Role of capsular modified heptose in the virulence of Campylobacter jejuni

Molecular Microbiology

Volumn 96, Issue 6, 2015, Pages 1136-1158

  Wong, Anthony ^a   Lange, Dirk ^a,e   Houle, Sebastien ^b   Arbatsky, Nikolay P ^c   Valvano, Miguel A ^a,d   Knirel, Yuriy A ^c   Dozois, Charles M ^b   Creuzenet, Carole ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b INRS INSTITUT ARMAND FRAPPIER   (Canada)

^c N D ZELINSKY INSTITUTE OF ORGANIC CHEMISTRY   (Russian Federation)

^d QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^e JACK BELL RESEARCH CENTRE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HEPTOSE; BACTERIAL POLYSACCHARIDE; BILE ACID; CARRIER PROTEIN; EPIMERASE; ESCHERICHIA COLI PROTEIN; KPSM PROTEIN, E COLI; MULTIENZYME COMPLEX; OXIDOREDUCTASE; WCAG PROTEIN, E COLI;

ARTICLE; BACTERIAL VIRULENCE; CAMPYLOBACTER JEJUNI; CELL ADHESION; CELL INVASION; CELL SURVIVAL; CHICKEN; CONTROLLED STUDY; GENE; GENE CLUSTER; GENE FUNCTION; GENE INACTIVATION; INTESTINE CELL; MACROPHAGE; MLGHB GENE; MLGHC GENE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; WCAG GENE; ANIMAL; BACTERIAL CAPSULE; CACO 2 CELL LINE; CAMPYLOBACTERIOSIS; CARBOHYDRATE ANALYSIS; ENZYMOLOGY; GASTROINTESTINAL TRACT; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MOUSE; PATHOGENICITY; RAW 264.7 CELL LINE; VIRULENCE;

BACTERIA (MICROORGANISMS); CAMPYLOBACTER JEJUNI; MURINAE;

ANIMALS; BACTERIAL CAPSULES; BILE ACIDS AND SALTS; CACO-2 CELLS; CAMPYLOBACTER INFECTIONS; CAMPYLOBACTER JEJUNI; CARBOHYDRATE EPIMERASES; CARBOHYDRATE SEQUENCE; CHICKENS; ESCHERICHIA COLI PROTEINS; GASTROINTESTINAL TRACT; GENE KNOCKOUT TECHNIQUES; HEPTOSES; HUMANS; KETONE OXIDOREDUCTASES; MEMBRANE TRANSPORT PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; POLYSACCHARIDES, BACTERIAL; RAW 264.7 CELLS; VIRULENCE;

EID: 84930766119     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12995     Document Type: Article

References (125)

1. van Alphen, L.B., Wenzel, C.Q., Richards, M.R., Fodor, C., Ashmus, R.A., Stahl, M., etal. (2014) Biological roles of the O-methyl phosphoramidate capsule modification in Campylobacter jejuni. PLoS ONE 9: e87051.
2. Ashgar, S.S., Oldfield, N.J., Wooldridge, K.G., Jones, M.A., Irving, G.J., Turner, D.P., and Ala'Aldeen, D.A. (2007) CapA, an autotransporter protein of Campylobacter jejuni, mediates association with human epithelial cells and colonization of the chicken gut. J Bacteriol 189: 1856-1865.
3. 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.
4. 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.
5. Aspinall, G.O., Lynch, C.M., Pang, H., Shaver, R.T., and Moran, A.P. (1995a) Chemical structures of the core region of Campylobacter jejuni O:3 lipopolysaccharide and an associated polysaccharide. Eur J Biochem 231: 570-578.
6. Aspinall, G.O., Monteiro, M.A., Pang, H., Kurjanczyk, L.A., and Penner, J.L. (1995b) Lipo-oligosaccharide of Campylobacter lari strain PC 637. Structure of the liberated oligosaccharide and an associated extracellular polysaccharide. Carbohydr Res 279: 227-244.
7. 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.
8. 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.
9. Beery, J.T., Hugdahl, M.B., and Doyle, M.P. (1988) Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl Environ Microbiol 54: 2365-2370.
10. Begley, M., Gahan, C.G., and Hill, C. (2002) Bile stress response in Listeria monocytogenes LO28: adaptation, cross-protection, and identification of genetic loci involved in bile resistance. Appl Environ Microbiol 68: 6005-6012.
11. Benz, I., and Schmidt, M.A. (2001) Glycosylation with heptose residues mediated by the aah gene product is essential for adherence of the AIDA-I adhesin. Mol Microbiol 40: 1403-1413.
12. Biswas, D., Itoh, K., and Sasakawa, C. (2000) Uptake pathways of clinical and healthy animal isolates of Campylobacter jejuni into INT-407 cells. FEMS Immunol Med Microbiol 29: 203-211.
13. Biswas, D., Fernando, U.M., Reiman, C.D., Willson, P.J., Townsend, H.G., Potter, A.A., and Allan, B.J. (2007) Correlation between in vitro secretion of virulence-associated proteins of Campylobacter jejuni and colonization of chickens. Curr Microbiol 54: 207-212.
14. Black, R., Levine, M., Clements, M., Hughes, T., and Blaser, M. (1988) Experimental Campylobacter infections in humans. J Infect Dis 157: 472-478.
15. Boulnois, G.J., and Roberts, I.S. (1990) Genetics of capsular polysaccharide production in bacteria. Curr Top Microbiol Immunol 150: 1-18.
16. Boulnois, G.J., Roberts, I.S., Hodge, R., Hardy, K.R., Jann, K.B., and Timmis, K.N. (1987) Analysis of the K1 capsule biosynthesis genes of Escherichia coli: definition of three functional regions for capsule production. Mol Gen Genet 208: 242-246.
17. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
18. Butty, F.D., Aucoin, M., Morrison, L., Ho, N., Shaw, G.S., 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.
19. Campbell, N.B., Ruaux, C.G., Shifflett, D.E., Steiner, J.M., Williams, D.A., and Blikslager, A.T. (2004) Physiological concentrations of bile salts inhibit recovery of ischemic-injured porcine ileum. Am J Physiol Gastrointest Liver Physiol 287: G399-G407.
20. Carrillo, C.D., Taboada, E., Nash, J.H., Lanthier, P., Kelly, J., Lau, P.C., etal. (2004) Genome-wide expression analyses of Campylobacter jejuni NCTC11168 reveals coordinate regulation of motility and virulence by flhA. J Biol Chem 279: 20327-20338.
21. Champion, O.L., Karlyshev, A.V., Senior, N.J., Woodward, M., La Ragione, R., Howard, S.L., etal. (2010) Insect infection model for Campylobacter jejuni reveals that O-methyl phosphoramidate has insecticidal activity. J Infect Dis 201: 776-782.
22. 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.
23. Corcionivoschi, N., Clyne, M., Lyons, A., Elmi, A., Gundogdu, O., Wren, B.W., etal. (2009) Campylobacter jejuni cocultured with epithelial cells reduces surface capsular polysaccharide expression. Infect Immun 77: 1959-1967.
24. Corcoran, A.T., Annuk, H., and Moran, A.P. (2006) The structure of the lipid anchor of Campylobacter jejuni polysaccharide. FEMS Microbiol Lett 257: 228-235.
25. Cortes, G., Borrell, N., de Astorza, B., Gomez, C., Sauleda, J., and Alberti, S. (2002) Molecular analysis of the contribution of the capsular polysaccharide and the lipopolysaccharide O side chain to the virulence of Klebsiella pneumoniae in a murine model of pneumonia. Infect Immun 70: 2583-2590.
26. Cuthbertson, L., Kos, V., and Whitfield, C. (2010) ABC transporters involved in export of cell surface glycoconjugates. Microbiol Mol Biol Rev 74: 341-362.
27. Day, W.A., Jr, Sajecki, J.L., Pitts, T.M., and Joens, L.A. (2000) Role of catalase in Campylobacter jejuni intracellular survival. Infect Immun 68: 6337-6345.
28. De Melo, M.A., Gabbiani, G., and Pechere, J.C. (1989) Cellular events and intracellular survival of Campylobacter jejuni during infection of HEp-2 cells. Infect Immun 57: 2214-2222.
29. Donahue, J.P., Israel, D.A., Peek, R.M., Blaser, M.J., and Miller, G.G. (2000) Overcoming the restriction barrier to plasmid transformation of Helicobacter pylori. Mol Microbiol 37: 1066-1074.
30. Dugar, G., Herbig, A., Forstner, K.U., Heidrich, N., Reinhardt, R., Nieselt, K., and Sharma, C.M. (2013) High-resolution transcriptome maps reveal strain-specific regulatory features of multiple Campylobacter jejuni isolates. PLoS Genet 9: e1003495.
31. Everest, P.H., Goossens, H., Butzler, J.P., Lloyd, D., Knutton, S., Ketley, J.M., and Williams, P.H. (1992) Differentiated Caco-2 cells as a model for enteric invasion by Campylobacter jejuni and C. coli. J Med Microbiol 37: 319-325.
32. Fauchere, J.L., Rosenau, A., Veron, M., Moyen, E.N., Richard, S., and Pfister, A. (1986) Association with HeLa cells of Campylobacter jejuni and Campylobacter coli isolated from human feces. Infect Immun 54: 283-287.
33. Ferruzza, S., Rossi, C., Scarino, M.L., and Sambuy, Y. (2012) A protocol for in situ enzyme assays to assess the differentiation of human intestinal Caco-2 cells. Toxicol in Vitro 26: 1247-1251.
34. Fomsgaard, A., Freudenberg, M.A., and Galanos, C. (1990) Modification of the silver staining technique to detect lipopolysaccharide in polyacrylamide gels. J Clin Microbiol 28: 2627-2631.
35. Ganan, M., Campos, G., Munoz, R., Carrascosa, A.V., de Pascual-Teresa, S., and Martinez-Rodriguez, A.J. (2010) Effect of growth phase on the adherence to and invasion of Caco-2 epithelial cells by Campylobacter. Int J Food Microbiol 140: 14-18.
36. Gerritsen van der Hoop, A., and Veringa, E.M. (1993) Cholecystitis caused by Campylobacter jejuni. Clin Infect Dis 17: 133.
37. Godschalk, P.C., Heikema, A.P., Gilbert, M., Komagamine, T., Ang, C.W., Glerum, J., etal. (2004) The crucial role of Campylobacter jejuni genes in anti-ganglioside antibody induction in Guillain-Barre syndrome. J Clin Invest 114: 1659-1665.
38. Godschalk, P.C., Kuijf, M.L., Li, J., St Michael, F., Ang, C.W., Jacobs, B.C., etal. (2007) Structural characterization of Campylobacter jejuni lipooligosaccharide outer cores associated with Guillain-Barre and Miller Fisher syndromes. Infect Immun 75: 1245-1254.
39. Guerry, P., Ewing, C.P., Hickey, T.E., Prendergast, M.M., and Moran, A.P. (2000) Sialylation of lipooligosaccharide cores affects immunogenicity and serum resistance of Campylobacter jejuni. Infect Immun 68: 6656-6662.
40. 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.
41. Guerry, P., Ewing, C.P., Schirm, M., Lorenzo, M., Kelly, J., Pattarini, D., etal. (2006) Changes in flagellin glycosylation affect Campylobacter autoagglutination and virulence. Mol Microbiol 60: 299-311.
42. Hashimoto, Y., Li, N., Yokoyama, H., and Ezaki, T. (1993) Complete nucleotide sequence and molecular characterization of ViaB region encoding Vi antigen in Salmonella typhi. J Bacteriol 175: 4456-4465.
43. Heckman, K.L., and Pease, L.R. (2007) Gene splicing and mutagenesis by PCR-driven overlap extension. Nat Protoc 2: 924-932.
44. Heuermann, D., and Haas, R. (1998) A stable shuttle vector system for efficient genetic complementation of Helicobacter pylori strains by transformation and conjugation. Mol Gen Genet 257: 519-528.
45. Hitchcock, P.J., and Brown, T.M. (1983) Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 154: 269-277.
46. 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.
47. Hsieh, Y.C., Liang, S.M., Tsai, W.L., Chen, Y.H., Liu, T.Y., and Liang, C.M. (2003) Study of capsular polysaccharide from Vibrio parahaemolyticus. Infect Immun 71: 3329-3336.
48. Jann, K., Dengler, T., and Jann, B. (1992) Core-lipid A on the K40 polysaccharide of Escherichia coli O8:K40:H9, a representative of group I capsular polysaccharides. Zentralbl Bakteriol 276: 196-204.
49. Jin, S., Joe, A., Lynett, J., Hani, E.K., Sherman, P., and Chan, V.L. (2001) JlpA, a novel surface-exposed lipoprotein specific to Campylobacter jejuni, mediates adherence to host epithelial cells. Mol Microbiol 39: 1225-1236.
50. Jones, M.A., Marston, K.L., Woodall, C.A., Maskell, D.J., Linton, D., Karlyshev, A.V., etal. (2004) Adaptation of Campylobacter jejuni NCTC11168 to high-level colonization of the avian gastrointestinal tract. Infect Immun 72: 3769-3776.
51. Kakuda, T., and DiRita, V.J. (2006) Cj1496c encodes a Campylobacter jejuni glycoprotein that influences invasion of human epithelial cells and colonization of the chick gastrointestinal tract. Infect Immun 74: 4715-4723.
52. Karlyshev, A.V., and Wren, B.W. (2001) Detection and initial characterization of novel capsular polysaccharide among diverse Campylobacter jejuni strains using alcian blue dye. J Clin Microbiol 39: 279-284.
53. Karlyshev, A.V., and Wren, B.W. (2005) Development and application of an insertional system for gene delivery and expression in Campylobacter jejuni. Appl Environ Microbiol 71: 4004-4013.
54. Karlyshev, A.V., Henderson, J., Ketley, J.M., and Wren, B.W. (1999) Procedure for the investigation of bacterial genomes: random shot-gun cloning, sample sequencing and mutagenesis of Campylobacter jejuni. Biotechniques 26: 54, 56.
55. Karlyshev, A.V., Linton, D., Gregson, N.A., Lastovica, A.J., and 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.
56. Karlyshev, A.V., McCrossan, M.V., and Wren, B.W. (2001) Demonstration of polysaccharide capsule in Campylobacter jejuni using electron microscopy. Infect Immun 69: 5921-5924.
57. Karlyshev, A.V., Everest, P., Linton, D., Cawthraw, S., Newell, D.G., and Wren, B.W. (2004) The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 150: 1957-1964.
58. Karlyshev, A.V., Champion, O.L., Churcher, C., Brisson, J.R., Jarrell, H.C., Gilbert, M., etal. (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.
59. Karmali, M.A., Penner, J.L., Fleming, P.C., Williams, A., and Hennessy, J.N. (1983) The serotype and biotype distribution of clinical isolates of Campylobacter jejuni and Campylobacter coli over a three-year period. J Infect Dis 147: 243-246.
60. 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.
61. Kiehlbauch, J.A., Albach, R.A., Baum, L.L., and Chang, K.P. (1985) Phagocytosis of Campylobacter jejuni and its intracellular survival in mononuclear phagocytes. Infect Immun 48: 446-451.
62. Kilcoyne, M., Moran, A.P., Shashkov, A.S., Senchenkova, S.N., Ferris, J.A., Corcoran, A.T., and Savage, A.V. (2006) Molecular origin of two polysaccharides of Campylobacter jejuni 81116. FEMS Microbiol Lett 263: 214-222.
63. 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.
64. 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.
65. Konkel, M.E., Hayes, S.F., Joens, L.A., and Cieplak, W., Jr (1992) Characteristics of the internalization and intracellular survival of Campylobacter jejuni in human epithelial cell cultures. Microb Pathog 13: 357-370.
66. Konkel, M.E., Kim, B.J., Rivera-Amill, V., and Garvis, S.G. (1999) Bacterial secreted proteins are required for the internalization of Campylobacter jejuni into cultured mammalian cells. Mol Microbiol 32: 691-701.
67. Konkel, M.E., Klena, J.D., Rivera-Amill, V., Monteville, M.R., Biswas, D., Raphael, B., and Mickelson, J. (2004) Secretion of virulence proteins from Campylobacter jejuni is dependent on a functional flagellar export apparatus. J Bacteriol 186: 3296-3303.
68. Konkel, M.E., Christensen, J.E., Keech, A.M., Monteville, M.R., Klena, J.D., and Garvis, S.G. (2005) Identification of a fibronectin-binding domain within the Campylobacter jejuni CadF protein. Mol Microbiol 57: 1022-1035.
69. Kroll, J.S., Hopkins, I., and Moxon, E.R. (1988) Capsule loss in H. influenzae type b occurs by recombination-mediated disruption of a gene essential for polysaccharide export. Cell 53: 347-356.
70. Lee, A., O'Rourke, J.L., Barrington, P.J., and Trust, T.J. (1986) Mucus colonization as a determinant of pathogenicity in intestinal infection by Campylobacter jejuni: a mouse cecal model. Infect Immun 51: 536-546.
71. Lin, J., Sahin, O., Michel, L.O., and Zhang, Q. (2003) Critical role of multidrug efflux pump CmeABC in bile resistance and in vivo colonization of Campylobacter jejuni. Infect Immun 71: 4250-4259.
72. Lin, J., Cagliero, C., Guo, B., Barton, Y.W., Maurel, M.C., Payot, S., and Zhang, Q. (2005) Bile salts modulate expression of the CmeABC multidrug efflux pump in Campylobacter jejuni. J Bacteriol 187: 7417-7424.
73. 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.
74. McCallum, M., Shaw, S.D., Shaw, G.S., and Creuzenet, C. (2012) Complete 6-deoxy-D-altro-heptose biosynthesis pathway from Campylobacter jejuni: more complex than anticipated. J Biol Chem 287: 29776-29788.
75. McCallum, M., Shaw, G.S., and Creuzenet, C. (2013) Comparison of predicted epimerases and reductases of the Campylobacter jejuni D-altro- and L-gluco-heptose synthesis pathways. J Biol Chem 288: 19569-19580.
76. McNally, D.J., Lamoureux, M.P., Karlyshev, A.V., Fiori, L.M., Li, J., Thacker, G., etal. (2007) Commonality and biosynthesis of the O-methyl phosphoramidate capsule modification in Campylobacter jejuni. J Biol Chem 282: 28566-28576.
77. Manninen, K.I., Prescott, J.F., and Dohoo, I.R. (1982) Pathogenicity of Campylobacter jejuni isolates from animals and humans. Infect Immun 38: 46-52.
78. Maue, A.C., Mohawk, K.L., Giles, D.K., Poly, F., Ewing, C.P., Jiao, Y., etal. (2013) The polysaccharide capsule of Campylobacter jejuni modulates the host immune response. Infect Immun 81: 665-672.
79. Merkx-Jacques, A., Obhi, R.K., Bethune, G., and Creuzenet, C. (2004) The Helicobacter pylori flaA1 and wbpB genes control lipopolysaccharide and flagellum synthesis and function. J Bacteriol 186: 2253-2265.
80. Misawa, N., and Blaser, M.J. (2000) Detection and characterization of autoagglutination activity by Campylobacter jejuni. Infect Immun 68: 6168-6175.
81. Mishu, B., and Blaser, M.J. (1993) Role of infection due to Campylobacter jejuni in the initiation of Guillain-Barre syndrome. Clin Infect Dis 17: 104-108.
82. Mixter, P.F., Klena, J.D., Flom, G.A., Siegesmund, A.M., and Konkel, M.E. (2003) In vivo tracking of Campylobacter jejuni by using a novel recombinant expressing green fluorescent protein. Appl Environ Microbiol 69: 2864-2874.
83. Newell, D.G., and Pearson, A. (1984) The invasion of epithelial cell lines and the intestinal epithelium of infant mice by Campylobacter jejuni/coli. J Diarrhoeal Dis Res 2: 19-26.
84. Newell, D.G., McBride, H., Saunders, F., Dehele, Y., and Pearson, A.D. (1985) The virulence of clinical and environmental isolates of Campylobacter jejuni. J Hyg (Lond) 94: 45-54.
85. 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.
86. Nuijten, P.J., Bleumink-Pluym, N.M., Gaastra, W., and van der Zeijst, B.A. (1989) Flagellin expression in Campylobacter jejuni is regulated at the transcriptional level. Infect Immun 57: 1084-1088.
87. Pace, J.L., Chai, T.J., Rossi, H.A., and Jiang, X. (1997) Effect of bile on Vibrio parahaemolyticus. Appl Environ Microbiol 63: 2372-2377.
88. Parkhill, J., Wren, B.W., Mungall, K., Ketley, J.M., Churcher, C., Basham, D., etal. (2000) The genome sequence of the food-borne pathogen Campylobacter jejuni reveals hypervariable sequences. Nature 403: 665-668.
89. Pavelka, M.S., Jr, Hayes, S.F., and Silver, R.P. (1994) Characterization of KpsT, the ATP-binding component of the ABC-transporter involved with the export of capsular polysialic acid in Escherichia coli K1. J Biol Chem 269: 20149-20158.
90. Pei, Z., and Blaser, M.J. (1993) PEB1, the major cell-binding factor of Campylobacter jejuni, is a homolog of the binding component in gram-negative nutrient transport systems. J Biol Chem 268: 18717-18725.
91. Penner, J.L., Hennessy, J.N., and Congi, R.V. (1983) Serotyping of Campylobacter jejuni and Campylobacter coli on the basis of thermostable antigens. Eur J Clin Microbiol 2: 378-383.
92. Perez de la Cruz Moreno, M., Oth, M., Deferme, S., Lammert, F., Tack, J., Dressman, J., and Augustijns, P. (2006) Characterization of fasted-state human intestinal fluids collected from duodenum and jejunum. J Pharm Pharmacol 58: 1079-1089.
93. 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.
94. Peterson, P.K., Verhoef, J., and Quie, P.G. (1977) Influence of temperature on opsonization and phagocytosis of staphylococci. Infect Immun 15: 175-179.
95. Pfaffl, M.W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
96. Preston, M.A., and Penner, J.L. (1989) Characterization of cross-reacting serotypes of Campylobacter jejuni. Can J Microbiol 35: 265-273.
97. Rautelin, H., and Hanninen, M.L. (2000) Campylobacters: the most common bacterial enteropathogens in the Nordic countries. Ann Med 32: 440-445.
98. 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.
99. 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.
100. Roberts, I.S., Mountford, R., Hodge, R., Jann, K.B., and Boulnois, G.J. (1988a) Common organization of gene clusters for production of different capsular polysaccharides (K antigens) in Escherichia coli. J Bacteriol 170: 1305-1310.
101. Roberts, M., Roberts, I., Korhonen, T.K., Jann, K., Bitter-Suermann, D., Boulnois, G.J., and Williams, P.H. (1988b) DNA probes for K-antigen (capsule) typing of Escherichia coli. J Clin Microbiol 26: 385-387.
102. Rowe, S., Hodson, N., Griffiths, G., and Roberts, I.S. (2000) Regulation of the Escherichia coli K5 capsule gene cluster: evidence for the roles of H-NS, BipA, and integration host factor in regulation of group 2 capsule gene clusters in pathogenic E. coli. J Bacteriol 182: 2741-2745.
103. St Michael, F., Szymanski, C.M., Li, J., Chan, K.H., Khieu, N.H., Larocque, S., etal. (2002) The structures of the lipooligosaccharide and capsule polysaccharide of Campylobacter jejuni genome sequenced strain NCTC 11168. Eur J Biochem 269: 5119-5136.
104. Salloway, S., Mermel, L.A., Seamans, M., Aspinall, G.O., Nam Shin, J.E., Kurjanczyk, L.A., and Penner, J.L. (1996) Miller-Fisher syndrome associated with Campylobacter jejuni bearing lipopolysaccharide molecules that mimic human ganglioside GD3. Infect Immun 64: 2945-2949.
105. 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.
106. Silver, R.P., Prior, K., Nsahlai, C., and Wright, L.F. (2001) ABC transporters and the export of capsular polysaccharides from gram-negative bacteria. Res Microbiol 152: 357-364.
107. van Sorge, N.M., Cole, J.N., Kuipers, K., Henningham, A., Aziz, R.K., Kasirer-Friede, A., etal. (2014) The classical lancefield antigen of group a Streptococcus is a virulence determinant with implications for vaccine design. Cell Host Microbe 15: 729-740.
108. Sternberg, M.J., Tamaddoni-Nezhad, A., Lesk, V.I., Kay, E., Hitchen, P.G., Cootes, A., etal. (2013) Gene Function Hypotheses for the Campylobacter jejuni Glycome Generated by a Logic-Based Approach. J Mol Biol 425: 186-197.
109. Stevens, M.P., Clarke, B.R., and Roberts, I.S. (1997) Regulation of the Escherichia coli K5 capsule gene cluster by transcription antitermination. Mol Microbiol 24: 1001-1012.
110. 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.
111. Szymanski, C.M., Burr, D.H., and Guerry, P. (2002) Campylobacter protein glycosylation affects host cell interactions. Infect Immun 70: 2242-2244.
112. Szymanski, C.M., Michael, F.S., Jarrell, H.C., Li, J., Gilbert, M., Larocque, S., etal. (2003) Detection of conserved N-linked glycans and phase-variable lipooligosaccharides and capsules from campylobacter cells by mass spectrometry and high resolution magic angle spinning NMR spectroscopy. J Biol Chem 278: 24509-24520.
113. Udayakumar, D., and Sanaullah, M. (2009) Campylobacter cholecystitis. Int J Med Sci 6: 374-375.
114. 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.
115. Vijayakumar, S., Merkx-Jacques, A., Ratnayake, D., Gryski, I., Obhi, R.K., Houle, S., etal. (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.
116. Vogel, U., Weinberger, A., Frank, R., Muller, A., Kohl, J., Atkinson, J.P., and Frosch, M. (1997) Complement factor C3 deposition and serum resistance in isogenic capsule and lipooligosaccharide sialic acid mutants of serogroup B Neisseria meningitidis. Infect Immun 65: 4022-4029.
117. Wassenaar, T.M., and Blaser, M.J. (1999) Pathophysiology of Campylobacter jejuni infections of humans. Microbes Infect 1: 1023-1033.
118. Wassenaar, T.M., Fry, B.N., and van der Zeijst, B.A. (1993) Genetic manipulation of Campylobacter: evaluation of natural transformation and electro-transformation. Gene 132: 131-135.
119. Wassenaar, T.M., Engelskirchen, M., Park, S., and Lastovica, A. (1997) Differential uptake and killing potential of Campylobacter jejuni by human peripheral monocytes/macrophages. Med Microbiol Immunol (Berl) 186: 139-144.
120. Westphal, O., and Jann, K. (1965) Bacterial lipopolysaccharide. Extraction with phenol-water and further applications of the procedure. Methods Carbohydr Chem 5: 83-91.
121. Whitfield, C. (2006) Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 75: 39-68.
122. Whitfield, C., and Roberts, I.S. (1999) Structure, assembly and regulation of expression of capsules in Escherichia coli. Mol Microbiol 31: 1307-1319.
123. Woodman, M.E., Worth, R.G., and Wooten, R.M. (2012) Capsule influences the deposition of critical complement C3 levels required for the killing of Burkholderia pseudomallei via NADPH-oxidase induction by human neutrophils. PLoS ONE 7: e52276.
124. Wosten, M.M., Boeve, M., Koot, M.G., van Nuenen, A.C., and van der Zeijst, B.A. (1998) Identification of Campylobacter jejuni promoter sequences. J Bacteriol 180: 594-599.
125. Yuki, N., Taki, T., Takahashi, M., Saito, K., Yoshino, H., Tai, T., etal. (1994) Molecular mimicry between GQ1b ganglioside and lipopolysaccharides of Campylobacter jejuni isolated from patients with Fisher's syndrome. Ann Neurol 36: 791-793.