Campylobacter jejuni lipooligosaccharide sialylation, phosphorylation, and amide/ester linkage modifications fine-tune human toll-like receptor 4 activation

Journal of Biological Chemistry

Volumn 288, Issue 27, 2013, Pages 19661-19672

  Stephenson, Holly N ^a,d   John, Constance M ^b   Naz, Neveda ^c   Gundogdu, Ozan ^c   Dorrell, Nick ^c   Wren, Brendan W ^c   Jarvis, Gary A ^b   Bajaj Elliott, Mona ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c LONDON SCHOOL OF HYGIENE AND TROPICAL MEDICINE   (United Kingdom)

^d MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 ,3-DIAMINO-2 ,3-DIDEOXY-D-GLUCOSE; CAMPYLOBACTER JEJUNI; INFLAMMATORY RESPONSE; LIPOOLIGOSACCHARIDES; STRUCTURAL COMPONENT; STRUCTURAL VARIATIONS; TOLL-LIKE RECEPTOR 4; TOLL-LIKE RECEPTORS;

AGRICULTURE; BODY FLUIDS; CHEMICAL ACTIVATION; GLYCOSYLATION; PHOSPHORYLATION; STRAIN;

BACTERIA;

BACTERIAL PROTEIN; CAMPYLOBACTER JEJUNI LIPOOLIGOSACCHARIDE; CYTOKINE; GLUCOSAMINE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; CELL ACTIVATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME SYNTHESIS; HUMAN; HUMAN CELL; INFLAMMATION; INNATE IMMUNITY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MONOCYTE; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SIALYLATION; STRUCTURE ACTIVITY RELATION;

CAMPYLOBACTER; INNATE IMMUNITY; LIPOPOLYSACCHARIDE (LPS); MONOCYTES; TOLL-LIKE RECEPTORS (TLR);

CAMPYLOBACTER JEJUNI; CARBOHYDRATE CONFORMATION; CELL LINE, TUMOR; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; MONOCYTES; PHOSPHORYLATION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TOLL-LIKE RECEPTOR 4;

EID: 84880074886     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.468298     Document Type: Article

References (42)

1. Allos, B. M. (2001) Campylobacter jejuni infections: update on emerging issues and trends. Clin. Infect. Dis. 32, 1201-1206
2. Gardner, T. J., Fitzgerald, C., Xavier, C., Klein, R., Pruckler, J., Stroika, S., and McLaughlin, J. B. (2011) Outbreak of campylobacteriosis associated with consumption of raw peas. Clin. Infect. Dis. 53, 26-32
3. Kemp, R., Leatherbarrow, A. J., Williams, N. J., Hart, C. A., Clough, H. E., Turner, J., Wright, E. J., and French, N. P. (2005) Prevalence and genetic diversity of Campylobacter spp. in environmental water samples from a 100-square-kilometer predominantly dairy farming area. Appl. Environ. Microbiol. 71, 1876-1882
4. Black, R. E., Levine, M. M., Clements, M. L., Hughes, T. P., and Blaser, M. J. (1988) Experimental Campylobacter jejuni infection in humans. J. Infect. Dis. 157, 472-479
5. de Zoete, M. R., Keestra, A. M., Roszczenko, P., and van Putten, J. P. (2010) Activation of human and chicken toll-like receptors by Campylobacter spp. Infect. Immun. 78, 1229-1238
6. Rathinam, V. A., Appledorn, D. M., Hoag, K. A., Amalfitano, A., and Mansfield, L. S. (2009) Campylobacter jejuni-induced activation of dendritic cells involves cooperative signaling through Toll-like receptor 4 (TLR4)-MyD88 and TLR4-TRIF axes. Infect. Immun. 77, 2499-2507
7. Andersen-Nissen, E., Smith, K. D., Strobe, K. L., Barrett, S. L., Cookson, B. T., Logan, S. M., and Aderem, A. (2005) Evasion of Toll-like receptor 5 by flagellated bacteria. Proc. Natl. Acad. Sci. U.S.A. 102, 9247-9252
8. Hu, L., Bray, M. D., Osorio, M., and Kopecko, D. J. (2006) Campylobacter jejuni induces maturation and cytokine production in human dendritic cells. Infect. Immun. 74, 2697-2705
9. Kuijf, M. L., Samsom, J. N., van Rijs, W., Bax, M., Huizinga, R., Heikema, A. P., van Doorn, P. A., van Belkum, A., van Kooyk, Y., Burgers, P. C., Luider, T. M., Endtz, H. P., Nieuwenhuis, E. E., and Jacobs, B. C. (2010) TLR4-mediated sensing of Campylobacter jejuni by dendritic cells is determined by sialylation. J. Immunol. 185, 748-755
10. Lepper, P. M., Triantafilou, M., Schumann, C., Schneider, E. M., and Triantafilou, K. (2005) Lipopolysaccharides from Helicobacter pylori can act as antagonists for Toll-like receptor 4. Cell. Microbiol. 7, 519-528
11. Mortensen, N. P., Kuijf, M. L., Ang, C. W., Schiellerup, P., Krogfelt, K. A., Jacobs, B. C., van Belkum, A., Endtz, H. P., and Bergman, M. P. (2009) Sialylation of Campylobacter jejuni lipo-oligosaccharides is associated with severe gastro-enteritis and reactive arthritis. Microbes Infect. 11, 988-994
12. Park, B. S., Song, D. H., Kim, H. M., Choi, B. S., Lee, H., and Lee, J. O. (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458, 1191-1195
13. Moran, A. P., Zähringer, U., Seydel, U., Scholz, D., Stütz, P., and Rietschel, E. T. (1991) Structural analysis of the lipidAcomponent of Campylobacter jejuni CCUG 10936 (serotype O: 2) lipopolysaccharide. Description of a lipid A containing a hybrid backbone of 2-amino-2-deoxy-D-glucose and 2,3-diamino-2,3-dideoxy-D-glucose. Eur. J. Biochem. 198, 459-469
14. Moran, A. P., Rietschel, E. T., Kosunen, T. U., and Zähringer, U. (1991) Chemical characterization of Campylobacter jejuni lipopolysaccharides containing N-acetylneuraminic acid and 2,3-diamino-2,3-dideoxy-D-glucose. J. Bacteriol. 173, 618-626
15. Parker, C. T., Horn, S. T., Gilbert, M., Miller, W. G., Woodward, D. L., and Mandrell, R. E. (2005) Comparison of Campylobacter jejuni lipooligosaccharide biosynthesis loci from a variety of sources. J. Clin. Microbiol. 43, 2771-2781
16. Parker, C. T., Gilbert, M., Yuki, N., Endtz, H. P., and Mandrell, R. E. (2008) Characterization of lipooligosaccharide-biosynthetic loci of Campylobacter jejuni reveals new lipooligosaccharide classes: evidence of mosaic organizations. J. Bacteriol. 190, 5681-5689
17. Godschalk, P. C., Heikema, A. P., Gilbert, M., Komagamine, T., Ang, C. W., Glerum, J., Brochu, D., Li, J., Yuki, N., Jacobs, B. C., van Belkum, A., and Endtz, H. P. (2004) The crucial role of Campylobacter jejuni genes in anti-ganglioside antibody induction in Guillain-Barré syndrome. J. Clin. Investig. 114, 1659-1665
18. van Mourik, A., Steeghs, L., van Laar, J., Meiring, H. D., Hamstra, H. J., van Putten, J. P., and Wösten, M. M. (2010) Altered linkage of hydroxyacyl chains in lipid A of Campylobacter jejuni reduces TLR4 activation and antimicrobial resistance. J. Biol. Chem. 285, 15828-15836
19. Szymanski, C. M., Michael, F. S., Jarrell, H. C., Li, J., Gilbert, M., Larocque, S., Vinogradov, E., and Brisson, J. R. (2003) Detection of conserved Nlinked 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
20. Cullen, T. W., O'Brien, J. P., Hendrixson, D. R., Giles, D. K., Hobb, R. I., Thompson, S. A., Brodbelt, J. S., and Trent, M. S. (2013) EptC of Campylobacter jejuni mediates phenotypes involved in host interactions and virulence. Infect. Immun. 81, 430-440
21. Champion, O. L., Gaunt, M. W., Gundogdu, O., Elmi, A., Witney, A. A., Hinds, J., Dorrell, N., and Wren, B. W. (2005) Comparative phylogenomics of the food-borne pathogen Campylobacter jejuni reveals genetic markers predictive of infection source. Proc. Natl. Acad. Sci. U.S.A. 102, 16043-16048
22. Hepworth, P. J., Ashelford, K. E., Hinds, J., Gould, K. A., Witney, A. A., Williams, N. J., Leatherbarrow, H., French, N. P., Birtles, R. J., Mendonca, C., Dorrell, N., Wren, B. W., Wigley, P., Hall, N., and Winstanley, C. (2011) Genomic variations define divergence of water/wildlife-associated Campylobacter jejuni niche specialists from common clonal complexes. Environ. Microbiol. 13, 1549-1560
23. Gundogdu, O., Mills, D. C., Elmi, A., Martin, M. J., Wren, B. W., and Dorrell, N. (2011) The Campylobacter jejuni transcriptional regulator Cj1556 plays a role in the oxidative and aerobic stress response and is important for bacterial survival in vivo. J. Bacteriol. 193, 4238-4249
24. John, C. M., Liu, M., and Jarvis, G. A. (2009) Natural phosphoryl and acyl variants of lipid A from Neisseria meningitidis strain 89I differentially induce tumor necrosis factor-α in human monocytes. J. Biol. Chem. 284, 21515-21525
25. John, C. M., Liu, M., and Jarvis, G. A. (2009) Profiles of structural heterogeneity in native lipooligosaccharides of Neisseria and cytokine induction. J. Lipid Res. 50, 424-438
26. Domon, B. C., and Costello, C. E. (1988) A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconj. J. 5, 397-409
27. Dzieciatkowska, M., Brochu, D., van Belkum, A., Heikema, A. P., Yuki, N., Houliston, R. S., Richards, J. C., Gilbert, M., and Li, J. (2007) Mass spectrometric analysis of intact lipooligosaccharide: direct evidence for Oacetylated sialic acids and discovery of O-linked glycine expressed by Campylobacter jejuni. Biochemistry 46, 14704-14714
28. Phillips, N. J., Apicella, M. A., Griffiss, J. M., and Gibson, B. W. (1993) Structural studies of the lipooligosaccharides from Haemophilus influenzae type b strain A2. Biochemistry 32, 2003-2012
29. Poltorak, A., He, X., Smirnova, I., Liu, M. Y., Van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi-Castagnoli, P., Layton, B., and Beutler, B. (1998) Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 2085-2088
30. Beutler, B. (1990) TNF in pathophysiology: biosynthetic regulation. J. Invest. Dermatol. 95, 81S-84S
31. Liu, M., John, C. M., and Jarvis, G. A. (2010) Phosphoryl moieties of lipidA from Neisseria meningitidis and N. gonorrhoeae lipooligosaccharides play an important role in activation of both MyD88- and TRIF-dependent TLR4-MD-2 signaling pathways. J. Immunol. 185, 6974-6984
32. Lock, K., Zhang, J., Lu, J., Lee, S. H., and Crocker, P. R. (2004) Expression of CD33-related siglecs on human mononuclear phagocytes, monocyte-derived dendritic cells and plasmacytoid dendritic cells. Immunobiology 209, 199-207
33. Javed, M. A., Cawthraw, S. A., Baig, A., Li, J., McNally, A., Oldfield, N. J., Newell, D. G., and Manning, G. (2012) Cj1136 is required for lipooligosaccharide biosynthesis, hyperinvasion, and chick colonization by Campylobacter jejuni. Infect. Immun. 80, 2361-2370
34. Varki, A., and Gagneux, P. (2012) Multifarious roles of sialic acids in immunity. Ann. N.Y. Acad. Sci. 1253, 16-36
35. Louwen, R., Heikema, A., van Belkum, A., Ott, A., Gilbert, M., Ang, W., Endtz, H. P., Bergman, M. P., and Nieuwenhuis, E. E. (2008) The sialylated lipooligosaccharide outer core in Campylobacter jejuni is an important determinant for epithelial cell invasion. Infect. Immun. 76, 4431-4438
36. Jarvis, G. A., and Vedros, N. A. (1987) Sialic acid of group B Neisseria meningitidis regulates alternative complement pathway activation. Infect. Immun. 55, 174-180
37. Cullen, T. W., Madsen, J. A., Ivanov, P. L., Brodbelt, J. S., and Trent, M. S. (2012) Characterization of unique modification of flagellar rod protein FlgG by Campylobacter jejuni lipid A phosphoethanolamine transferase, linking bacterial locomotion and antimicrobial peptide resistance. J. Biol. Chem. 287, 3326-3336
38. Scott, N. E., Nothaft, H., Edwards, A. V., Labbate, M., Djordjevic, S. P., Larsen, M. R., Szymanski, C. M., and Cordwell, S. J. (2012) Modification of the Campylobacter jejuni N-linked glycan by EptC protein-mediated addition of phosphoethanolamine. J. Biol. Chem. 287, 29384-29396
39. Cekic, C., Casella, C. R., Eaves, C. A., Matsuzawa, A., Ichijo, H., and Mitchell, T. C. (2009) Selective activation of the p38 MAPK pathway by synthetic monophosphoryl lipid A. J. Biol. Chem. 284, 31982-31991
40. Mata-Haro, V., Cekic, C., Martin, M., Chilton, P. M., Casella, C. R., and Mitchell, T. C. (2007) The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 316, 1628-1632
41. Cullen, T. W., Giles, D. K., Wolf, L. N., Ecobichon, C., Boneca, I. G., and Trent, M. S. (2011) Helicobacter pylori versus the host: remodeling of the bacterial outer membrane is required for survival in the gastric mucosa. PLoS Pathog. 7, e1002454
42. John, C. M., Liu, M., Phillips, N. J., Yang, Z., Funk, C. R., Zimmerman, L. I., Griffiss, J. M., Stein, D. C., and Jarvis, G. A. (2012) Lack of lipid A pyrophosphorylation and functional lptA reduces inflammation by Neisseria commensals. Infect. Immun. 80, 4014-4026