Sequential biosynthesis of sulfated and/or sialylated Lewis x determinants by transferases of the human bronchial mucosa

Glycobiology

Volumn 9, Issue 11, 1999, Pages 1199-1211

  Degroote, Sophie ^a   Ducourouble, Marie Paule ^a   Roussel, Philippe ^a   Lamblin, Geneviève ^a  

^a INSERM   (France)

Author keywords

6 sulfo sialyl lewis x; Biosynthesis; Bronchial mucins; Cystic fibrosis; Transferases

Indexed keywords

ADENOSINE 3' PHOSPHATE 5' PHOSPHOSULFATE; CARBOHYDRATE; EPITOPE; FUCOSYLTRANSFERASE; LEWIS X; MUCIN; OLIGOSACCHARIDE; SIALYLTRANSFERASE; TRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; BRONCHUS MUCOSA; CARBOHYDRATE SYNTHESIS; CYSTIC FIBROSIS; HUMAN; HUMAN TISSUE; ISOTOPE LABELING; MICROSOME; PRIORITY JOURNAL; SIALYLATION; SULFATION;

BRONCHUS;

EID: 0032750616     PISSN: 09596658     EISSN: None     Source Type: Journal    
DOI: 10.1093/glycob/9.11.1199     Document Type: Article

References (52)

1. Barasch,J. and Al-Awqati,Q. (1993) Defective acidification of the biosynthetic pathway in cystic fibrosis. J. Cell Sci., 17 (Suppl.), 229-233.
2. Barasch,J., Kiss,B., Prince,A., Saiman,L., Gruenert,D. and Al-Awqati,Q. (1991) Defective acidification of intracellular organelles in cystic fibrosis. Nature, 352, 70-73.
3. Boat,T.F., Cheng,P.W. and Wood,R.E. (1977) Tracheobronchial mucus secretion in vivo and in vitro by epithelial tissues from cystic fibrosis and control subjects. Mod. Probl. Paediatr., 19, 141-152.
4. Bobek,L.A., Tsai,H., Biesbrock,A.R. and Levine,M.J. (1993) Molecular cloning, sequence, and specificity of expression of the gene encoding the low molecular weight human salivary mucin (MUC7). J. Biol. Chem., 268, 20563-20569.
5. Bowman,K.G., Hemmerich,S., Bhakta,S., Singer,M.S., Bistrup,A., Rosen,S.D. and Bertozzi,C.R. (1998) Identification of an N-acetylglucosamine-6-O-sulfotransferase activity specific to lymphoid tissue: an enzyme with a possible role in lymphocyte homing. Chem. Biol., 5, 447-460.
6. Breg,J., Van Halbeek,H., Vliegenthart,J.F., Lamblin,G., Houvenaghel,M.C. and Roussel,P. (1987) Structure of sialyl-oligosaccharides isolated from bronchial mucus glycoproteins of patients (blood group O) suffering from cystic fibrosis. Eur. J. Biochem., 168, 57-68.
7. Britten,C.J., van den Eijnden,D.H., McDowell,W., Kelly,V.A., Witham,S.J., Edbrooke,M.R., Bird,M.I., de Vries,T. and Smithers,N. (1998) Acceptor specificity of the human leukocyte α3fucosyltransferase: role of FucT-VII in the generation of selectin ligands. Glycobiology, 8, 321-327.
8. Carnoy,C., Ramphal,R., Scharfman,A., Lo-Guidice,J.M., Houdret,N., Klein,A., Galabert,C., Lamblin,G. and Roussel,P. (1993) Altered carbohydrate composition of salivary mucins from patients with cystic fibrosis and the adhesion of Pseudomonas aeruginosa. Am. J. Respir. Cell Mol. Biol., 9, 323-334.
9. Chandrasekaran,E.V., Jain,R.K., Larsen,R.D., Wlasichuk,K., DiCioccio,R.A. and Matta,K.L. (1996a) Specificity analysis of three clonal and five non-clonal α1,3-L-fucosyltransferases with sulfated, sialylated, or fucosylated synthetic carbohydrates as acceptors in relation to the assembly of 3′-sialyl-6′-sulfo Lewis x (the L-selectin ligand) and related complex structures. Biochemistry, 35, 8925-8933.
10. Chandrasekaran,E.V., Jain,R.K., Larsen,R.D., Wlasichuk,K. and Matta,K.L. (1996b) Characterization of the specificities of human blood group H gene-specified α1,2-L-fucosyltransferase toward sulfated/sialylated/fucosylated acceptors: evidence for an inverse relationship between α1,2-L-fucosylation of Gal and α1,6-L-fucosylation of asparagine-linked GlcNAc. Biochemistry, 35, 8914-8924.
11. Chandrasekaran,E.V., Jain,R.K., Vig,R. and Matta,K.L. (1997) The enzymatic sulfation of glycoprotein carbohydrate units: blood group T-hapten specific and two other distinct Gal-3-O-sulfotransferases as evident from specificities and kinetics and the influence of sulfate and fucose residues occurring in the carbohydrate chain on C-3 sulfation of terminal Gal. Glycobiology, 7, 753-768.
12. Cheng,P.W., Boat,T.F., Cranfill,K., Yankaskas,J.R. and Boucher,R.C. (1989) Increased sulfation of glycoconjugates by cultured nasal epithelial cells from patients with cystic fibrosis. J. Clin. Invest., 84, 68-72.
13. Crommie,D. and Rosen,S.D. (1995) Biosynthesis of GlyCAM-1, amucin-like ligand for L-selectin. J. Biol. Chem., 270, 22614-22624.
14. Crottet,P., Kim,Y.J. and Varki,A. (1996) Subsets of sialylated, sulfated mucins of diverse origins are recognized by L-selectin. Lack of evidence for unique oligosaccharide sequences mediating binding. Glycobiology, 6, 191-208.
15. Davril,M., Degroote,S., Humbert,P., Galabert,C., Dumur,V., Lafitte,J.J., Lamblin,G. and Roussel,P. (1999) The sialylation of bronchial mucins secreted by patients suffering from cystic fibrosis or from chronic bronchitis is related to the severity of airway infection. Glycobiology, 9, 311-321.
16. De Vries,T., Srnka,C.A., Palcic,M.M., Swiedler,S.J., van den Eijnden,D.H. and Macher,B.A. (1995) Acceptor specificity of different length constructs of human recombinant α1,3/4-fucosyltransferases. Replacement of the stem region and the transmembrane domain of fucosyltransferase V by protein A results in an enzyme with GDP-fucose hydrolyzing activity. J. Biol. Chem., 270, 8712-8722.
17. De Vries,T., Palcic,M.P., Schoenmakers,P.S., van den Eijnden,D.H. and Joziasse,D.H. (1996) Acceptor specificity of GDP-Fuc:Galβ1-4GlcNAc-R α-fucosyltransferase VI (FucT VI) expressed in insect cells as soluble, secreted enzyme. Glycobiology, 7, 921-927.
18. Degroote,S., Lo-Guidice,J.M., Strecker,G., Ducourouble,M.P., Roussel,P. Lamblin,G. (1997) Characterization of an N-acetylglucosamine-6-O-sulfotransferase from human respiratory mucosa active on mucin carbohyrate chains. J. Biol. Chem., 272, 29493-29501.
19. Desseyn,J.L., Buisine,M.P., Porchet,N., Aubert,J.P., Degand,P. and Laine,A. (1998) Evolutionary history of the 11p15 human mucin gene family. J. Mol. Evol., 46, 102-106.
20. Dosanjh,A., Lencer,W., Brown,D., Ausiello,D.A. and Stow,J.L. (1994) Heterologous expression of ΔF508 CFTR results in decreased sialylation of membrane glycoconjugates. Am. J. Physiol., 266, C360-C366.
21. Emery,N., Lo-Guidice,J.M., Lafitte,J.J., Lhermitte,M. and Roussel,P. (1997) The fucosylation and secretion of mucins synthesized in human bronchial cells vary according to growth conditions. Glycobiology, 7, 95-101.
22. Galustian,C., Lawson,A.M., Komba,S., Ishida,H., Kiso,M. and Feizi,T. (1997) Sialyl-Lewis x sequence 6-O-sulfated at N-acetylglucosamine rather than at galactose is the preferred ligand for L-selection and de-N-acetylation of the sialic acid enhances the binding strength. Biochem. Biophys. Res. Commun., 240, 748-751.
23. Høiby,N. (1988) Hemophilus influenzae, Staphylococcus aureus, Pseudomonas cepacia, and Pseudomonas aeruginosa in patients with cystic fibrosis. Chest, 94, 97S-103S.
24. Jeffery,P.K. and Li,D. (1997) Airway mucosa: secretory cells, mucus and mucin genes. Eur. Respir. J., 10, 1655-1662.
25. Kelly,R.J., Rouquier,S., Giorgi,D., Lennon,G.G. and Lowe,J.B. (1995) Sequence and expression of a candidate for the human Secretor blood group α(1,2)fucosyltransferase gene (FUT2). Homozygosity for an enzyme-inactivating nonsense mutation commonly correlates with the non-secretor phenotype. J. Biol. Chem., 270, 4640-4649.
26. Kitagawa,H. and Paulson,J.C. (1994) Differential expression of five sialyltransferase genes in human tissues. J. Biol. Chem., 269, 17872-17878.
27. Kukowska-Latallo,J.F., Larsen,R.D., Nair,R.P. and Lowe,J.B. (1990) A cloned human cDNA determines expression of a mouse stage-specific embryonic antigen and the Lewis blood group α(1,3/1,4)fucosyltransferase. Genes Dev., 4, 1288-1303.
28. Kumar,R., Potvin,B., Muller,W.A. and Stanley,P. (1991) Cloning of a hauman α(1,3)-fucosyltransferase gene that encodes ELFT but does not confer ELAM-1 recognition on Chinese hamster ovary cell transfectants. J. Biol. Chem., 266, 21777-21783.
29. Lamblin,G., Lafitte,J.J., Lhermitte,M., Degand,P. and Roussel,P. (1977) Mucins from cystic fibrosis sputum. Mod. Probl. Paediatr., 19, 153-164.
30. 1H-n. m. r. spectroscopic study. Biochem. J., 275, 199-206.
31. Larsen,R.D., Ernst,L.K., Nair,R.P. and Lowe,J.B (1990) Molecular cloning, sequence, and expression of a human GDP-L-fucose:β-D-galactoside 2-α-L-fucosyltransferase cDNA that can form the H blood group antigen. Proc. Natl Acad. Sci. USA, 87, 6674-6678.
32. Lo-Guidice,J.M., Wieruszeski,J.M., Lemoine,J., Verbert,A., Roussel,P. and Lamblin,G. (1994) Sialylation and sulfation of the carbohydrate chains in respiratory mucins from a patient with cystic fibrosis. J. Biol. Chem., 269, 18794-18813.
33. Lo-Guidice,J.M., Perini, J.M., Lafitte,J.J., Ducourouble,M.P., Roussel,P. and Lamblin,G. (1995) Characterization of a sulfotransferase from human airways responsible for the 3-O-sulfation of terminal galactose in N-acetyllactosamine-containing mucin carbohydrate chains. J. Biol. Chem., 270, 27544-27550.
34. Majuri,M.L., Pinola,M., Niemelä,R., Tiisala,S., Natunen,J., Renkonen,O. and Renkonen,R. (1994) α2,3-sialyl and α1,3-fucosyltransferase-dependent synthesis of sialyl Lewis x, an essential oligosaccharide present on L-selectin counterreceptors, in cultured endothelial cells. Eur. J. Immunol., 24, 3205-3210.
35. Mawhinney,T.P., Landrum,D.C., Gayer,D.A. and Barbero,G.J. (1992) Sulfated sialyl-oligosaccharides derived from tracheobronchial mucous glycoproteins of a patient suffering from cystic fibrosis. Carbohydr. Res., 235, 179-197.
36. Natsuka,S., Gersten,K.M., Zenita,K., Kannagi,R. and Lowe,J.B. (1994) Molecular cloning of a cDNA encoding novel human leukocyte α-1,3-fucosyltransferase capable of synthesizing the sialyl Lewis x determinant. J. Biol. Chem., 269, 16789-16794.
37. Pasyk,E.A. and Foskett,J.K. (1997) Cystic fibrosis transmembrane conductance regulator-associated ATP and adenosine 3′-phosphate 5′-phosphosulfate channels in endoplasmic reticulum and plasma membranes. J. Biol. Chem., 272, 7746-7751.
38. Pind,S., Riordan,J.R. and Williams,D.B. (1994) Participation of the endoplasmic reticulum chaperone calnexin (p88, 1P90) in the biogenesis of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem., 269, 12784-12788.
39. Riordan,J.R. (1993) The cystic fibrosis transmembrane conductance regulator. Annu. Rev. Physiol., 55, 609-630.
40. Roussel,P. and Lamblin,G. (1996) Human mucosal mucins in diseases. In Montreuil,J., Vliegenthart,J.F.G. and Schachter, H. (eds.), Glycoproteins and Disease. Elsevier Science B. V., Amsterdam, pp. 351-393.
41. Roussel,P., Lamblin,G. and Degand,P. (1975) Heterogeneity of the carbohydrate chains of sulfated bronchial glycoproteins isolated from a patient suffering from cystic fibrosis. J. Biol. Chem., 250, 2114-2122.
42. Sasaki,K., Kurata,K., Nagata,M., Watanaba,E., Ohta,S., Hanai,N. and Nishi,T. (1995) Expression cloning of a novel α1,3-fucosyltransferase that is involved in biosynthesis of the sialyl Lewis x carbohydrate determinants in leukocytes. J. Biol. Chem., 269, 14730-14737.
43. Scudder,P.R., Shailubhai,K., Duffin,K.L., Streeter,P.R. and Jacob,G.S. (1994) Enzymatic synthesis of a 6′-sulphated sialyl-Lewis x which is an inhibitor of L-selectin binding to peripheral addressin. Glycobiology, 4, 929-932.
44. Shankar,V., Pichan,P., Eddy,R.L., Tonk,V., Nowak,N., Sait,S.N., Shows,T.B., Schultz,R.E., Gotway,G., Elkins,R.C., Gilmore,M.S. and Sachdev,G.P. (1997) Chromosomal localization of a human mucin gene (MUC8) and cloning of the cDNA corresponding to the carboxy terminus. Am. J. Respir. Cell Mol. Biol., 16, 232-241.
45. Spiro,R.G., Yasumoto,Y. and Bhoyroo,V. (1996) Characterization of a rat liver golgi sulphotransferase responsible for the 6-O-sulphation of N-acetylglucosamine residues in β-linkage to mannose: role in assembly of sialyl-galactosyl-N-acetylglucosamine 6-sulphate sequence of N-linked oligosaccharides. Biochem. J., 319, 209-216.
46. 13C-NMR assignments for sialylated oligosaccharide-alditols related to mucins. Study of thirteen components from hen ovomucin and swallow nest mucin. Biochimie (Paris), 74, 39-51.
47. Uchimura,K., Muramatsu,H., Kadomatsu,K., Fan,Q.W., Kurosawa,N., Mitsuoka,C., Kannagi,R., Habuchi,O. and Muramatsu,T. (1998a) Molecular cloning and characterization of an N-acetylglucosamine-6-O-sulfotransferase. J. Biol. Chem., 273, 22577-22583.
48. Uchimura,K., Muramatsu,H., Kaname,T., Ogawa,H., Yamakawa,T., Fan,Q.W., Mitsuoka,C., Kannagi,R., Habuchi,O., Yokoyama,I., Yamamura,Ki., Ozaki,T., Nakagawara,A., Kadomatsu,K. and Muramatsu,T. (1998b) Human N-acetylglucosamine-6-O-sulfotransferase involved in the biosynthesis of 6-sulfo sialyl Lewis x: molecular cloning, chromosomal mapping, and expression in various organs and tumor cells. J. Biochem. (Tokyo), 124, 670-678.
49. Van Kuik,J.A., Breg,J., Kolsteeg,C.E.M., Kamerling,J.P. and Vliegenthart,J.F.G. (1987) Primary structure of the acidic carbohydrate chain of hemocyanin from Panulirus interruphis. FEBS Lett., 221, 150-154.
50. Weston,B.W., Nair,R.P., Larsen,R.D. and Lowe,J.B. (1992a) Isolation of a novel haman α(1,3)fucosyltransferase gene and molecular comparison to the human Lewis blood group α(1,3/1,4)fucosyltransferase gene. Syntenic, homologous, nonallelic genes encoding enzymes with distinct acceptor substrate specificities. J. Biol. Chem., 267, 4152-4160.
51. Weston,B.W., Smith,P.L., Kelly,R.J. and Lowe,J.B. (1992b) Molecular cloning of a fouth member of a human α(1,3)fucosyltransferase gene family. Multiple homologous sequences that determine expression of the Lewis x, sialyl Lewis x, and difucosyl sialyl Lewis x epitopes. J. Biol. Chem., 267, 24575-24584.
52. Zhang,Y., Doranz,B., Yankaskas,J.R. and Engelhardt,J.F. (1995) Genotypic analysis of respiratory mucous sulfation defects in cystic fibrosis. J. Clin. Invest., 96, 2997-3004.