Muc5ac gastric mucin glycosylation is shaped by FUT2 activity and functionally impacts Helicobacter pylori binding

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Magalhães, Ana ^a,b   Rossez, Yannick ^c   Robbe Masselot, Catherine ^c   Maes, Emmanuel ^c   Gomes, Joana ^a,b   Shevtsova, Anna ^d   Bugaytsova, Jeanna ^d   Borén, Thomas ^d   Reis, Celso A ^a,b,e  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF PORTO   (Portugal)

^c UNIV LILLE   (France)

^d UMEÅ UNIVERSITY   (Sweden)

^e University of Porto   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BABA PROTEIN, HELICOBACTER PYLORI; FUCOSYLTRANSFERASE; GALACTOSIDE 2-ALPHA-L-FUCOSYLTRANSFERASE; MUC5AC PROTEIN, MOUSE; MUCIN 5AC; POLYSACCHARIDE; PROTEIN BINDING; STOMACH MUCIN;

ANIMAL; BACTERIUM ADHERENCE; BLOOD GROUP LEWIS SYSTEM; C57BL MOUSE; GENETICS; GLYCOSYLATION; HELICOBACTER INFECTION; HELICOBACTER PYLORI; HUMAN; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; MUCUS; PHYSIOLOGY; STOMACH MUCOSA;

ADHESINS, BACTERIAL; ANIMALS; BACTERIAL ADHESION; FUCOSYLTRANSFERASES; GASTRIC MUCINS; GASTRIC MUCOSA; GLYCOSYLATION; HELICOBACTER INFECTIONS; HELICOBACTER PYLORI; HUMANS; LEWIS BLOOD-GROUP SYSTEM; MICE, INBRED C57BL; MICE, KNOCKOUT; MUCIN 5AC; MUCUS; POLYSACCHARIDES; PROTEIN BINDING;

EID: 84969271212     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep25575     Document Type: Article

References (51)

1. McGuckin, M. A., Lindén, S. K., Sutton, P. and Florin, T. H. Mucin dynamics and enteric pathogens. Nat Rev Micro 9, 265-278, doi: 10.1038/nrmicro2538 (2011).
2. Pinho, S. S. and Reis, C. A. Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer 15, 540-555, doi: 10.1038/ nrc3982 (2015).
3. Magalhaes, A., Ismail, M. N. and Reis, C. A. Sweet receptors mediate the adhesion of the gastric pathogen Helicobacter pylori: glycoproteomic strategies. Expert Rev Proteomics 7, 307-310, doi: 10.1586/epr.10.18 (2010).
4. Moore, M. E., Borén, T. and Solnick, J. V. Life at the margins: Modulation of attachment proteins in Helicobacter pylori. Gut Microbes 2, 42-46, doi: 10.4161/gmic.2.1.14626 (2011).
5. Polk, D. B. and Peek, R. M. Helicobacter pylori: gastric cancer and beyond. Nat Rev Cancer 10, 403-414, doi: 10.1038/nrc2857 (2010).
6. Malfertheiner, P., Link, A. and Selgrad, M. Helicobacter pylori: perspectives and time trends. Nat Rev Gastroenterol Hepatol 11, 628-638, doi: 10.1038/nrgastro.2014.99 (2014).
7. Hidaka, E. et al. Helicobacter pylori and two ultrastructurally distinct layers of gastric mucous cell mucins in the surface mucous gel layer. Gut 49, 474-480, doi: 10.1136/gut.49.4.474 (2001).
8. Schreiber, S. et al. The spatial orientation of Helicobacter pylori in the gastric mucus. Proc Natl Acad Sci USA 101, 5024-5029, doi: 10.1073/pnas.0308386101 (2004).
9. Reis, C. A. et al. Immunohistochemical study of MUC5AC expression in human gastric carcinomas using a novel monoclonal antibody. Int J Cancer 74, 112-121, doi: 10.1002/(sici)1097-0215(19970220)74:1 3.0.co;2-h (1997).
10. Squire, J. M. et al. Quantitative MUC5AC and MUC6 mucin estimations in gastric mucus by a least-squares minimization method. Anal Biochem 439, 204-211, doi: http://dx.doi.org/10.1016/j.ab.2013.04.013 (2013).
11. Kenny, D. T. et al. Presence of terminal N-acetylgalactosamine? 1-4N-acetylglucosamine residues on O-linked oligosaccharides from gastric MUC5AC: Involvement in Helicobacter pylori colonization? Glycobiology 22, 1077-1085, doi: 10.1093/glycob/cws076 (2012).
12. Rossez, Y. et al. Almost all human gastric mucin O-glycans harbor blood group A, B or H antigens and are potential binding sites for Helicobacter pylori. Glycobiology 22, 1193-1206, doi: 10.1093/glycob/cws072 (2012).
13. Stone, E. L. et al. Glycosyltransferase Function in Core 2-Type Protein O Glycosylation. Mol Cell Biol 29, 3770-3782, doi: 10.1128/ mcb.00204-09 (2009).
14. Holmén Larsson, J. M., Thomsson, K. A., Rodriguez-Pieiro, A. M., Karlsson, H. and Hansson, G. C. Studies of mucus in mouse stomach, small intestine, and colon. III. Gastrointestinal Muc5ac and Muc2 mucin O-glycan patterns reveal a regiospecific distribution. Am J of Physiol Gastrointest Liver Physiol 305, G357-G363, doi: 10.1152/ajpgi.00048.2013 (2013).
15. Ilver, D. et al. Helicobacter pylori Adhesin Binding Fucosylated Histo-Blood Group Antigens Revealed by Retagging. Science 279, 373-377, doi: 10.1126/science.279.5349.373 (1998).
16. Boren, T., Falk, P., Roth, K. A., Larson, G. and Normark, S. Attachment of Helicobacter pylori to human gastric epithelium mediated by blood group antigens. Science 262, 1892-1895, doi: 10.1126/science.8018146 (1993).
17. Linden, S. et al. Strain- and blood group dependent binding of Helicobacter pylori to human gastric MUC5AC glycoforms. Gastroenterology 123, 1923-1930, doi: 10.1053/gast.2002.37076 (2002).
18. Van de Bovenkamp, J. H. et al. The MUC5AC glycoprotein is the primary receptor for Helicobacter pylori in the human stomach. Helicobacter 8, 521-532, doi: 10.1046/j.1523-5378.2003.00173.x (2003).
19. Gerhard, M. et al. Clinical relevance of the Helicobacter pylori gene for blood-group antigen-binding adhesin. Proc Natl Acad Sci USA 96, 12778-12783, doi: 10.1073/pnas.96.22.12778 (1999).
20. Rossez, Y. et al. The LacdiNAc-Specific Adhesin LabA Mediates Adhesion of Helicobacter pylori to Human Gastric Mucosa. J Infect Dis 210, 1286-1295, doi: 10.1093/infdis/jiu239 (2014).
21. Magalhes, A. et al. Helicobacter pylori chronic infection and mucosal inflammation switches the human gastric glycosylation pathways. Biochim Biophys Acta 1852, 1928-1939, doi: http://dx.doi.org/10.1016/j.bbadis.2015.07.001 (2015).
22. Marcos, N. et al. Helicobacter pylori induces beta3GnT5 in human gastric cell lines, modulating expression of the SabA ligand sialyl- Lewis x. J Clin Invest 118, 12, doi: 10.1172/JCI34324 (2008).
23. Mahdavi, J. et al. Helicobacter pylori SabA Adhesin in Persistent Infection and Chronic Inflammation. Science 297, 573-578, doi: 10.1126/science.1069076 (2002).
24. Ota, H. et al. Helicobacter pylori infection produces reversible glycosylation changes to gastric mucins. Virchows Archiv 433, 419-426, doi: 10.1007/s004280050269 (1998).
25. Mollicone, R., Bara, J., Le Pendu, J. and Oriol, R. Immunohistologic pattern of type 1 (Lea, Leb) and type 2 (X, Y, H) blood grouprelated antigens in the human pyloric and duodenal mucosae. Lab Invest 53, 9 (1985).
26. Azevedo, M. et al. Infection by Helicobacter pylori expressing the BabA adhesin is influenced by the secretor phenotype. J Pathol 215, 308-316, doi: 10.1002/path.2363 (2008).
27. Ikehara, Y. et al. Polymorphisms of Two Fucosyltransferase Genes (Lewis and Secretor Genes) Involving Type I Lewis Antigens Are Associated with the Presence of Anti-Helicobacter pylori IgG Antibody. Cancer Epidemiol Biomarkers Prev 10, 971-977 (2001).
28. Magalhaes, A. et al. Fut2-null mice display an altered glycosylation profile and impaired BabA-mediated Helicobacter pylori adhesion to gastric mucosa. Glycobiology 19, 1525-1536, doi: 10.1093/glycob/cwp131 (2009).
29. Stone, E. L. et al. Glycosyltransferase Function in Core 2-Type Protein O-Glycosylation. Mol. Cell. Biol. MCB.00204-00209, doi: 10.1128/mcb.00204-09 (2009).
30. Bolos, C. D., Garrido, M. and Real, F. X. MUC6 apomucin shows a distinct normal tissue distribution that correlates with Lewis antigen expression in the human stomach. Gastroenterology 109, 723-734 (1995).
31. Aspholm, M. et al. SabA Is the H. pylori Hemagglutinin and Is Polymorphic in Binding to Sialylated Glycans. PLos Pathog 2, e110, http://dx.doi.org/10.1371/journal.ppat.0020110 (2006).
32. Joncquel Chevalier Curt, M. et al. Alteration or adaptation, the two roads for human gastric mucin glycosylation infected by Helicobacter pylori. Glycobiology 25, 617-631, doi: 10.1093/glycob/cwv004 (2015).
33. Ho, S. B. et al. Expression cloning of gastric mucin complementary DNA and localization of mucin gene expression. Gastroenterology 109, 735-747, doi: http://dx.doi.org/10.1016/0016-5085(95)90380-1 (1995).
34. Reis, C. A. et al. Immunohistochemical study of the expression of MUC6 mucin and co-expression of other secreted mucins (MUC5AC and MUC2) in human gastric carcinomas. J Histochem Cytochem. 48, 377-388, doi: 10.1177/002215540004800307 (2000).
35. Jonckheere, N. et al. Transcriptional activation of the murine Muc5ac mucin gene in epithelial cancer cells by TGF-beta/Smad4 signalling pathway is potentiated by Sp1. Biochem. J. 377, 797-808, doi: 10.1042/bj20030948 (2004).
36. Lidell, M. E., Bara, J. and Hansson, G. C. Mapping of the 45M1 epitope to the C-terminal cysteine-rich part of the human MUC5AC mucin. FEBS Journal 275, 481-489, doi: 10.1111/j.1742-4658.2007.06215.x (2008).
37. Nordman, H. et al. Gastric MUC5AC and MUC6 are large oligomeric mucins that differ in size, glycosylation and tissue distribution. Biochem J 364, 191-200, doi: 10.1042/bj3640191 (2002).
38. Costache, M. et al. Evolution of Fucosyltransferase Genes in Vertebrates. J. Biol. Chem. 272, 29721-29728, doi: 10.1074/ jbc.272.47.29721 (1997).
39. Gersten, K. M. et al. Molecular Cloning, Expression, Chromosomal Assignment, and Tissue-specific Expression of a Murine alpha- (1,3)-Fucosyltransferase Locus Corresponding to the Human ELAM-1 Ligand Fucosyl Transferase. J. Biol. Chem. 270, 25047-25056, doi: 10.1074/jbc.270.42.25047 (1995).
40. Nairn, A. V. et al. Regulation of Glycan Structures in Animal Tissues: Transcript profiling of glycan-related genes. J. Biol. Chem. 283, 17298-17313, doi: 10.1074/jbc.M801964200 (2008).
41. Skoog, E. C. et al. Human Gastric Mucins Differently Regulate Helicobacter pylori Proliferation, Gene Expression and Interactions with Host Cells. PLos One 7, e36378, doi: 10.1371/journal.pone.0036378 (2012).
42. Domino, S. E., Zhang, L., Gillespie, P. J., Saunders, T. L. and Lowe, J. B. Deficiency of Reproductive Tract alpha (1,2)Fucosylated Glycans and Normal Fertility in Mice with Targeted Deletions of the FUT1 or FUT2 alpha (1,2)Fucosyltransferase Locus. Mol. Cell. Biol. 21, 8336-8345, doi: 10.1128/mcb.21.24.8336-8345.2001 (2001).
43. Falk, P. G., Bry, L., Holgersson, J. and Gordon, J. I. Expression of a human alpha-1,3/4-fucosyltransferase in the pit cell lineage of FVB/N mouse stomach results in production of Leb-containing glycoconjugates: a potential transgenic mouse model for studying Helicobacter pylori infection. Proc Natl Acad Sci USA 92, 1515-1519 (1995).
44. Pinto, R. et al. Identification of new cancer biomarkers based on aberrant mucin glycoforms by in situ proximity ligation. J Cell Mol Med 16, 1474-1484, doi: 10.1111/j.1582-4934.2011.01436.x (2012).
45. Hovenberg, H. W., Davies, J. R., Herrmann, A., Linden, C. J. and Carlstedt, I. MUC5AC, but not MUC2, is a prominent mucin in respiratory secretions. Glycoconj J 13, 839-847 (1996).
46. Walker, J. M. The Protein Protocols Handbook (Humana Press Inc, 2009).
47. Aspholm, M. et al. in Methods in Enzymology Vol. Volume 417 (ed Minoru, Fukuda) 293-339 (Academic Press, 2006).
48. Daher, N., Bara, J. and Moubarak, M. Non A non B and Lewis related antigens in normal human prostates: an immunohistological study of 20 anti-glycoconjugate monoclonal antibodies. Rev Fr Transfus Immunohematol 30, 4 (1987).
49. Manimala, J. C., Roach, T. A., Li, Z. and Gildersleeve, J. C. High-throughput carbohydrate microarray profiling of 27 antibodies demonstrates widespread specificity problems. Glycobiology. 17, 17C-23C, doi: 10.1093/glycob/cwm047 (2007).
50. Sakamoto, J. et al. Expression of Lewisa, Lewisb, X, and Y Blood Group Antigens in Human Colonic Tumors and Normal Tissue and in Human Tumor-derived Cell Lines. Cancer Res 46, 1553-1561 (1986).
51. Odenbreit, S., Kavermann, H., Püls, J. and Haas, R. CagA tyrosine phosphorylation and interleukin-8 induction by Helicobacter pylori are independent from AlpAB, HopZ and Bab group outer membrane proteins. Int J Med Microbiol 292, 257-266, doi: http://dx.doi. org/10.1078/1438-4221-00205 (2002).