Assessment of glycan interactions of clinical and avian isolates of Campylobacter jejuni

BMC Microbiology

Victoria Korolik¹  Joe Tiralongo¹  Lauren E Hartley-Tassell¹  Greg Tram¹  Christopher J Day¹ 

[1] Institute for Glycomics, G26, Griffith University Gold Coast Campus, Queensland 4222, Australia

关键词: Glycoconjugates;    Glycan array;    Host-bacterial interactions;   

Others  :  1142892
DOI  :  10.1186/1471-2180-13-228

 received in 2013-07-29, accepted in 2013-09-27,  发布年份 2013

【 摘 要 】

Background

Campylobacter jejuni strain 11168 was demonstrated to have a broad specificity for eukaryotic surface glycosylation using glycan array analysis. The initial screen indicated that sialic acid and mannose are important binding partners after environmental stress, while galactose and fucose structures are likely to be involved in persistent infection.

Results

In this broader study, five additional human/clinical isolates and six chicken isolates were fully assessed to determine their glycan binding capacity using an extended glycan array. C. jejuni 11168 was rescreened here due to the presence of glycoaminoglycan (GAG) and other structures that were not available on our previous glycan array. The current array analysis of additional C. jejuni strains confirmed the growth condition dependent differences in glycan binding that was previously observed for C. jejuni 11168. We noted strain to strain variations, particularly for the human isolates C. jejuni 520 and 81116 and the chicken isolate C. jejuni 331, with the majority of differences observed in galactose, mannose and GAG binding. Chicken isolates were found to bind to a broader range of glycans compared to the human isolates, recognising branched mannose and carageenan (red seaweed) glycans. Glycan array data was confirmed using cell-based lectin inhibition assays with the fucose (UEA-I) and mannose (ConA) binding lectins.

Conclusions

This study confirms that all C. jejuni strains tested bind to a broad range of glycans, with the majority of strains (all except 81116) altering recognition of sialic acid and mannose after environmental stress. Galactose and fucose structures were bound best by all strains when C. jejuni was grown under host like conditions confirming the likelihood of these structures being involved in persistent infection.

【 授权许可】

   
2013 Day et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Smith DC, Lord JM, Roberts LM, Johannes L: Glycosphingolipids as toxin receptors. Semin Cell Dev Biol 2004, 15(4):397-408.
• [2]Lehmann F, Tiralongo E, Tiralongo J: Sialic acid-specific lectins: occurrence, specificity and function. Cell Mol Life Sci 2006, 63(12):1331-1354.
• [3]Day CJ, Tiralongo J, Hartnell RD, Logue CA, Wilson JC, von Itzstein M, Korolik V: Differential carbohydrate recognition by Campylobacter jejuni strain 11168: influences of temperature and growth conditions. PLoS One 2009, 4(3):e4927.
• [4]Day CJ, Semchenko EA, Korolik V: Glycoconjugates play a key role in campylobacter jejuni infection: interactions between host and pathogen. Front Cell Infect Microbiol 2012, 2:9.
• [5]Newburg DS, Ruiz-Palacios GM, Morrow AL: Human milk glycans protect infants against enteric pathogens. Annu Rev Nutr 2005, 25:37-58.
• [6]Morrow AL, Ruiz-Palacios GM, Jiang X, Newburg DS: Human-milk glycans that inhibit pathogen binding protect breast-feeding infants against infectious diarrhea. J Nutr 2005, 135(5):1304-1307.
• [7]Yamaoka Y: Roles of Helicobacter pylori BabA in gastroduodenal pathogenesis. World J Gastroenterol 2008, 14(27):4265-4272.
• [8]Juge N: Microbial adhesins to gastrointestinal mucus. Trends Microbiol 2012, 20(1):30-39.
• [9]Mahdavi J, Sonden B, Hurtig M, Olfat FO, Forsberg L, Roche N, Angstrom J, Larsson T, Teneberg S, Karlsson KA, et al.: Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 2002, 297(5581):573-578.
• [10]McAuley JL, Linden SK, Png CW, King RM, Pennington HL, Gendler SJ, Florin TH, Hill GR, Korolik V, McGuckin MA: MUC1 cell surface mucin is a critical element of the mucosal barrier to infection. J Clin Invest 2007, 117(8):2313-2324.
• [11]Varki A: Multiple changes in sialic acid biology during human evolution. Glycoconj J 2009, 26(3):231-245.
• [12]Le Pendu J: Histo-blood group antigen and human milk oligosaccharides: genetic polymorphism and risk of infectious diseases. Adv Exp Med Biol 2004, 554:135-143.
• [13]Suzuki N, Laskowski M Jr, Lee YC: Phylogenetic expression of Galalpha1-4Gal on avian glycoproteins: glycan differentiation inscribed in the early history of modern birds. Proc Natl Acad Sci USA 2004, 101(24):9023-9028.
• [14]Galili U, Clark MR, Shohet SB, Buehler J, Macher BA: Evolutionary relationship between the natural anti-Gal antibody and the Gal alpha 1––3Gal epitope in primates. Proc Natl Acad Sci USA 1987, 84(5):1369-1373.
• [15]Yang Z, Bergstrom J, Karlsson KA: Glycoproteins with Gal alpha 4Gal are absent from human erythrocyte membranes, indicating that glycolipids are the sole carriers of blood group P activities. J Biol Chem 1994, 269(20):14620-14624.
• [16]Sandrin MS, McKenzie IF: Gal alpha (1,3)Gal, the major xenoantigen(s) recognised in pigs by human natural antibodies. Immunol Rev 1994, 141:169-190.
• [17]Garratty G: Blood group antigens as tumor markers, parasitic/bacterial/viral receptors, and their association with immunologically important proteins. Immunol Invest 1995, 24(1–2):213-232.
• [18]Houliston RS, Vinogradov E, Dzieciatkowska M, Li J, St Michael F, Karwaski MF, Brochu D, Jarrell HC, Parker CT, Yuki N, et al.: Lipooligosaccharide of Campylobacter jejuni: similarity with multiple types of mammalian glycans beyond gangliosides. J Biol Chem 2011, 286(14):12361-12370.
• [19]Hald B, Skovgard H, Pedersen K, Bunkenborg H: Influxed insects as vectors for Campylobacter jejuni and Campylobacter coli in Danish broiler houses. Poult Sci 2008, 87(7):1428-1434.
• [20]Schallenberg M, Bremer PJ, Henkel S, Launhardt A, Burns CW: Survival of Campylobacter jejuni in water: effect of grazing by the freshwater crustacean Daphnia carinata (Cladocera). Appl Environ Microbiol 2005, 71(9):5085-5088.
• [21]Holden KM, Gilbert M, Coloe PJ, Li J, Fry BN: The role of WlaRG, WlaTB and WlaTC in lipooligosaccharide synthesis by Campylobacter jejuni strain 81116. Microb Pathog 2012, 52(6):344-352.
• [22]St Michael F, Szymanski CM, Li J, Chan KH, Khieu NH, Larocque S, Wakarchuk WW, Brisson JR, Monteiro MA: The structures of the lipooligosaccharide and capsule polysaccharide of Campylobacter jejuni genome sequenced strain NCTC 11168. Eur J Biochem 2002, 269(21):5119-5136.
• [23]Semchenko EA, Day CJ, Wilson JC, Grice ID, Moran AP, Korolik V: Temperature-dependent phenotypic variation of Campylobacter jejuni lipooligosaccharides. BMC Microbiol 2010, 10:305. BioMed Central Full Text
• [24]Semchenko EA, Day CJ, Moutin M, Wilson JC, Tiralongo J, Korolik V: Structural heterogeneity of terminal glycans in Campylobacter jejuni lipooligosaccharides. PLoS One 2012, 7(7):e40920.
• [25]Yamada KM, Kennedy DW, Kimata K, Pratt RM: Characterization of fibronectin interactions with glycosaminoglycans and identification of active proteolytic fragments. J Biol Chem 1980, 255(13):6055-6063.
• [26]Konkel ME, Garvis SG, Tipton SL, Anderson DE Jr, Cieplak W Jr: Identification and molecular cloning of a gene encoding a fibronectin-binding protein (CadF) from Campylobacter jejuni. Mol Microbiol 1997, 24(5):953-963.
• [27]Chung CY, Erickson HP: Glycosaminoglycans modulate fibronectin matrix assembly and are essential for matrix incorporation of tenascin-C. J Cell Sci 1997, 110(Pt 12):1413-1419.
• [28]Calderon-Gomez LI, Hartley LE, McCormack A, Ringoir DD, Korolik V: Potential use of characterised hyper-colonising strain(s) of Campylobacter jejuni to reduce circulation of environmental strains in commercial poultry. Vet Microbiol 2009, 134(3–4):353-361.
• [29]Korolik V, Alderton MR, Smith SC, Chang J, Coloe PJ: Isolation and molecular analysis of colonising and non-colonising strains of Campylobacter jejuni and Campylobacter coli following experimental infection of young chickens. Vet Microbiol 1998, 60(2–4):239-249.
• [30]Hartley-Tassell LE, Shewell LK, Day CJ, Wilson JC, Sandhu R, Ketley JM, Korolik V: Identification and characterization of the aspartate chemosensory receptor of Campylobacter jejuni. Mol Microbiol 2010, 75(3):710-730.
• [31]Arndt NX, Tiralongo J, Madge PD, von Itzstein M, Day CJ: Differential carbohydrate binding and cell surface glycosylation of human cancer cell lines. J Cell Biochem 2011, 112(9):2230-2240.