Identification of glycoprotein receptors within the human salivary proteome for the lectin-like BabA and SabA adhesins of Helicobacter pylori by fluorescence-based 2-D bacterial overlay

Proteomics

Volumn 9, Issue 6, 2009, Pages 1582-1592

  Walz, Anke ^a   Odenbreit, Stefan ^b   Stühler, Kai ^c   Wattenberg, Andreas ^d   Meyer, Helmut E ^c   Mahdavi, Jafar ^e   Borén, Thomas ^f   Ruhl, Stefan ^a,g  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY OF MUNICH   (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

^d PROTAGEN AG   (Germany)

^e QUEEN S MEDICAL CENTRE   (United Kingdom)

^f UMEÅ UNIVERSITY   (Sweden)

^g UNIVERSITY AT BUFFALO   (United States)

Author keywords

Adhesins; Helicobacter pylori; Proteome map; Saliva

Indexed keywords

ADHESIN; BABA ADHESIN; CARBONATE DEHYDRATASE VI; GLYCOPROTEIN; GLYCOPROTEIN GP 340; IMMUNOGLOBULIN A1; MUCIN 5B; MUCIN 7; PROTEOME; SABA ADHESIN; SALIVA PROTEIN; SECRETORY COMPONENT; UNCLASSIFIED DRUG;

ARTICLE; HELICOBACTER PYLORI; HUMAN; HUMAN TISSUE; INNATE IMMUNITY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; SALIVA;

ADHESINS, BACTERIAL; BACTERIAL ADHESION; BLOTTING, WESTERN; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENCE; GLYCOPROTEINS; HELICOBACTER PYLORI; HUMANS; LECTINS; MOLECULAR WEIGHT; PROTEIN BINDING; PROTEOME; RECEPTORS, CELL SURFACE; SALIVA; SALIVARY PROTEINS AND PEPTIDES;

BACTERIA (MICROORGANISMS); HELICOBACTER PYLORI;

EID: 63049099439     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200700808     Document Type: Article

References (46)

1. Pizarro-Cerdá, J., Cossart, P., Bacterial adhesion and entry into host cells. Cell 2006, 124, 715-727.
2. Dunn, B. E., Cohen, H., Blaser, M. J., Helicobacter pylori. Clin. Microbiol. Rev. 1997, 10, 720-741.
3. Ernst, P. B., Gold, B. D., The disease spectrum of Helicobacter pylori: The immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu. Rev. Microbiol. 2000, 54, 615-640.
4. Suerbaum, S., Michetti, P., Helicobacter pylori infection. N. Engl. J. Med. 2002, 347, 1175-1186.
5. Dowsett, S. A., Kowolik, M. J., Oral Helicobacter pylori: Can we stomach it? Crit. Rev. Oral Biol. Med. 2003, 14, 226-233.
6. Bürgers, R., Schneider-Brachert, W., Reischl, U., Behr, A. et al., Helicobacter pylori in human oral cavity and stomach. Eur. J. Oral Sci. 2008, 116, 297-304.
7. Gerhard, M., Hirmo, S., Wadström, T., Miller-Podraza, H. et al., Helicobacter pylori: Molecular and cellular Biology, Horizon Scientific Press, Wymondham, UK 2001, pp. 185-206.
8. Borén, T., Falk, P., Roth, K. A., Larson, G., Normark, S., Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 1993, 262, 1892-1895.
9. Ilver, D., Arnqvist, A., Ogren, J., Frick, I. M. et al., Helicobacter pylori adhesin binding fucosylated histo-blood group antigens revealed by retagging. Science 1998, 279, 373-377.
10. Mahdavi, J., Sondén, B., Hurtig, M., Olfat, F. O. et al., Helicobacter pylori SabA adhesin in persistent infection and chronic inflammation. Science 2002, 297, 573-578.
11. Aspholm-Hurtig, M., Dailide, G., Lahmann, M., Kalia, A. et al., Functional adaptation of BabA, the H. pylori ABO blood group antigen binding adhesin. Science 2004, 305, 519-522.
12. Walz, A., Odenbreit, S., Mahdavi, J., Borén, T., Ruhl, S., Identification and characterization of binding properties of Helicobacter pylori by glycoconjugate arrays. Glycobiology 2005, 15, 700-708.
13. Aspholm, M., Kalia, A., Ruhl, S., Schedin, S. et al., Helicobacter pylori adhesion to carbohydrates. Methods Enzymol. 2006, 417, 293-339.
14. Mentis, A., Tzouvelekis, L., Spiliadis, C., Blackwell, C. C., Weir, D. M., Inhibition of Helicobacter pylori haemagglutination activity by human salivary mucins. FEMS Microbiol. Immunol. 1990, 2, 125-127.
15. Veerman, E. C., Bank, C. M., Namavar, F., Appelmelk, B. J. et al., Sulfated glycans on oral mucin as receptors for Helicobacter pylori. Glycobiology 1997, 7, 737-743.
16. Namavar, F., Sparrius, M., Veerman, E. C., Appelmelk, B. J., Vandenbroucke-Grauls, C. M., Neutrophil-activating protein mediates adhesion of Helicobacter pylori to sulfated carbohydrates on high-molecular-weight salivary mucin. Infect. Immun. 1998, 66, 444-447.
17. Prakobphol, A., Borén, T., Ma, W., Zhixiang, P., Fisher, S. J., Highly glycosylated human salivary molecules present oligosaccharides that mediate adhesion of leukocytes and Helicobacter pylori. Biochemistry 2005, 44, 2216-2224.
18. Prakobphol, A., Xu, F., Hoang, V. M., Larsson, T. et al., Salivary agglutinin, which binds Streptococcus mutans and Helicobacter pylori, is the lung scavenger receptor cysteine-rich protein gp-340. J. Biol. Chem. 2000, 275, 39860-39866.
19. Prakobphol, A., Murray, P. A., Fisher, S. J., Bacterial adherence on replicas of sodium dodecyl sulfate-polyacrylamide gels. Anal. Biochem. 1987, 164, 5-11.
20. Ruhl, S., Sandberg, A. L., Cisar, J. O., Recognition of immunoglobulin A1 by oral actinomyces and streptococcal lectins. Infect. Immun. 1996, 64, 5421-5424.
21. Walz, A., Stühler, K., Wattenberg, A., Hawranke, E. et al., Proteome analysis of glandular parotid and submandibular-sublingual saliva in comparison to whole human saliva by two-dimensional gel electrophoresis. Proteomics 2006, 6, 1631-1639.
22. Ruhl, S., Sandberg, A. L., Cisar, J. O., Salivary receptors for the proline-rich protein-binding and lectin-like adhesins of oral actinomyces and streptococci. J. Dent. Res. 2004, 83, 505-510.
23. Steinberg, T. H., Pretty On Top, K., Berggren, K. N., Kemper, C. et al., Rapid and simple single nanogram detection of glycoproteins in polyacrylamide gels and on electroblots. Proteomics 2001, 1, 841-855.
24. Görg, A., Obermaier, C., Boguth, G., Harder, A. et al., The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 2000, 21, 1037-1053.
25. Ruhl, S., Rayment, S. A., Schmalz, G., Hiller, K. A., Troxler, R. F., Proteins in whole saliva during the first year of infancy. J. Dent. Res. 2005, 84, 29-34.
26. Alm, R. A., Ling, L. S., Moir, D. T., King, B. L. et al., Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 1999, 397, 176-180.
27. Tabak, L. A., In defense of the oral cavity: Structure, biosynthesis, and function of salivary mucins. Annu. Rev. Physiol. 1995, 57, 547-564.
28. Norderhaug, I. N., Johansen, F. E., Schjerven, H., Brandtzaeg, P., Regulation of the formation and external transport of secretory immunoglobulins. Crit. Rev. Immunol. 1999, 19, 481-508.
29. Yamashita, K., Tachibana, Y., Nakayama, T., Kitamura, M. et al., Structural studies of the sugar chains of human parotid alpha-amylase. J. Biol. Chem. 1980, 255, 5635-5642.
30. Prakobphol, A., Leffler, H., Fisher, S. J., The high-molecular-weight human mucin is the primary salivary carrier of ABH, Le(a), and Le(b) blood group antigens. Crit. Rev. Oral Biol. Med. 1993, 4, 325-333.
31. Thomsson, K. A., Prakobphol, A., Leffler, H., Reddy, M. S. et al., The salivary mucin MG1 (MUC5B) carries a repertoire of unique oligosaccharides that is large and diverse. Glycobiology 2002, 12, 1-14.
32. Linden, S., Mahdavi, J., Hedenbro, J., Borén, T., Carlstedt, I., Effects of pH on Helicobacter pylori binding to human gastric mucins: Identification of binding to nonMUC5AC mucins. Biochem. J. 2004, 384, 263-270.
33. Prakobphol, A., Thomsson, K. A., Hansson, G. C., Rosen, S. D. et al., Human low-molecular-weight salivary mucin expresses the sialyl lewisx determinant and has L-selectin ligand activity. Biochemistry 1998, 37, 4916-4927.
34. Eriksson, C., Frangsmyr, L., Danielsson, N. L., Loimaranta, V. et al., Variant size- and glycoforms of the scavenger receptor cysteine-rich protein gp-340 with differential bacterial aggregation. Glycoconj. J. 2007, 24, 131-142.
35. Hartshorn, K. L., Ligtenberg, A., White, M. R., van Eijk, M. et al., Salivary agglutinin and lung scavenger receptor cysteine-rich glycoprotein 340 have broad anti-influenza activities and interactions with surfactant protein D that vary according to donor source and sialylation. Biochem. J. 2006, 393, 545-553.
36. Gillece-Castro, B. L., Prakobphol, A., Burlingame, A. L., Leffler, H., Fisher, S. J., Structure and bacterial receptor activity of a human salivary proline-rich glycoprotein. J. Biol. Chem. 1991, 266, 17358-17368.
37. Murakami, H., Sly, W. S., Purification and characterization of human salivary carbonic anhydrase. J. Biol. Chem. 1987, 262, 1382-1388.
38. Thatcher, B. J., Doherty, A. E., Orvisky, E., Martin, B. M., Henkin, R. I., Gustin from human parotid saliva is carbonic anhydrase VI. Biochem. Biophys. Res. Commun. 1998, 250, 635-641.
39. 2-glycoprotein and its homology to histocompatibility antigens. Proc. Natl. Acad. Sci. USA 1988, 85, 679-683.
40. 2-glycoprotein of normal human plasma. J. Biol. Chem. 1961, 236, 1066-1074.
41. Geetha, C., Venkatesh, S. G., Bingle, L., Bingle, C. D., Gorr, S. U., Design and validation of anti-inflammatory peptides from human parotid secretory protein. J. Dent. Res. 2005, 84, 149-153.
42. Royle, L., Roos, A., Harvey, D. J., Wormald, M. R. et al., Secretory IgA N- and O-glycans provide a link between the innate and adaptive immune systems. J. Biol. Chem. 2003, 278, 20140-20153.
43. Andersen, R. N., Ganeshkumar, N., Kolenbrander, P. E., Helicobacter pylori adheres selectively to Fusobacterium spp. Oral Microbiol. Immunol. 1998, 13, 51-54.
44. McColl, K. E., When saliva meets acid: Chemical warfare at the oesophagogastric junction. Gut 2005, 54, 1-3.
45. Ligtenberg, A. J., Veerman, E. C., Nieuw Amerongen, A. V., Mollenhauer, J., Salivary agglutinin/glycoprotein-340/DMBT1: A single molecule with variable composition and with different functions in infection, inflammation and cancer. Biol. Chem. 2007, 388, 1275-1289.
46. Rogers, J. D., Palmer, R. J., Jr., Kolenbrander, P. E., Scannapieco, F. A., Role of Streptococcus gordonii amylase-binding protein A in adhesion to hydroxyapatite, starch metabolism, and biofilm formation. Infect. Immun. 2001, 69, 7046-7056.