Complete 6-deoxy-D-altro-heptose biosynthesis pathway from Campylobacter jejuni: More complex than anticipated

Journal of Biological Chemistry

Volumn 287, Issue 35, 2012, Pages 29776-29788

  McCallum, Matthew ^a   Shaw, Steven D ^a   Shaw, Gary S ^a   Creuzenet, Carole ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBACTERIAL EFFECTS; BIOSYNTHESIS PATHWAYS; BIOSYNTHETIC PATHWAY; CAMPYLOBACTER JEJUNI; EPIMERIZATION; INFECTION MODELS; MOLECULAR TOOLS; POTENTIAL ACTIVITIES;

BACTERIA; BIOCHEMISTRY; CARBOHYDRATES; STRAIN;

BIOSYNTHESIS;

EPIMERASE; GUANOSINE DIPHOSPHATE; GUANOSINE DIPHOSPHATE 6 DEOXY DEXTRO ALTRO HEPATOSE; HEPTOSE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CAMPYLOBACTER JEJUNI; CARBOHYDRATE SYNTHESIS; ENZYME ACTIVITY; ENZYME MECHANISM; EPIMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION;

BACTERIAL PROTEINS; CAMPYLOBACTER JEJUNI; CARBOHYDRATE METABOLISM; HEPTOSES;

CAMPYLOBACTER JEJUNI;

EID: 84865463329     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.390492     Document Type: Article

References (53)

1. Dasti, J. I., Tareen, A. M., Lugert, R., Zautner, A. E., and Gross, U. (2010) Campylobacter jejuni. A brief overview on pathogenicity-associated factors and disease-mediating mechanisms. Int. J. Med. Microbiol. 300, 205-211
2. Kirkpatrick, B. D., and Tribble, D. R. (2011) Update on human Campylobacter jejuni infections. Curr. Opin. Gastroenterol. 27, 1-7
3. Poropatich, K. O., Walker, C. L., and Black, R. E. (2010) Quantifying the association between Campylobacter infection and Guillain-Barre syndrome. A systematic review. J. Health Popul. Nutr. 28, 545-552
4. Kalischuk, L. D., and Buret, A. G. (2010) A role for Campylobacter jejuni-induced enteritis in inflammatory bowel disease? Am. J. Physiol. Gastrointest. Liver Physiol. 298, G1-G9
5. Lindow, J. C., Poly, F., Tribble, D. R., Guerry, P., Carmolli, M. P., Baqar, S., Porter, C. K., Pierce, K. K., Darsley, M. J., Sadigh, K. S., Dill, E. A., Campylobacter Study Team, and Kirkpatrick, B. D. (2010) Caught in the act. In vivo development of macrolide resistance to Campylobacter jejuni infection. J. Clin. Microbiol. 48, 3012-3015
6. Kittl, S., Kuhnert, P., Hächler, H., and Korczak, B. M. (2011) Comparison of genotypes and antibiotic resistance of Campylobacter jejuni isolated from humans and slaughtered chickens in Switzerland. J. Appl. Microbiol. 110, 513-520
7. 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
8. Lin, J., Yan, M., Sahin, O., Pereira, S., Chang, Y. J., and Zhang, Q. (2007) Effect of macrolide usage on emergence of erythromycin-resistant Campylobacter isolates in chickens. Antimicrob. Agents Chemother. 51, 1678-1686
9. Monteiro, M. A., Baqar, S., Hall, E. R., Chen, Y. H., Porter, C. K., Bentzel, D. E., Applebee, L., and Guerry, P. (2009) Capsule polysaccharide conjugate vaccine against diarrheal disease caused by Campylobacter jejuni. Infect. Immun. 77, 1128-1136
10. Szymanski, C. M., King, M., Haardt, M., and Armstrong, G. D. (1995) Campylobacter jejuni motility and invasion of Caco-2 cells. Infect. Immun. 63, 4295-4300
11. Guerry, P., Ewing, C. P., Schirm, M., Lorenzo, M., Kelly, J., Pattarini, D., Majam, G., Thibault, P., and Logan, S. (2006) Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol. Microbiol. 60, 299-311
12. 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
13. Szymanski, C. M., Burr, D. H., and Guerry, P. (2002) Campylobacter protein glycosylation affects host cell interactions. Infect. Immun. 70, 2242-2244
14. Guerry, P., Szymanski, C. M., Prendergast, M. M., Hickey, T. E., Ewing, C. P., Pattarini, D. L., and Moran, A. P. (2002) Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect. Immun. 70, 787-793
15. 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
16. Keo, T., Collins, J., Kunwar, P., Blaser, M. J., and Iovine, N. M. (2011) Campylobacter capsule and lipooligosaccharide confer resistance to serum and cationic antimicrobials. Virulence 2, 30-40
17. Guerry, P., and Szymanski, C. M. (2008) Campylobacter sugars sticking out. Trends Microbiol. 16, 428-435
18. 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
19. 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
20. 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
21. 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
22. 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
23. Kanipes, M. I., Papp-Szabo, E., Guerry, P., and Monteiro, M. A. (2006) Mutation of waaC, encoding heptosyltransferase I in Campylobacter jejuni 81-176, affects the structure of both lipooligosaccharide and capsular carbohydrate. J. Bacteriol. 188, 3273-3279
24. 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
25. 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
26. 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
27. Peng, W., Jayasuriya, A. B., Imamura, A., and Lowary, T. L. (2011) Synthesis of the 6-O-methyl-D-glycero-α-L-gluco-heptopyranose moiety present in the capsular polysaccharide from Campylobacter jejuni NCTC 11168. Org. Lett. 13, 5290-5293
28. McCallum, M., Shaw, G. S., and Creuzenet, C. (2011) Characterization of the dehydratase WcbK and the reductase WcaG involved in GDP-6-deoxy-manno- heptose biosynthesis in Campylobacter jejuni. Biochem. J. 439, 235-248
29. 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
30. Stern, R. J., Lee, T. Y., Lee, T. J., Yan, W., Scherman, M. S., Vissa, V. D., Kim, S. K., Wanner, B. L., and McNeil, M. R. (1999) Conversion of dTDP-4-keto-6-deoxyglucose to free dTDP-4-keto-rhamnose by the rmlC gene products of Escherichia coli and Mycobacterium tuberculosis. Microbiology 145, 663-671
31. Xiang, S. H., Haase, A. M., and Reeves, P. R. (1993) Variation of the rfb gene clusters in. Salmonella enterica. J. Bacteriol. 175, 4877-4884
32. Yao, Z., and Valvano, M. A. (1994) Genetic analysis of the O-specific lipopolysaccharide biosynthesis region (rfb) of Escherichia coli K-12 W3110. Identification of genes that confer group 6 specificity to Shigella flexneri serotypes Y and 4a. J. Bacteriol. 176, 4133-4143
33. Rizzi, M., Tonetti, M., Vigevani, P., Sturla, L., Bisso, A., Flora, A. D., Bordo, D., and Bolognesi, M. (1998) GDP-4-keto-6-deoxy-D-mannose epimerase/ reductase from Escherichia coli, a key enzyme in the biosynthesis of GDP-L-fucose, displays the structural characteristics of the RED protein homology superfamily. Structure 6, 1453-1465
34. Järvinen, N., Mäki, M., Räbinä, J., Roos, C., Mattila, P., and Renkonen, R. (2001) Cloning and expression of Helicobacter pylori GDP-L-fucose synthesizing enzymes (GMD and GMER) in Saccharomyces cerevisiae. Eur. J. Biochem. 268, 6458-6464
35. 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
36. Smallcombe, S. H., Patt, S. L., and Keifer, P. A. (1995) WET solvent suppression and its applications to LC NMR and high resolution NMR spectroscopy. J. Magn. Reson. A117, 295-303
37. Bax, A., and Davis, D. G. (1985) MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 65, 355-360
38. 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
39. 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
40. Creuzenet, C., Belanger, M., Wakarchuk, W. W., and Lam, J. S. (2000) Expression, purification, and biochemical characterization of WbpP, a new UDP-GlcNAc C4 epimerase from Pseudomonas aeruginosa serotype O6. J. Biol. Chem. 275, 19060-19067
41. 4 reductase from Helicobacter pylori. J. Biol. Chem. 275, 34873-34880
42. Shashkov, A. S., Pakulski, Z., Grzeszczyk, B., and Zamojski, A. (2001) Distribution of pyranose and furanose forms of 6-deoxyheptoses in water solution. Carbohydr. Res. 330, 289-294
43. Gabriel, O., and Lindquist, L. C. (1968) Biological mechanisms involved in the formation of deoxy sugars. IV. Enzymatic conversion of thymidine diphosphoglucose-4T to thymidine diphospho-4-keto-6-deoxyglucose-6T. J. Biol. Chem. 243, 1479-1484
44. Melo, A., Elliott, W. H., and Glaser, L. (1968) The mechanism of 6-deoxyhexose synthesis. I. Intramolecular hydrogen transfer catalyzed by deoxythymidine diphosphate D-glucose oxidoreductase. J. Biol. Chem. 243, 1467-1474
45. Hegeman, A. D., Gross, J. W., and Frey, P. A. (2002) Concerted and stepwise dehydration mechanisms observed in wild-type and mutated Escherichia coli dTDP-glucose 4,6-dehydratase. Biochemistry 41, 2797-2804
46. Melo, A., and Glaser, L. (1968) The mechanism of 6-deoxyhexose synthesis. II. Conversion of deoxythymidine diphosphate 4-keto-6-deoxy-D-glucose to deoxythymidine diphosphate L-rhamnose. J. Biol. Chem. 243, 1475-1478
47. Major, L. L., Wolucka, B. A., and Naismith, J. H. (2005) Structure and function of GDP-mannose-3′,5′-epimerase. An enzyme which performs three chemical reactions at the same active site. J. Am. Chem. Soc. 127, 18309-18320
48. 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
49. Ito, S. (2009) Features and applications of microbial sugar epimerases. Appl. Microbiol. Biotechnol. 84, 1053-1060
50. Dong, C., Major, L. L., Srikannathasan, V., Errey, J. C., Giraud, M. F., Lam, J. S., Graninger, M., Messner, P., McNeil, M. R., Field, R. A., Whitfield, C., and Naismith, J. H. (2007) RmlC, a C3′ and C5′ carbohydrate epimerase, appears to operate via an intermediate with an unusual twist boat conformation. J. Mol. Biol. 365, 146-159
51. Lau, S. T., and Tanner, M. E. (2008) Mechanism and active site residues of GDP-fucose synthase. J. Am. Chem. Soc. 130, 17593-17602
52. Aspinall, G. O., Monteiro, M. A., Pang, H., Kurjanczyk, L. A., and Penner, J. L. (1995) Lipo-oligosaccharide of Campylobacter lari strain PC 637. Structure of the liberated oligosaccharide and an associated extracellular polysaccharide. Carbohydr. Res. 279, 227-244
53. 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