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

Volumn 48, Issue 32, 2009, Pages 7764-7775

  Butty, Frank D ^a   Aucoin, Monique ^a   Morrison, Leslie ^a   Ho, Nathan ^a   Shaw, Gary ^a   Creuzenet, Carole ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PATHOGENS; BARRIER FUNCTIONS; BIOCHEMICAL CHARACTERIZATION; BIOSYNTHESIS PATHWAYS; DEHYDRATION REACTIONS; HIGH EFFICIENCY; IN-VITRO; IN-VIVO; KINETIC ANALYSIS; NAD(P)H; NMR ANALYSIS; O-ANTIGEN; REACTION PRODUCTS; SUBSTRATE SPECIFICITY; YERSINIA PSEUDOTUBERCULOSIS;

ANTIGENS; BACTERIOLOGY; BIOCHEMISTRY; BIOPOLYMERS; CARBOHYDRATES; DEHYDRATION; MASS SPECTROMETRY; POLYSACCHARIDES; PURIFICATION; SYNTHESIS (CHEMICAL);

SUBSTRATES;

CARBOHYDRATE DERIVATIVE; GUANOSINE DIPHOSPHATE DEXTRO GLYCERO DEXTRO MANNO HEPTOSE; GUANOSINE DIPHOSPHATE MANNOSE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); UNCLASSIFIED DRUG;

ARTICLE; BACILLUS; CHEMICAL REACTION; CONTROLLED STUDY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME SYNTHESIS; MASS SPECTROMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REDUCTION;

BACTERIAL PROTEINS; HEPTOSES; HYDRO-LYASES; MOLECULAR STRUCTURE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDOREDUCTASES; YERSINIA PSEUDOTUBERCULOSIS;

ANEURINIBACILLUS THERMOAEROPHILUS; BACTERIA (MICROORGANISMS); YERSINIA PSEUDOTUBERCULOSIS;

EID: 68849129696     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901065t     Document Type: Article

References (48)

1. 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.
2. Skurnik, M., and Zhang, L. (1996) Molecular genetics and biochemistry of Yersinia lipopolysaccharide. APMIS 104, 849-872.
3. 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.
4. 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.
5. Knirel, Y. A., Paramonov, N. A., Shashkov, A. S., Kochetkov, N. K., Yarullin, R. G., Farber, S. M., and Efremenko, V. I. (1992) Structure of the polysaccharide chains of Pseudomonas pseudomallei lipopolysaccharides. Carbohydr. Res. 233, 185-193.
6. Perry, M. B., MacLean, L. L., Schollaardt, T., Bryan, L. E., and Ho, M. (1995) Structural characterization of the lipopolysaccharide O antigens of Burkholderia pseudomallei. Infect. Immun. 63, 3348-3352.
7. DeShazer, D., Waag, D. M., Fritz, D. L., and Woods, D. E. (2001) Identification of a Burkholderia mallei polysaccharide gene cluster by subtractive hybridization and demonstration that the encoded capsule is an essential virulence determinant. Microb. Pathog. 30, 253-269.
8. 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.
9. 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.
10. Pacinelli, E., Wang, L., and Reeves, P. R. (2002) Relationship of Yersinia pseudotuberculosis O antigens IA, IIA, and IVB: the IIA gene cluster was derived from that of IVB. Infect. Immun. 70, 3271-3276.
11. 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.
12. Graziani, A., Zamyatina, A., and Kosma, P. (2004) A convenient synthesis of GDP D-glycero-alpha-D-manno-heptopyranose. Carbohydr. Res. 339, 147-1451.
13. Kneidinger, B., Graninger, M., Puchberger, M., Kosma, P., and Messner, P. (2001) Biosynthesis of nucleotide-activated D-glycero- D-manno-heptose. J. Biol. Chem. 276, 20935-20944.
14. Kneidinger, B., Marolda, C., Graninger, M., Zamyatina, A., McArthur, F., Kosma, P., Valvano, M. A., and Messner, P. (2002) Biosynthesis pathway of ADP-L-glycero-beta-D-manno-heptose in Escherichia coli. J. Bacteriol. 184, 363-369.
15. 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 (Part 1), 63-69.
16. Moore, J. T., Uppal, A., Maley, F., and Maley, G. F. (1993) Overcoming inclusion body formation in a high-level expression system. Protein Expression Purif. 4, 160-163.
17. 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.
18. Bax, A., and Davis, D. G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65, 355-360.
19. Piantini, U., Sorensen, O. W., and Ernst, R. R. (1982) Multiple quantum filters for elicidating NMR coupling networks. J. Am. Chem. Soc. 104, 6800-6801.
20. 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.
21. John, B. K., Plant, D., and Hurd, R. E. (1992) Improved protondetected heteronuclear correlation using gradient-enhanced z and zz filters. J. Magn. Reson. A101, 113-117.
22. Ishiyama, N., Creuzenet, C., Miller, W. L., Demendi, M., Anderson, E. M., Harauz, G., Lam, J. S., and Berghuis, A. M. (2006) Structural studies of FlaA1 from Helicobacter pylori reveal the mechanism for inverting 4,6-dehydratase activity. J. Biol. Chem. 281, 24489-24495.
23. 4 reductase from Helicobacter pylori. J. Biol. Chem. 275, 34873-34880.
24. 6 dehydratase from Campylobacter jejuni. FEBS Lett. 559, 136-140.
25. Wu, B., Zhang, Y., and Wang, P. G. (2001) Identification and characterization of GDP-d-mannose 4,6-dehydratase and GDP-lfucose snthetase in a GDP-l-fucose biosynthetic gene cluster from Helicobacter pylori. Biochem. Biophys. Res. Commun. 285, 364-371.
26. Ramm, M., Wolfender, J. L., Queiroz, E. F., Hostettmann, K., and Hamburger, M. (2004) Rapid analysis of nucleotide-activated sugars by high-performance liquid chromatography coupled with diodearray detection, electrospray ionization mass spectrometry and nuclear magnetic resonance. J. Chromatogr. A 1034, 139-148.
27. McNally, D. J., Schoenhofen, I. C., Mulrooney, E. F., Whitfield, D. M., Vinogradov, E., Lam, J. S., Logan, S. M., and Brisson, J. R. (2006) Identification of labile UDP-ketosugars in Helicobacter pylori, Campylobacter jejuni and Pseudomonas aeruginosa: key metabolites used to make glycan virulence factors. ChemBioChem 7, 1865-1868.
28. 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.
29. 6 dehydratase essential for lipopolysaccharide biosynthesis in Pseudomonas aeruginosa. Mol. Microbiol. 41, 1295-1310.
30. Schoenhofen, I. C., McNally, D. J., Brisson, J. R., and Logan, S. M. (2006) Elucidation of the CMP-pseudaminic acid pathway in Helicobacter pylori: synthesis from UDP-N-acetylglucosamine by a single enzymatic reaction. Glycobiology 16, 8C-14C.
31. Vijayakumar, S., Merkx-Jacques, A., Ratnayake, D., Gryski, I., Obhi, R. K., Houle, S., Dozois, C., and Creuzenet, C. (2006) Cj1121c, a novel UDP-4-keto-6-deoxy-GlcNAc C4 aminotransferase essential for protein glycosylation and virulence in Campylobacter jejuni. J. Biol. Chem. 281, 27733-27743.
32. Bisso, A., Sturla, L., Zanardi, D., De Flora, A., and Tonetti, M. (1999) Structural and enzymatic characterization of human recombinant GDP-D-mannose-4,6-dehydratase. FEBS Lett. 456, 370-374.
33. 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.
34. Wu, B., Zhang, Y., and Wang, P. G. (2001) Identification and characterization of GDP-D-mannose 4,6-dehydratase and GDP-lfucose synthetase in a GDP-l-fucose biosynthetic gene cluster from Helicobacter pylori. Biochem. Biophys. Res. Commun. 285, 364-371.
35. 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.
36. 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.
37. 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., Goodhead, I., Sanders, M., Stevens, K., White, B., Parkhill, J., Wren, B. W., and Szymanski, C. M. (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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. Parkhill, J., Wren, B. W., Mungall, K., Ketley, J. M., Churcher, C., Basham, D., Chillingworth, T., Davies, R. M., Feltwell, T., Holroyd, S., Jagels, K., Karlyshev, A. V., Moule, S., Pallen, M. J., Penn, C. W., Quail, M. A., Rajandream, M. A., Rutherford, K. M., van Vliet, A. H., Whitehead, S., and Barrell, B. G. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665-668.
44. Skurnik, M., Venho, R., Toivanen, P., and al-Hendy, A. (1995) A novel locus of Yersinia enterocolitica serotype O:3 involved in lipopolysaccharide outer core biosynthesis. Mol. Microbiol. 17, 575-594.
45. Straley, S. C., and Perry, R. D. (1995) Environmental modulation of gene expression and pathogenesis in Yersinia. Trends Microbiol. 3, 310-317.
46. 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.
47. Skurnik, M., Peippo, A., and Ervela, E. (2000) Characterization of the O-antigen gene clusters of Yersinia pseudotuberculosis and the cryptic O-antigen gene cluster of Yersinia pestis shows that the plague bacillus is most closely related to and has evolved from Y. pseudotuberculosis serotype O:1b. Mol. Microbiol. 37, 316-330.
48. Valvano, M. A., Messner, P., and Kosma, P. (2002) Novel pathways for biosynthesis of nucleotide-activated glycero-manno-heptose precursors of bacterial glycoproteins and cell surface polysaccharides. Microbiology 148, 1979-1989.