Helicobacter pylori binding to new glycans based on N-acetyllactosamine

Glycobiology

Volumn 19, Issue 4, 2009, Pages 399-407

  Miller Podraza, Halina ^a   Weikkolainen, Krista ^b   Larsson, Thomas ^a   Linde, Petra ^a   Helin, Jari ^c   Natunen, Jari ^c   Karlsson, Karl Anders ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b UNIVERSITY OF HELSINKI   (Finland)

^c GLYKOS FINLAND LTD   (Finland)

Author keywords

Binding; Epitope; Helicobacter pylori; Neolacto; Structure

Indexed keywords

CARBOHYDRATE; EPITOPE; GLYCAN DERIVATIVE; N ACETYLGLUCOSAMINE; N ACETYLLACTOSAMINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIUM ADHERENCE; BINDING AFFINITY; CELL INTERACTION; CONTROLLED STUDY; HELICOBACTER PYLORI; HOST PATHOGEN INTERACTION; MOLECULAR RECOGNITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE;

ACETYLGLUCOSAMINE; BACTERIAL ADHESION; EPITOPES; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI;

EID: 62449141068     PISSN: 09596658     EISSN: 14602423     Source Type: Journal    
DOI: 10.1093/glycob/cwn150     Document Type: Article

References (64)

1. Abul Milh M, Barnett Foster D, Lindgwood CA. 2001. In vitro binding of Helicobacter pylori to monohexosylceramides. Glycoconj J. 18:253-260.
2. Ångström J, Teneberg S, Abul Milh M, Larsson T, Leonardsson I, Olsson B-M, Ölwegård-Halvarsson M, Danielsson D, Näslund I, Ljungh Å, et al. 1998. The lactosylceramide binding specificity of Helicobacter pylori. Glycobiology. 8:297-309.
3. Ascencio F, Fransson LA, Wadström T. 1993. Affinity of the gastric pathogen Helicobacter pylori for the N-sulphated glycosaminoglycan heparan sulfate. J Med Microbiol. 38:240-244.
4. Blaser MJ. 1992. Hypotheses on the pathogenesis and natural history of Helicobacter pylori-induced inflammation. Gastroenterology 102:720-727.
5. Blumberg K, Liniere F, Pustilnik L, Bush CA. 1982. Fractionation of oligosaccharides containing N-acetyl amino sugars by reverse-phase high-pressure liquid chromatography. Anal Biochem. 119:407-412.
6. Borén T, Falk P, Roth K-A, Normark S. 1993. Attachment of Helicobacter pylori to human gastric epithelium is mediated by blood group antigens. Science. 262:1892-1895.
7. Brew K, Vanaman TC, Hill RL. 1968. The role of alpha-lactalbumin and the A protein in lactose synthetase: A unique mechanism for the control of a biological reaction. Proc Natl Acad Sci USA. 59:491-497.
8. Bytzer P. 2005. Treatment of Helicobacter pylori. Helicobacter. 10(Suppl S):40-46.
9. Chaturvedi G, Tewari R, Mrigank N, Agnihotri N, Vishwakarma RA, Ganguly NK. 2001. Inhibition of Helicobacter pylori adherence by a peptide derived from neuraminyl lactose binding adhesion. Mol Cell Biochem 228:83-89.
10. Chou DK, Schachner M, Jungalwala FB. 2002. HNK-1 sulfotransferase null mice express glucuronyl glycoconjugates and show normal cerebellar granule neuron migration in vivo and in vitro. J Neurochem. 82:1239-1251
11. Defaye J, Gadelle A, Pedersen C. 1989. Hydrogen fluoride catalyzed formation of glycosides. Preparation of methyl 2-acetamido-2-deoxy-β-D-gluco and β-D-galactopyranosides and of β-(1-6)-linked 2-acetamido-2-deoxy-D-gluco and -D-galacto-pyranosyl oligosaccharides. Carbohydr Res. 186:177-188.
12. Disney MD, Seeberger PH. 2004. The use of carbohydrate microarrays to study carbohydrate-cell interactions to detect pathogens. Chem Biol 11:1701-1707.
13. Domon B, Costello CE. 1988. A systematic nomenclature for carbohydrate fragmentation in FAB-MS/MS spectra of glycoconjugates. Glycoconj J 5:397-409.
14. Dunn BE, Cohen H, Blaser MJ. 1997. Helicobacter pylori. Clin Microbiol Rev. 10:720-741.
15. Evans DG, Evans DJ Jr, Moulds JJ, Graham DY. 1988. N Acetylneuraminyllactose-binding fibrillar hemagglutinin of Campylobacter pylori: A putative colonization factor antigen. Infect Immun. 56:2896-2906.
16. Figueiredo C, Machado JC, Yamaoka Y. 2005. Pathogenesis of Helicobacter pylori infection. Helicobacter 10(Suppl S):14-20.
17. Folch J, Lees M, Sloane-Stanley GH. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem. 226:497-509.
18. Ford AC, Delaney BC, Forman D, Moayyedi P. 2004. Eradication therapy in Helicobacter pylori positive peptic ulcer disease: Systematic review and economic analysis. Am J Gastroenterol. 99:1833-1855.
19. Fuccio L, Zagari RM, Minardi ME, Bazzoli F. 2007. Systematic review: Helicobacter pylori eradication for the prevention of gastric cancer. Aliment Pharmacol Ther. 25:133-131.
20. Fukuda MN, Dell A, Oates JE, Wu P, Klock JC, Fukuda M. 1985. Structures of glycosphingolipids isolated from human granulocytes. The presence of a series of linear poly-N-acetyllactosaminylceramide and its significance in glycolipids of whole blood cells. J Biol Chem. 260:1067-1082.
21. Hanisch FG, Chai W, Rosankiewicz JR, Lawson AM, Stou MS, Feizi T. 1993. Core-typing of O-liked glycans from human gastric mucins: Lack of evidence for the occurence of the sequence Gal1-6GalNAc. Eur J Biochem. 217:645-655.
22. Hirmo S, Kelm S, Iwersen M, Hotta K, Goso Y, Ishihara K, Suguri T, Morita M, Wadström T, Schauer R. 1998. Inhibition of Helicobacter pylori sialic acid-specific hemagglutination by human gastrointestinal mucins and milk glycoproteins. FEMS Immunol Med Microbiol. 20:275-281.
23. Hirmo S, Kelm S, Schauer R, Nilsson B, Wadström T. 1996. Adhesion of Helicobacter pylori strains to α-2,3-linked sialic acids. Glycoconj J. 13:1005-1011.
24. IARC. 1994. Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7-14 June, IARC Monogr. Eval. Carcinog. Risks Hum. 61:1-241.
25. Johansson P, Nilsson J, Ångström J, Miller-Podraza H. 2005. Interaction of Helicobacter pylori with sialylated carbohydrates: The dependence on different parts of the binding trisaccharide Neu5Acα3Galβ4GlcNAc. Glycobiology. 15:625-636.
26. Karlsson K-A. 2000. The human gastric colonizer Helicobacter pylori A challenge for host-parasite glycobiology. Glycobiology. 10:761-771.
27. Kizuka Y, Matsui T, Takematsu H, Kozutsumi Y, Kawasaki T, Oka S. 2006. Physical and functional association of glucuronyltransferases and sulfotransferases involved in HNK-1 biosynthesis. J Biol Chem. 281:13644-13651.
28. Kornilov AV, Sherman AA, Kononov LO, Shashkov AS, Nifant'ev NE. 2000. Synthesis of 3-O-sulfoglucuronyl lacto-N-neotetraose 2-aminoethyl glycoside and biotinylated neoglycoconjugates thereof. Carbohydr Res. 329:717-730.
29. Kuo SH, Chen LT, Doong SL, Yeh KT, Wu MS, Mao TL, Hsu HC, Wang HP, Lin JT, Cheng AL. 2005. Expression of CD86 and increased infiltration of NK cells are associated with Helicobacter pylori-dependent state of early stage high-grade gastric lymphoma. World J Gastroenterol. 11:4357-4362.
30. Linden S, Mahdavi J, Hedenbro J, Boren T, Carlstedt I. 2004. Effect of pH on Helicobacter pylori binding to human gastric mucins. Identification of binding to non-MUC5AC mucins. Biochem J. 384:263-270.
31. Linden S, Nordman H, Hedenbro J, Hurtig M, Boren T. 2002. Strain- and blood group-dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms. Gastroenterology. 123:1923-1930.
32. Lingwood CA, Huesca M, Kuksis A. 1992. The glycerolipid receptor for Helicobacter pylori adhesion to eukaryotic cells in vitro. Infect Immun. 60:2470-2474.
33. Mahdavi J, Sondén B, Hurtig M, Olfat FO, Forsberg L, et al. 2002. Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science. 297:573-578.
34. Marshall BJ, Windsor HM. 2005. The relation of Helicobacter pylori to gastric carcinoma and lymphoma: Pathophysiology, epidemiology, screening, clinical presentation, treatment and prevention. Med Clin North Am. 89:313-344.
35. McGee DJ, Mobley HLT. 1999. Mechanisms of Helicobacter pylori infections: Bacterial factors. Curr Top Microbiol Immunol. 241:155-180.
36. Miller-Podraza H, Abul Milh M, Bergström J, Karlsson K-A. 1996. Recognition of glycoconjugates by Helicobacter pylori: An apparently high-affinity binding of human polyglycosylceramides, a second sialic acid-based specificity. Glycoconj J. 13:453-460.
37. Miller-Podraza H, Bergström J, Teneberg S, Abul-Milh M, Longard M, Olsson B-M, Uggla L, Karlsson K-A. 1999. Helicobacter pylori and neutrophils: Sialic acid-dependent binding to various isolated glycoconjugates. Infect Immun. 67:6309-6313.
38. Miller-Podraza H, Johansson P, Ångström J, Larsson T, Longard M, Karlsson K-A. 2004. Studies on gangliosides with affinity for Helicobacter pylori: Binding to natural and chemically modified structures. Glycobiology. 14:205-217.
39. Miller-Podraza H, Lanne B, Ångström J, Teneberg S, Abul-Milh M, Jovall P-Å, Karlsson H, Karlsson K-A. 2005. Novel binding epitope for Helicobacter pylori found in neolacto carbohydrate chains. J Biol Chem. 280:19695-19703.
40. Muthing J, Spanbroeck R, Peter-Katalinic J, Hanish FG, Hanski C, Hasegawa A, Unland F, Lehman J, Tschesche H, Egge H. 1996. Isolation and structural characterization of fucosylated gangliosides with linear poly-N-acetyllactosaminyl chains from human granulocytes. Glycobiology. 6:147-156.
41. Natomi H, Saitoh T, Sugano K, Wamori M, Fukayama M, Nagai Y. 1993. Systematic analysis of glycosphingolipids in the human gastrointestinal tract: Enrichment of sulfatides with hydroxylated longer-chain fatty acids in the gastric and duodenal mucosa. Lipids. 28:737-742.
42. Ong E, Suzuki M, Belot F, Yeh JC, Franceschini I, Angata K, Hindsgaul O, Fukuda M. 2002. Biosynthesis of HNK-1 glycans on O-linked oligosaccharides attaches to the neutral cell adhesion molecule (NCAM). The requirement for core 2 beta1, 6-N-acetyglucosaminyltransferase and the musclespecific domain in NCAM. J Biol Chem. 277:18182-18190.
43. Peek RM Jr, Blaser MJ. 2002. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer. 2:28-37.
44. Piller F, Cartron J-P. 1983. UDP-GlcNAc:GAlβ1-4Glc(Nac) β1-3N cetylglucosaminyltransferase. Identification and characterization in human serum. J Biol Chem. 258:12293-12299.
45. Pilotto A, Malfertheiner P. 2002. Review article: An approach to Helicobacter pylori infection in elderly. Aliment Pharmacol Ther 16:683-691.
46. Prakobphol A, Boren T, Ma W, Zhixiang P, Fisher S. 2005. Glycosylated human salivary molecules present oligosaccacharides that mediate adhesion of leukocytes and Helicobacter pylori. Biochemistry. 44:2216-2224.
47. Prakobphol A, Thompson KA, Hansson GC, Rosen SD, Singer MS, Phillips NJ, Medzihradszky KF, Burlingame AL, Leffler H, Fischer SJ. 1998. Human low-molecular-weight salivary mucin expresses the sialyl Lewis x determinant and has L-selectin ligand activity. Biochemistry. 37:4916-4927.
48. Rubinsztein-Dunlop S, Guy B, Lissolo L, Fischer H. 2005. Identification of two new Helicobacter pylori surface proteins involved in attachment to epithelial cell lines. J Med Microbiol. 54:427-434.
49. Slomiany BL, Piotrowski J, Samanta A, VanHorn K, Murty VLN, Slomiany A. 1989. Campylobacter pylori colonization factor shows specificity for lactosylceramide and GM3 ganglioside. Biochem Int. 19:929-936.
50. Stevens J, Blixt O, Tumpey TM, Taubenberger JK, Paulson JC, Wilson IA. 2006. Structure and receptor specificity of the hemagglutinin from an H5N1 influenza virus. Science. 312:404-410.
51. Stroud MR, Handa K, Salyan MEK, Ito K, Levery SB, Hakomori S-i, Reinhold BB, Reinhold VN. 1996. Monosialogangliosides of human myelogenous leukemia HL60 cells and normal human leukocytes: 1. Separation of E-selectin binding from nonbinding gangliosides, and absence of sialosyllex having tetraosyl to octaosyl core. Biochemistry. 35:758-769.
52. Syder AJ, Janaki L, Guruge JL, Li Q, Hu Y, Oleksiewicz CM, Robin G, Lorenz RG, Sherif M, Karam SM, et al. 1999. Helicobacter pylori attaches to NeuAcα2,3Galβ1,4 glycoconjugates produced in the stomach of transgenic mice lacking parietal cells. Mol Cell. 3:263-274.
53. Tagawa H, Kizuka Y, Ikeda T, Itoh S, Kawasaki N, Kurihara H, Onozato ML, Tojo A, Sakai T, Kawasaki T, et al. 2005. A non-sulfated form of the HNK-1 carbohydrate is expressed in mouse kidney. J Biol Chem. 280:23876-23883.
54. Tarkkanen J, Kosunen TU, Saksela E. 1993. Contact of lymphocytes with Helicobacter pylori augments natural killer cell activity and induces production of gamma-interferon. Infect Immun. 61:3012-3016.
55. Teneberg S, Leonardsson I, Karlsson H, Jovall P-Å, Ångström J, Danielsson D, Näslund I, Ljungh Å, Wadström T, Karlsson K-A. 2002. Lactotetrasosylceramide, a novel glycosphingolipid receptor for Helicobacter pylori present in human gastric epithelium. J Biol Chem. 277:19709-19719.
56. Teneberg S, Lönnroth I, Torres Lopez JF, Galili U, Ölwegård Halvarsson M, Ångström J, Karlsson K-A. 1996. Molecular mimicry in the recognition of glycosphingolipids by Galα3Galβ4GlcNAcβ-binding Clostridium difficile toxin A, human natural anti α-galactosyl IgG and the monoclonal abtibody Gal-13: Characterization of a binding-active human glycosphingolipid, nonidentical with the animal receptor. Glycobiology. 6:599-609.
57. Terayama K, Oka S, Seiki T, Miki Y, Nakamura A, Kozutsumi Y, Takio K, Kawasaki T. 1997. Cloning and functional expression of a novel glucuronyltransferase involved in the biosynthesis of the carbohydrate epitope HNK-1. Proc Natl Acad Sci USA. 94:6093-6098.
58. Theocharis AD, Vynios DH, Papageorgakopoulou N, Skandalis SS, Theocharis DA. 2003. Altered content composition and structure of glycosaminoglycans and proteoglycans in gastric carcinoma. Int J Biochem Cell Biol. 35:376-390.
59. Thompson KA, Prakobphol A, Leffler H, Reddy MS, Levine MJ, Fischer SJ, Hansson GC. 2002. The salivary mucin MG1 (MUC5B) carries a repertoire of unique oligosaccharides that is large and diverse. Glycobiology. 12:1-14.
60. Van de Bovenkamp JHB, Mahdavi J, Korteland Van Male AM, Buller HA, Einerhand AWC, Boren T, Dekker J. 2003. The MUC5AC glycoprotein is the primary receptor for Helicobacter pylori in the human stomach. Helicobacter. 8:521-532.
61. Van Der Wouden EJ, Thijs JC, Van Zwet AA, Kleibeuker JH. 2000. Review article: Nitroimidazole resistance in Helicobacter pylori. Aliment Pharmacol Ther. 14:7-14.
62. Wu JY, Kim JJ, Reddy R, Wang WM, Graham DY, Kwon DH. 2005. Tetracycline-resistant clinical Helicobacter pylori isolates with and without mutations in 16S rRNA-encoding genes. Antimicrob Agents Chemother. 49:578-583.
63. Yasukochi T, Fukase K, Suda Y, Takagaki K, Endo M,Kusumoto S. 1997. Enzymatic synthesis of 4-methylumbelliferyl glycosides of trisaccaride and core tetrasaccharide, Gal(β1-3)Gal(β1-4)Xyl and GlcA(β1-3)Gal(β1-3)Gal(β1-4)Xyl, corresponding to the linkage region of proteoglycans. Bull Chem Soc Jpn. 70:2719-2725.
64. Yun CH, Lundgren A, Azem J, Sjöling Å, Holmgren J, Svennerholm A-M, Lundin BS. 2005. Natural killer cells and Helicobacter pylori infection: Bacterial antigens and interleukin-12 act synergistically to induce gamma interferon production. Infect Immun. 73:1482-1490.