Identification of O-glycan structures from chicken intestinal mucins provides insight into Campylobactor jejuni pathogenicity

Molecular and Cellular Proteomics

Volumn 14, Issue 6, 2015, Pages 1464-1477

  Struwe, Weston B ^a,d   Gough, Ronan ^b   Gallagher, Mary E ^b   Kenny, Diarmuid T ^c   Carrington, Stephen D ^b   Karlsson, Niclas G ^c   Rudd, Pauline M ^b,c  

^a NATIONAL INSTITUTE FOR BIOPROCESSING RESEARCH AND TRAINING   (Ireland)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; FUCOSE; GALACTOSE; GLUCOSE; GLYCAN; MANNOSE; MUCIN; N ACETYLNEURAMINIC ACID; N GLYCOLOYLNEURAMINIC ACID; SULFATE; POLYSACCHARIDE;

ANIMAL TISSUE; ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BINDING AFFINITY; CAMPYLOBACTER JEJUNI; CARBOHYDRATE ANALYSIS; CECUM; CONTROLLED STUDY; HUMAN; HUMAN CELL; LARGE INTESTINE; LIQUID CHROMATOGRAPHY; MALE; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN PURIFICATION; PROTEIN STRUCTURE; SMALL INTESTINE; SPECIES INVASION; STRUCTURE ANALYSIS; SULFATION; ANIMAL; CHEMISTRY; CHICKEN; FEMALE; PATHOGENICITY;

CAMPYLOBACTER JEJUNI; GALLUS GALLUS; NEGIBACTERIA;

ANIMALS; CAMPYLOBACTER JEJUNI; CHICKENS; FEMALE; HUMANS; INTESTINE, LARGE; INTESTINE, SMALL; MUCINS; POLYSACCHARIDES;

EID: 84930455882     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M114.044867     Document Type: Article

References (38)

1. Janssen, R., Krogfelt, K. A., Cawthraw, S. A., van Pelt, W., Wagenaar, J. A., and Owen, R. J. (2008) Host-pathogen interactions in Campylobacter infections: The host perspective. Clin. Microbiol. Rev. 21, 505-518
2. Young, K. T., Davis, L. M., and Dirita, V. J. (2007) Campylobacter jejuni: Molecular biology and pathogenesis. Nat. Rev. Microbiol. 5, 665-679
3. (FSIS), F. S. a. I. S. (1996) Nationwide broiler chicken microbiological baseline data collection program (1994-1995). United States Department of Agriculture, Washington, DC
4. Alemka, A., Whelan, S., Gough, R., Clyne, M., Gallagher, M. E., Carrington, S. D., and Bourke, B. (2010) Purified chicken intestinal mucin attenuates Campylobacter jejuni pathogenicity in vitro. J. Med. Microbiol. 59, 898-903
5. Johansson, M. E., Phillipson, M., Petersson, J., Velcich, A., Holm, L., and Hansson, G. C. (2008) The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl. Acad. Sci. U.S.A. 105, 15064-15069
6. McGuckin, M. A., Linden, S. K., Sutton, P., and Florin, T. H. Mucin dynamics and enteric pathogens. Nat. Rev. Microbiol. 9, 265-278
7. Day, C. J., Tiralongo, J., Hartnell, R. D., Logue, C. A., Wilson, J. C., von Itzstein, M., and Korolik, V. (2009) Differential carbohydrate recognition by Campylobacter jejuni strain 11168: Influences of temperature and growth conditions. PloS One 4, e4927
8. Hugdahl, M. B., Beery, J. T., and Doyle, M. P. (1988) Chemotactic behavior of Campylobacter jejuni. Infect. Immun. 56, 1560-1566
9. Lindén, S., Nordman, H., Hedenbro, J., Hurtig, M., Boren, T., and Carlstedt, I. (2002) Strain- and blood group-dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms. Gastroenterology 123, 1923-1930
10. Mahdavi, J., Sonden, B., Hurtig, M., Olfat, F. O., Forsberg, L., Roche, N., Angstrom, J., Larsson, T., Teneberg, S., Karlsson, K. A., Altraja, S., Wadström, T., Kersulyte, D., Berg, D. E., Dubois, A., Petersson, C., Magnusson, K. E., Norberg, T., Lindh, F., Lundskog, B. B., Arnqvist, A., Hammarström, L., and Boren, T. (2002) Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 297, 573-578
11. McAuley, J. L., Linden, S. K., Png, C. W., King, R. M., Pennington, H. L., Gendler, S. J., Florin, T. H., Hill, G. R., Korolik, V., and McGuckin, M. A. (2007) MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J. Clin. Invest. 117, 2313-2324
12. Ruiz-Palacios, G. M., Cervantes, L. E., Ramos, P., Chavez-Munguia, B., and Newburg, D. S. (2003) Campylobacter jejuni binds intestinal H(O) antigen (Fuc alpha 1, 2Gal beta 1, 4GlcNAc), and fucosyloligosaccharides of human milk inhibit its binding and infection. J. Biol. Chem. 278, 14112-14120
13. Stahl, M., Friis, L. M., Nothaft, H., Liu, X., Li, J., Szymanski, C. M., and Stintzi, A. L-fucose utilization provides Campylobacter jejuni with a competitive advantage. Proc. Natl. Acad. Sci. U.S.A. 108, 7194-7199
14. Van der Sluis, M., De Koning, B. A., De Bruijn, A. C., Velcich, A., Meijerink, J. P., Van Goudoever, J. B., Büller, H. A., Dekker, J., Van Seuningen, I., Renes, I. B., and Einerhand, A. W. (2006) Muc2-deficient mice spontaneously develop colitis, indicating that MUC2 is critical for colonic protection. Gastroenterology 131, 117-129
15. Flanagan, R. C., Neal-McKinney, J. M., Dhillon, A. S., Miller, W. G., and Konkel, M. E. (2009) Examination of Campylobacter jejuni putative adhesions leads to the identification of a new protein, designated FlpA, required for chicken colonization. Infect. Immun. 77, 2399-2407
16. Russell, R. G., and Blake, D. C., Jr. (1994) Cell association and invasion of Caco-2 cells by Campylobacter jejuni. Infect. Immun. 62, 3773-3779
17. Davies, J. R., and Carlstedt, I. (2000) Isolation of large gel-forming mucins. Methods Mol. Biol. 125, 3-13
18. Tierney, J. B., Matthews, E., Carrington, S. D., and Mulcahy, G. (2007) Interaction of Eimeria tenella with intestinal mucin in vitro. J. Parasitol. 93, 634-638
19. Schulz, B. L., Packer, N. H., and Karlsson, N. G. (2002) Small-scale analysis of O-linked oligosaccharides from glycoproteins and mucins separated by gel electrophoresis. Anal. Chem. 74, 6088-6097
20. Karlsson, N. G., Schulz, B. L., and Packer, N. H. (2004) Structural determination of neutral O-linked oligosaccharide alditols by negative ion LCelectrospray- MSn. J. Am. Soc. Mass Spectrom. 15, 659-672
21. Hayes, C. A., Karlsson, N. G., Struwe, W. B., Lisacek, F., Rudd, P. M., Packer, N. H., and Campbell, M. P. (2011) UniCarb-DB: Z database resource for glycomic discovery. Bioinformatics 27, 1343-1344
22. Tareke, E., Rydberg, P., Karlsson, P., Eriksson, S., and Töornqvist, M. (2002) Analysis of acrylamide, a carcinogen formed in heated foodstuffs. J. Agri. Food Chem. 50, 4998-5006
23. Damerell, D., Ceroni, A., Maass, K., Ranzinger, R., Dell, A., and Haslam, S. M. (2012) The GlycanBuilder and GlycoWorkbench glycoinformatics tools: updates and new developments. Biol. Chem. 393, 1357-1362
24. Domon, B., and Costello, C. E. (1988) A systematic nomenclature for carbohydrate fragmentations in FAB-MS/MS spectra of glycoconjugates. Glycoconjugate J. 5, 397-409
25. Harvey, D. J., Merry, A. H., Royle, L., Campbell, M. P., Dwek, R. A., and Rudd, P. M. (2009) Proposal for a standard system for drawing structural diagrams of N- and O-linked carbohydrates and related compounds. Proteomics 9, 3796-3801
26. Doohan, R. A., Hayes, C. A., Harhen, B., and Karlsson, N. G. (2011) Negative ion CID fragmentation of O-linked oligosaccharide aldoses-charge induced and charge remote fragmentation. J. Am. Soc. Mass Spectrom.22, 1052-1062
27. Schauer, R., Srinivasan, G. V., Coddeville, B., Zanetta, J. P., and Guérardel, Y. (2009) Low incidence of N-glycolylneuraminic acid in birds and reptiles and its absence in the platypus. Carbohydrate Res. 344, 1494-1500
28. Robbe, C., Capon, C., Coddeville, B., and Michalski, J. C. (2004) Structural diversity and specific distribution of O-glycans in normal human mucins along the intestinal tract. Biochem. J. 384, 307-316
29. Larsson, J. M., Karlsson, H., Sjövall, H., and Hansson, G. C. (2009) A complex, but uniform O-glycosylation of the human MUC2 mucin from colonic biopsies analyzed by nanoLC/MSn. Glycobiology 19, 756-766
30. Kamisago, S., Iwamori, M., Tai, T., Mitamura, K., Yazaki, Y., and Sugano, K. (1996) Role of sulfatides in adhesion of Helicobacter pylori to gastric cancer cells. Infect Immun 64, 624-628
31. Veerman, E. C., Bank, C. M., Namavar, F., Appelmelk, B. J., Bolscher, J. G., and Nieuw Amerongen, A. V. (1997) Sulfated glycans on oral mucin as receptors for Helicobacter pylori. Glycobiology 7, 737-743
32. Dawson, P. A., Huxley, S., Gardiner, B., Tran, T., McAuley, J. L., Grimmond, S., McGuckin, M. A., and Markovich, D. (2009) Reduced mucin sulfonation and impaired intestinal barrier function in the hyposulfataemic NaS1 null mouse. Gut 58, 910-919
33. Sjogren, J., Struwe, W. B., Cosgrave, E., Rudd, P. M., Stervander, M., Allhorn, M., Hollands, A., Nizet, V., and Collin, M. (2013) EndoS2 is a unique and conserved enzyme of serotype M49 group A Streptococcus that hydrolyzes N-linked glycans on IgG and alpha1-acid glycoprotein. Biochem. J. 455, 107-118
34. Tu, Q. V., McGuckin, M. A., and Mendz, G. L. (2008) Campylobacter jejuni response to human mucin MUC2: Modulation of colonization and pathogenicity determinants. J .Med. Microbiol. 57, 795-802
35. Fujii, Y., Higashi, H., Ikuta, K., Kato, S., and Naiki, M. (1982) Specificities of human heterophilic Hanganutziu and Deicher (H-D) antibodies and avian antisera against H-D antigen-active glycosphingolipids. Mol. Immun. 19, 87-94
36. Tangvoranuntakul, P., Gagneux, P., Diaz, S., Bardor, M., Varki, N., Varki, A., and Muchmore, E. (2003) Human uptake and incorporation of an immunogenic nonhuman dietary sialic acid. Proc. Natl. Acad. Sci. U.S.A. 100, 12045-12050
37. Fernandez, F., Sharma, R., Hinton, M., and Bedford, M. R. (2000) Diet influences the colonisation of Campylobacter jejuni and distribution of mucin carbohydrates in the chick intestinal tract. Cell Mol. Life Sci. 57, 1793-1801
38. Sturkie, P. D., and Whittow, G. C. (2000) Sturkie's Avian Physiology, 5th ed., Academic Press, San Diego