^a   Creuzenet, Carole ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

C4 reductase; C6 dehydratase; Campylobacter jejuni; Capsule synthesis; GDP 6 deoxy altro heptose; Heptose modification

Indexed keywords

GUANOSINE DIPHOSPHATE 6 DEOXYMANNOHEPTOSE; HEPTOSE; HYDROLYASE; OXIDOREDUCTASE; PROTEIN WCAG; PROTEIN WCBK; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CAMPYLOBACTER JEJUNI; CATALYSIS; ENZYME ACTIVITY; ENZYME PURIFICATION; ENZYME SPECIFICITY; EPIMERIZATION; KINETICS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS;

BASE SEQUENCE; CAMPYLOBACTER JEJUNI; CLONING, MOLECULAR; DNA PRIMERS; GUANOSINE DIPHOSPHATE MANNOSE; HYDRO-LYASES; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDOREDUCTASES;

CAMPYLOBACTER JEJUNI; YERSINIA PSEUDOTUBERCULOSIS;

EID: 80053279494     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20110890     Document Type: Article

References (51)

1. Lecuit, M., Abachin, E., Martin, A., Poyart, C., Pochart, P., Suarez, F., Bengoufa, D., Feuillard, J., Lavergne, A., Gordon, J. I. et al. (2004) Immunoproliferative small intestinal disease associated with Campylobacter jejuni. N. Engl. J. Med. 350, 239-248 (Pubitemid 38067636)
2. Lecuit, M. and Lortholary, O. (2005) Immunoproliferative small intestinal disease associated with Campylobacter jejuni. Med. Mal. Infect. 35, S56-S58 (Pubitemid 40853741)
3. Al-Saleem, T. and Al-Mondhiry, H. (2005) Immunoproliferative small intestinal disease (IPSID): a model for mature B-cell neoplasms. Blood 105, 2274-2280 (Pubitemid 40387019)
4. Zhao, S., Young, S. R., Tong, E., Abbott, J. W., Womack, N., Friedman, S. L. and McDermott, P. F. (2010) Antimicrobial resistance of Campylobacter isolates from retail meat in the United States between 2002 and 2007. Appl. Environ. Microbiol. 76, 7949-7956
5. Sammarco, M. L., Ripabelli, G., Fanelli, I., Grasso, G. M. and Tamburro, M. (2010) Prevalence and biomolecular characterization of Campylobacter spp. isolated from retail meat. J. Food Prot. 73, 720-728
6. Arsenault, J., Michel, P., Berke, O., Ravel, A. and Gosselin, P. (2011) Environmental characteristics associated with campylobacteriosis: accounting for the effect of age and season. Epidemiol. Infect., doi:10.1017/S0950268811000628
7. Alfredson, D. A. and Korolik, V. (2007) Antibiotic resistance and resistance mechanisms in Campylobacter jejuni and Campylobacter coli. FEMS Microbiol. Lett. 277, 123-132 (Pubitemid 350145567)
8. Larkin, C., van Donkersgoed, C., Mahdi, A., Johnson, P., McNab, B. and Odumeru, J. (2006) Antibiotic resistance of Campylobacter jejuni and Campylobacter coli isolated from hog, beef, and chicken carcass samples from provincially inspected abattoirs in Ontario. J. Food Prot. 69, 22-26 (Pubitemid 43132515)
9. Cody, A. J., Clarke, L., Bowler, I. C. and Dingle, K. E. (2010) Ciprofloxacin-resistant campylobacteriosis in the UK. Lancet 376, 1987
10. Bachtiar, B. M., Coloe, P. J. and Fry, B. N. (2007) Knockout mutagenesis of the kpsE gene of Campylobacter jejuni 81116 and its involvement in bacterium-host interactions. FEMS Immunol. Med. Microbiol. 49, 149-154 (Pubitemid 46160597)
11. Bacon, D. J., Szymanski, C. M., Burr, D. H., Silver, R. P., Alm, R. A. and Guerry, P. (2001) A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol. Microbiol. 40, 769-777 (Pubitemid 32453128)
12. Jones, M. A., Marston, K. L., Woodall, C. A., Maskell, D. J., Linton, D., Karlyshev, A. V., Dorrell, N., Wren, B. W. and Barrow, P. A. (2004) Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect. Immun. 72, 3769-3776 (Pubitemid 38821888)
13. Aspinall, G. O., McDonald, A. G. and Pang, H. (1992) Structures of the O chains from lipopolysaccharides of Campylobacter jejuni serotypes O:23 and O:36. Carbohydr. Res. 231, 13-30
14. Chen, Y. H., Poly, F., Pakulski, Z., Guerry, P. and Monteiro, M. A. (2008) The chemical structure and genetic locus of Campylobacter jejuni CG8486 (serotype HS:4) capsular polysaccharide: the identification of 6-deoxy-D-ido-heptopyranose. Carbohydr. Res. 343, 1034-1040
15. St Michael, F., Szymanski, C. M., Li, J., Chan, K. H., Khieu, N. H., Larocque, S., Wakarchuk, W. W., Brisson, J. R. and Monteiro, M. A. (2002) The structures of the lipooligosaccharide and capsule polysaccharide of Campylobacter jejuni genome sequenced strain NCTC 11168. Eur. J. Biochem. 269, 5119-5136 (Pubitemid 35345126)
16. Aspinall, G. O., Lynch, C. M., Pang, H., Shaver, R. T. and Moran, A. P. (1995) Chemical structures of the core region of Campylobacter jejuni O:3 lipopolysaccharide and an associated polysaccharide. Eur. J. Biochem. 231, 570-578
17. Reckseidler, S. L., DeShazer, D., Sokol, P. A. and Woods, D. E. (2001) Detection of bacterial virulence genes by subtractive hybridization: identification of capsular polysaccharide of Burkholderia pseudomallei as a major virulence determinant. Infect. Immun. 69, 34-44 (Pubitemid 32038296)
18. Reckseidler-Zenteno, S. L., DeVinney, R. and Woods, D. E. (2005) The capsular polysaccharide of Burkholderia pseudomallei contributes to survival in serum by reducing complement factor C3b deposition. Infect. Immun. 73, 1106-1115 (Pubitemid 40165771)
19. Samuelsson, K., Lindberg, B. and Brubaker, R. R. (1974) Structure of O-specific side chains of lipopolysaccharides from Yersinia pseudotuberculosis. J. Bacteriol. 117, 1010-1016
20. Komandrova, N. A., Gorshkova, R. P., Isakov, V. V. and Ovodov, Iu S. (1984) Structure of O-specific polysaccharide isolated from the Yersinia pseudotuberculosis serotype 1A lipopolysaccharide. Bioorg. Khim. 10, 232-237
21. Skurnik, M. and Zhang, L. (1996) Molecular genetics and biochemistry of Yersinia lipopolysaccharide. APMIS 104, 849-872 (Pubitemid 27064732)
22. Ho, N., Kondakova, A. N., Knirel, Y. A. and Creuzenet, C. (2008) The biosynthesis and biological role of 6-deoxyheptose in the lipopolysaccharide O-antigen of Yersinia pseudotuberculosis. Mol. Microbiol. 68, 424-447 (Pubitemid 351422964)
23. Butty, F. D., Aucoin, M., Morrison, L., Ho, N., Shaw, G. and Creuzenet, C. (2009) Elucidating the formation of 6-deoxyheptose: biochemical characterization of the GDP-D-glycero-D-manno-heptose C6 dehydratase, DmhA and its associated C4 reductase DmhB. Biochemistry 48, 7764-7775
24. Kondakova, A. N., Ho, N., Bystrova, O. V., Shashkov, A. S., Lindner, B., Creuzenet, C. and Knirel, Y. A. (2008) Structural studies of the O-antigens of Yersinia pseudotuberculosis O:2a and mutants thereof with impaired 6-deoxy-D-manno-heptose biosynthesis pathway. Carbohydr. Res. 343, 1383-1389 (Pubitemid 351620947)
25. Karlyshev, A. V., Champion, O. L., Churcher, C., Brisson, J. R., Jarrell, H. C., Gilbert, M., Brochu, D., St Michael, F., Li, J., Wakarchuk, W. W. et al. (2005) Analysis of Campylobacter jejuni capsular loci reveals multiple mechanisms for the generation of structural diversity and the ability to form complex heptoses. Mol. Microbiol. 55, 90-103 (Pubitemid 40127887)
26. Newton, D. T. and Mangroo, D. (1999) Mapping the active site of the Haemophilus influenzae methionyl-tRNA formyltransferase: residues important for catalysis and tRNA binding. Biochem. J. 339, 63-69 (Pubitemid 29179291)
27. Demendi, M., Ishiyama, N., Lam, J. S., Berghuis, A. M. and Creuzenet, C. (2005) Towards a better understanding of the substrate specificity of the UDP-N-acetylglucosamine C4 epimerase WbpP. Biochem. J. 389, 173-180 (Pubitemid 40978020)
28. 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 (Pubitemid 40776796)
29. Bax, A. and Davis, D. G. (1985) MLEV-17-Based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65, 355-360
30. Kay, L. E., Keifer, P. and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity. J. Am. Chem. Soc. 114, 10663-10665
31. John, B. K., Plant, D. and Hurd, R. E. (1992) Improved proton-detected heteronuclear correlation using gradient-enhanced z and zz filters. J. Magn. Reson. A101, 113-117
32. Webb, N. A., Mulichak, A. M., Lam, J. S., Rocchetta, H. L. and Garavito, R. M. (2004) Crystal structure of a tetrameric GDP-D-mannose 4,6-dehydratase from a bacterial GDP-D-rhamnose biosynthetic pathway. Protein Sci. 13, 529-539 (Pubitemid 38124973)
33. Mulichak, A. M., Bonin, C. P., Reiter, W. D. and Garavito, R. M. (2002) Structure of the MUR1 GDP-mannose 4,6-dehydratase from Arabidopsis thaliana: implications for ligand binding and specificity. Biochemistry 41, 15578-15589 (Pubitemid 36062462)
34. Sobolev, V., Sorokine, A., Prilusky, J., Abola, E. E. and Edelman, M. (1999) Automated analysis of interatomic contacts in proteins. Bioinformatics 15, 327-332 (Pubitemid 29213759)
35. Willard, L., Ranjan, A., Zhang, H., Monzavi, H., Boyko, R. F., Sykes, B. D. and Wishart, D. S. (2003) VADAR: a web server for quantitative evaluation of protein structure quality. Nucleic Acids Res. 31, 3316-3319 (Pubitemid 37442148)
36. Somoza, J. R., Menon, S., Schmidt, H., Joseph-McCarthy, D., Dessen, A., Stahl, M. L., Somers, W. S. and Sullivan, F. X. (2000) Structural and kinetic analysis of Escherichia coli GDP-mannose 4,6 dehydratase provides insights into the enzyme's catalytic mechanism and regulation by GDP-fucose. Structure 8, 123-135 (Pubitemid 30097358)
37. Zhao, G., Liu, J., Liu, X., Chen, M., Zhang, H. and Wang, P. G. (2007) Cloning and characterization of GDP-perosamine synthetase (Per) from Escherichia coli O157:H7 and synthesis of GDP-perosamine in vitro. Biochem. Biophys. Res. Commun. 363, 525-530 (Pubitemid 47513662)
38. King, J. D., Poon, K. K., Webb, N. A., Anderson, E. M., McNally, D. J., Brisson, J. R., Messner, P., Garavito, R. M. and Lam, J. S. (2009) The structural basis for catalytic function of GMD and RMD, two closely related enzymes from the GDP-D-rhamnose biosynthesis pathway. FEBS J. 276, 2686-700
39. Maki, M., Jarvinen, N., Rabina, J., Roos, C., Maaheimo, H. and Renkonen, R. (2002) Functional expression of Pseudomonas aeruginosa GDP-4-keto-6-deoxy-D- mannose reductase which synthesizes GDP-rhamnose. Eur. J. Biochem. 269, 593-601 (Pubitemid 34128017)
40. Kneidinger, B., Graninger, M., Adam, G., Puchberger, M., Kosma, P., Zayni, S. and Messner, P. (2001) Identification of two GDP-6-deoxy-D-lyxo-4- hexulose reductases synthesizing GDP-D-rhamnose in Aneurinibacillus thermoaerophilus L420-91T. J. Biol. Chem. 276, 5577-5583
41. Aspinall, G. O., McDonald, A. G., Pang, H., Kurjanczyk, L. A. and Penner, J. L. (1993) An antigenic polysaccharide from Campylobacter coli serotype O:30. Structure of a teichoic acid-like antigenic polysaccharide associated with the lipopolysaccharide. J. Biol. Chem. 268, 18321-18329 (Pubitemid 23260360)
42. Aspinall, G. O., McDonald, A. G., Pang, H., Kurjanczyk, L. A. and Penner, J. L. (1993) Lipopolysaccharide of Campylobacter coli serotype O:30. Fractionation and structure of liberated core oligosaccharide. J. Biol. Chem. 268, 6263-6268 (Pubitemid 23099318)
43. Aspinall, G. O., Monteiro, M. A. and Pang, H. (1995) Lipo-oligosaccharide of the Campylobacter lari type strain ATCC 35221. Structure of the liberated oligosaccharide and an associated extracellular polysaccharide. Carbohydr. Res. 279, 245-264 (Pubitemid 26019377)
44. Hanniffy, O. M., Shashkov, A. S., Moran, A. P., Prendergast, M. M., Senchenkova, S. N., Knirel, Y. A. and Savage, A. V. (1999) Chemical structure of a polysaccharide from Campylobacter jejuni 176.83 (serotype O:41) containing only furanose sugars. Carbohydr. Res. 319, 124-132 (Pubitemid 29430269)
45. Parkhill, J., Wren, B. W., Mungall, K., Ketley, J. M., Churcher, C., Basham, D., Chillingworth, T., Davies, R. M., Feltwell, T., Holroyd, S. et al. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665-668 (Pubitemid 30104008)
46. 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
47. Sullivan, F. X., Kumar, R., Kriz, R., Stahl, M., Xu, G. Y., Rouse, J., Chang, X. J., Boodhoo, A., Potvin, B. and Cumming, D. A. (1998) Molecular cloning of human GDP-mannose 4,6-dehydratase and reconstitution of GDP-fucose biosynthesis in vitro. J. Biol. Chem. 273, 8193-8202 (Pubitemid 28168875)
48. Sturla, L., Bisso, A., Zanardi, D., Benatti, U., De Flora, A. and Tonetti, M. (1997) Expression, purification and characterization of GDP-D-mannose 4,6-dehydratase from Escherichia coli. FEBS Lett. 412, 126-130 (Pubitemid 27310014)
49. Wu, B., Zhang, Y. and Wang, P. G. (2001) Identification and characterization of GDP-D-mannose 4,6-dehydratase and GDP-L-fucose synthetase in a GDP-L-fucose biosynthetic gene cluster from Helicobacter pylori. Biochem. Biophys. Res. Commun. 285, 364-371 (Pubitemid 32918079)
50. Albermann, C. and Piepersberg, W. (2001) Expression and identification of the RfbE protein from Vibrio cholerae O1 and its use for the enzymatic synthesis of GDP-D-perosamine. Glycobiology 11, 655-661 (Pubitemid 32782683)
51. Szymanski, C. M., Yao, R., Ewing, C. P., Trust, T. J. and Guerry, P. (1999) Evidence for a system of general protein glycosylation in Campylobacter jejuni. Mol. Microbiol. 32, 1022-1030 (Pubitemid 29255768)