The structures of the lipooligosaccharide and capsule polysaccharide of campylobacter jejuni genome sequenced strain NCTC 11168

European Journal of Biochemistry

Volumn 269, Issue 21, 2002, Pages 5119-5136

  St Michael, Frank ^a   Szymanski, Christine M ^a   Li, Jianjun ^a   Chan, Kenneth H ^a   Khieu, Nam Huan ^a   Larocque, Suzon ^a   Wakarchuk, Warren W ^a   Brisson, Jean Robert ^a   Monteiro, Mario A ^a,b  

^a NATIONAL RESEARCH COUNCIL CANADA   (Canada)

^b PFIZER INC   (United States)

Author keywords

Capsule; Electron spray ionization mass spectrometry; Heptose; High resolution magic angle spinning NMR; Lipooligosaccharide

Indexed keywords

BACTERIAL PROTEIN; CARBOHYDRATE DERIVATIVE; GANGLIOSIDE; GANGLIOSIDE GM1; GANGLIOSIDE GM2; OLIGOSACCHARIDE; POLYSACCHARIDE;

ARTICLE; BACTERIAL GENOME; BACTERIAL STRAIN; BIOSYNTHESIS; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE SEQUENCE; GENETIC COMPLEMENTATION; MASS SPECTROMETRY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; NUCLEAR OVERHAUSER EFFECT; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BACTERIAL CAPSULES; CAMPYLOBACTER JEJUNI; CARBOHYDRATE SEQUENCE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENOME, BACTERIAL; LIPOPOLYSACCHARIDES; MAGNETIC RESONANCE SPECTROSCOPY; METHYLATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; POLYSACCHARIDES, BACTERIAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

ACRONICTA LEPORINA; BACTERIA (MICROORGANISMS); CAMPYLOBACTER; CAMPYLOBACTER JEJUNI; MARTES PENNANTI; PROKARYOTA;

EID: 0036424834     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2002.03201.x     Document Type: Article

References (63)

1. Allos, B.M. (2001) Campylobacter jejuni infections: Update on emerging issues and trends. Clin. Infect. Dis. 32, 1201-1206.
2. Altekruse, S.F., Stern, N.J., Fields, P.I. & Swerdlow, D.L. (1999) Campylobacter jejuni - An emerging foodborne pathogen. Emerg. Infect. Dis. 5, 28-35.
3. Kaldor, J. & Speed, B.R. (1984) Guillain-Barré syndrome and Campylobacter jejuni: A serological study. Br. Med. J. Clin. Res. 288, 1867-1870
4. Rhodes, K.M. & Tattersfield, A.E. (1982) Guillain-Barré syndrome associated with Campylobacter infection. Br. Med. J. Clin. Res. 285, 173-174.
5. Jacobs, B.C., Endtz, H., van der Meche, F.G., Hazenberg, M.P., Achtereekte, H.A. & van Doorn, P.A. (1995) Serum anti-GQ1b IgG antibodies recognize surface epitopes on Campylobacter jejuni from patients with Miller Fisher syndrome. Ann. Neurol. 37, 260-264.
6. Moran, A.P., Penner, J.L. & Aspinall, G.O. (2000) Campylobacter lipopolysaccharides. In Campylobacter (Nachamkin, I. & Blaser, M.J., eds), pp. 241-257. American. Society for Microbiology, Washington, D.C.
7. Moran, A.P. & Prendergast, M.M. (2001) Molecular mimicry in Campylobacter jejuni and Helicobacter pylori lipopolysaccharides: Contribution of gastrointestinal infections to autoimmunity. J. Autoimmun. 16 241-256.
8. 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. & Barrell, B.G. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403, 665-668.
9. Whitfield, C. & Roberts, I.S. (1999) Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol. Microbiol. 31, 1307-1319.
10. Bacon, D.J., Szymanski, C.M., Burr, D.H., Silver, R.P., Alm, R.A. & Guerry, P. (2001) A phase-variable capsule is involved in virulence of Campylobacter jejuni 81-176. Mol. Microbiol. 40, 769-777.
11. Karlyshev, A.V., Linton, D., Gregson, N.A., Lastovica, A.J. & Wren, B.W. (2000) Genetic and biochemical evidence of a Campylobacter jejuni capsular polysaccharide that accounts for Penner serotype specificity. Mol. Microbiol. 35, 529-541.
12. Guerry, P., Szymanski, C.M., Prendergast, M.M., Hickey, T.E., Ewing, C.P., Pattarini, D.L. & Moran, A.P. (2002) Phase variation of Campylobacter jejuni 81-176 lipooligosaccharide affects ganglioside mimicry and invasiveness in vitro. Infect. Immun. 70, 787-793.
13. Yuki, N., Taki, T., Inagaki, F., Kasama, T., Takahashi, M., Saito, K., Handa, S. & Miyatake, T. (1993) A bacterium lipopolysaccharide that elicits Guillain-Barré syndrome has a GM1 ganglioside-like structure. J. Exp. Med. 178, 1771-1775.
14. Brooks, B.W., Robertson, R.H., Lutze-Wallace, C.L. & Pfahler, W. (2001) Identification, characterization, and variation in expression of two serologically distinct O-antigen epitopes in lipopolysaccharides of Campylobacter fetus serotype A strains. Infect. Immun. 69, 7596-7602.
15. Guerry, P., Ewing, C.P., Hickey, T.E., Prendergast, M.M. & Moran, A.P. (2000) Sialylation of lipooligosaccharide cores affects immunogenicity and serum resistance of Campylobacter jejuni. Infect. Immun. 68, 6656-6662.
16. 13C NMR analysis. J. Biol. Chem. 275, 3896-3906.
17. Linton, D., Gilbert, M., Hitchen, P.G., Dell, A., Morris, H.R., Wakarchuk, W.W., Gregson, N.A. & Wren, B.W. (2000) Phase variation of a beta-1,3 galactosyltransferase involved in generation of the ganglioside GM1-like lipooligosaccharide of Campylobacter jejuni. Mol. Microbiol. 37, 501-514.
18. Ahmed, I.H., Manning, G., Wassenaar, T.M., Cawthraw, S. & Newell, D.G. (2002) Identification of genetic differences between two Campylobacter jejuni strains with different colonization potentials. Microbiology 148, 1203-1212.
19. Westphal, O. & Jann, K. (1965) Bacterial lipopolysaccharide. Extraction with phenol-water and further applications of the procedure. Methods Carbohydr. Chem. 5, 88-91.
20. Sawardeker, D.G., Sloneker, J.H. & Jeanes, A. (1965) Quantitative determination of monosaccharides as their alditol acetates by gas liquid chromatography. Anal. Chem. 37, 1602-1604.
21. Loetein, K., Lindberg, B. & Lonngren, J. (1978) Assignment of absolute configuration of sugars by G.L.C. of their acetylated glycosides formed from chiral alcohols. Carbohydr. Res. 62, 359-362.
22. Ciucanu, I. & Kerek, F. (1994) A simple and rapid method for the permethylation of carbohydrates. Carbohydr. Res. 131, 209-217.
23. Pritchard, D.G., Rener, B.P., Furner, R.L., Huang, D.H. & Krishna, N.R. (1988) Structure of the group G streptococcal polysaccharide. Carbohydr. Res. 173, 255-262.
24. Labigne-Roussel, A., Courcoux, P. & Tompkins, L. (1988) Gene disruption and replacement as a feasible approach for mutagenesis of Campylobacter jejuni. J. Bacteriol. 170, 1704-1708.
25. Guerry, P., Yao, R., Alm, R.A., Burr, D.H. & Trust, T.J. (1994) Systems of experimental genetics for Campylobacter species. Methods Enzymol. 235, 474-481.
26. Schmitz, A., Josenhans, C. & Suerbaum, S. (1997) Cloning and characterization of the Helicobacter pylori flbA gene, which codes for a membrane protein involved in coordinated expression of flagellar genes. J. Bacteriol. 179, 987-997.
27. Salloway, S., Mermel, L.A., Seamans, M., Aspinall, G.O., Nam Shin, J.E., Kurjanczyk, L.A. & Penner, J.L. (1996) Miller-Fisher syndrome associated with Campylobacter jejuni bearing lipopoly-saccharide molecules that mimic human ganglioside GD3. Infect. Immun. 64, 2945-2949.
28. Hitchcock, P.J. & Brown, T.M. (1983) Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J. Bacteriol. 154, 269-277.
29. Komuro, T. & Galanos, C. (1988) Analysis of Salmonella lipo-polysaccharides by sodium deoxycholate-polyacrylamide gel electrophoresis. J. Chromatogr. 450, 381-387.
30. Tsai, C.M. & Frasch, C.E. (1982) A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119, 115-119.
31. Fomsgaard, A., Freudenberg, M.A. & Galanos, C. (1990) Modification of the silver staining technique to detect lipopolysaccharide in polyacrylamide gels. J. Clin. Microbiol. 28, 2627-2631.
32. Guard-Petter, J., Lakshmi, B., Carlson, R. & Ingram, K. (1995) Characterization of lipopolysaccharide heterogeneity in Salmonella enteritidis by an improved gel electrophoresis method. Appl. Environ. Microbiol. 61, 2845-2851.
33. Uhrín, D. & Brisson, J.R. (2000) Structure determination of microbial polysaccharides by high resolution NMR spectroscopy. In NMR in Microbiology: Theory and Applications (Barbotin, J.N. & Portais, J.C., eds), pp. 165-210. Horizon Scientific Press, Wymondham, UK.
34. Jachymek, W., Niedziela, T., Petersson, C., Lugowski, C., Czaja, J. & Kenne, L. (1999) Structures of the O-specific polysaccharides from Yokenella regensburgei (Koserella trabulsii) strains PCM 2476, 2477, 2478, and 2494: High-resolution magic-angle spinning NMR investigation of the O-specific polysaccharides in native lipopolysaccharides and directly on the surface of living bacteria. Biochemistry 38, 11788-11795.
35. Peters, T., Meyer, B., Stuike, P., Somorjai, R. & Brisson, J.R. (1993) A Monte Carlo method for conformational analysis of saccharides. Carbohydr. Res. 238, 49-73.
36. Tvaroška, I. & Pérez, S. (1986) Conformational-energy calculations for oligosaccharides: A comparison of methods and a strategy of calculation. Carbohydr. Res. 149, 389-410.
37. Homans, S.W. (1990) A molecular mechanical force field for the conformational analysis of oligosaccharides: Comparison of theoretical and crystal structures of Manα1-3Manβ-14GlcNAc. Biochemistry 29, 9110-9118.
38. Kogan, G. & Uhrín, D. (2000) Current NMR methods in the structural elucidation of polysaccharides. In New Advances in Analytical Chemistry (Atta-ur-Rahman, ed.), pp. 73-134. Harwood Academic, Amsterdam.
39. Duus, J.Ø., Gotfredsen, C.H. & Bock, K. (2000) Carbohydrate structural determination by NMR spectroscopy: Modern methods and limitations. Chem. Rev. 100, 4589-4614.
40. Aspinall, G.O., McDonald, A.G., Pang, H., Kurjanczyk, L.A. & Penner, J.L. (1994) Lipopolysaccharides of Campylobacter jejuni serotype O:19: Structures of core oligosaccharide regions from the serostrain and two bacterial isolates from patients with the Guillain-Barré syndrome. Biochemistry 33, 241-249.
41. Vinogradov, E.V., Holst, O., Thomas-Oates, J.E., Broady, K.W. & Brade, H. (1992) The structure of the O-antigenic polysaccharide from lipopolysaccharide of Vibrio cholerae strain H11 (non-O1). Eur. J. Biochem. 210, 491-498.
42. Sadovskaya, I., Brisson, J.R., Khieu, N.H., Mutharia, L.M. & Altman, E. (1998) Structural characterization of the lipopolysaccharide O-antigen and capsular polysaccharide of Vibrio ordalii serotype O:2. Eur. J. Biochem. 253, 319-327.
43. Andrianopoulos, K., Wang, L. & Reeves, P.R. (1998) Identification of the fucose synthetase gene in the colanic acid gene cluster of Escherichia coli K-12. J. Bacteriol. 180, 998-1001.
44. Nassau, P.M., Martin, S.L., Brown, R.E., Weston, A., Monsey, D., McNeil, M.R. & Duncan, K. (1996) Galactofuranose biosynthesis in Escherichia coli K-12: identification and cloning of UDP-galactopyranose mutase. J. Bacteriol. 178, 1047-1052.
45. Sieberth, V., Rigg, G.P., Roberts, I.S. & Jann, K. (1995) Expression and characterization of UDPGlc dehydrogenase (KfiD), which is encoded in the type-specific region 2 of the Escherichia coli K5 capsule genes. J. Bacteriol. 177, 4562-4565.
46. Kneidinger, B., Graninger, M., Puchberger, M., Kosma, P. & Messner, P. (2001) Biosynthesis of nucleotide-activated D-glycero-D-manno-heptose. J. Biol. Chem. 276, 20935-20944.
47. Naess, V. & Hofstad, T. (1984) Chemical studies of partially hydrolysed lipopolysaccharides from four strains of Campylobacter jejuni and two strains of Campylobacter coli. J. Gen. Microbiol. 130, 2783-2789.
48. Gilbert, M., Karwaski, M.F., Bernatchez, S., Young, N.M., Taboada, E., Michniewicz, J., Cunningham, A.M. & Wakarchuk, W.W. (2002) The genetic bases for the variation in the lipooligosaccharide of the mucosal pathogen, Campylobacter jejuni. Biosynthesis of sialylated ganglioside mimics in the core oligosaccharide. J. Biol. Chem. 277, 327-337.
49. Hanniffy, O.M., Shashkov, A.S., Moran, A.P., Senchenkova, S.N. & Savage, A.V. (2001) Chemical structure of the core oligosaccharide of aerotolerant Campylobacter jejuni O:2 lipopolysaccharide. Carbohydr. Res. 330, 223-229.
50. Yuki, N., Yoshino, H., Sato, S. & Miyatake, T. (1990) Acute axonal polyneuropathy associated with anti-GM1 antibodies following Campylobacter enteritis. Neurology 40, 1900-1902.
51. Vinogradov, E., Frirdich, E., MacLean, L.L., Perry, M.B., Petersen, B.O., Duus, J.O. & Whitfield, C. (2002) Structures of lipopolysaccharides from Klebsiella pneumoniae. Elucidation 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.
52. Ninomiya, T., Sugiura, N., Tawada, A., Sugimoto, K., Watanabe, H. & Kimata, K. (2002) Molecular cloning and characterization of chondroitin polymerase from Escherichia coli strain K4. J. Biol. Chem. 277, 21567-21575.
53. Thibault, P., Logan, S.M., Kelly, J.F., Brisson, J.R., Ewing, C.P., Trust, T.J. & Guerry, P. (2001) Identification of the carbohydrate moieties and glycosylation motifs in Campylobacter jejuni flagellin. J. Biol. Chem. 276, 34862-34870.
54. Jabbouri, S., Relic, B., Hanin, M., Kamalaprija, P., Burger, U., Prome, D., Prome, J.C. & Broughton, W.J. (1998) nolO and noeI (HsnIII) of Rhizobium sp. NGR234 are involved in 3-O-carbamoylation and 2-O-methylation of Nod factors. J. Biol. Chem. 273, 12047-12055.
55. Serino, L. & Virji, M. (2002) Genetic and functional analysis of the phosphorylcholine moiety of commensal Neisseria lipopolysaccharide. Mol. Microbiol. 43, 437-448.
56. Kooistra, O., Luneberg, E., Knirel, Y.A., Frosch, M. & Zahringer, U. (2002) N-Methylation in polylegionaminic acid is associated with the phase-variable epitope of Legionella pneumophila serogroup 1 lipopolysaccharide. Identification of 5-(N,N-dimethylacetimidoyl) amino and 5-acetimidoyl (N-methyl) amino-7-acetamido-3,5,7,9-tetradeoxynon-2-ulosonic acid in the O-chain polysaccharide. Eur. J. Biochem. 269, 560-572.
57. Forsberg, L.S., Bhat, U.R. & Carlson, R.W. (2000) Structural characterization of the O-antigenic polysaccharide of the lipopolysaccharide from Rhizobium etli strain CE3. A unique O-acetylated glycan of discrete size, containing 3-O-methyl-6-deoxy-L-talose and 2,3,4-tri-O-methyl-1 fucose. J. Biol. Chem. 275, 18851-18863.
58. Hisatsune, K., Kondo, S., Isshiki, Y., Iguchi, T. & Haishima, Y. (1993) Occurrence of 2-O-methyl-N-(3-deoxy-L-glycero-tetronyl)-D-perosamine (4-amino-4,6-dideoxy-D-manno-pyranose) in lipopolysaccharide from Ogawa but not from Inaba O forms of O1 Vibrio cholerae. Biochem. Biophys. Res. Commun. 190, 302-307.
59. Schäffer, C., Wugeditsch, T., Kahlig, H., Scheberl, A., Zayni, S. & Messner, P. (2002) The surface layer (S-layer) glycoprotein of Geobacillus stearothermophilus NRS 2004/3a. Analysis of its glycosylation. J. Biol. Chem. 277, 6230-6239.
60. Stimson, E., Virji, M., Barker, S., Panico, M., Blench, I., Saunders, J., Payne, G., Moxon, E.R., Dell, A. & Morris, H.R. (1996) Discovery of a novel protein modification: alpha-glycerophosphate is a substituent of meningococcal pilin. Biochem. J. 316 (1), 29-33.
61. Harvey, H.A., Swords, W.E. & Apicella, M.A. (2001) The mimicry of human glycolipids and glycosphingolipids by the lipooligosaccharides of pathogenic Neisseria and Haemophilus. J. Autoimmun. 16, 257-262.
62. Lysenko, E.S., Gould, J., Bals, R., Wilson, J.M. & Weiser, J.N. (2000) Bacterial phosphorylcholine decreases susceptibility to the antimicrobial peptide LL-37/hCAP18 expressed in the upper respiratory tract. Infect. Immun. 68, 1664-1671.
63. Niebel, A., Gressent, F., Bono, J.J., Ranjeva, R. & Cullimore, J. (1999) Recent advances in the study of nod factor perception and signal transduction. Biochimie 81, 669-674.