1887

Abstract

is a key player in the pathology and morbidity of cystic fibrosis. Chronic obstructive pulmonary disease, which results from the most common and severe mutations in this genetic disorder, typically includes chronic infection with which, even with rugged antibiotic and physical therapy regimens, is rarely eradicated. It is not known whether the increased oligosaccharide sulfation characteristic of cystic fibrosis tracheobronchial mucins plays a role in the survival of in the airway. In this study, sulfated monosaccharides were synthesized and tested for their effects on the growth of clinical isolates and laboratory strains of this organism when supplied as the sole carbon source . Carbohydrate sulfation was observed to reduce, but not prohibit, growth of on carbohydrates normally utilized in their nonsulfated form. The various sulfated sugars employed as the sole carbon source gave characteristic and consistent growth profiles and maximum growth values across the strains tested. isolates from patients with cystic fibrosis often express a mucoid phenotype, which is thought to contribute to their ability to survive in harsh conditions. Carbohydrate sulfation effects on growth did not differ significantly between mucoid and nonmucoid strains. These results suggest that the additional sulfation of tracheobronchial mucin documented in cystic fibrosis may in fact contribute to the mucin’s resistance to utilization by and potentially other pathogens, providing an additional level of host protection, and limiting the available nutrient pool and thereby bacterial growth.

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2000-07-01
2019-10-19
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References

  1. Amerongen, A. V. N., Bolscher, J. G. M., Bloemena, E. & Veerman, E. C. O. ( 1998; ). Sulfomucins in the human body. Biol Chem 379, 1-18.[CrossRef]
    [Google Scholar]
  2. Ball, D. H. ( 1966; ). Preparation and some reactions of monoethylidene derivatives of d-galactose, methyl α- and β-d-galactopyranosides, and of d-threose. J Org Chem 31, 220-223.[CrossRef]
    [Google Scholar]
  3. Ball, D. H. & Jones, J. K. N. ( 1958; ). A synthesis of 3-O-β-d-galactopyranosyl-d-galactose. J Chem Soc 905–907.
    [Google Scholar]
  4. Boat, T. F., Cheng, P. W., Iyer, R. N., Carlson, D. M. & Polony, I. ( 1976; ). Human respiratory tract secretions. Mucous glycoproteins of nonpurulent tracheobronchial secretions, and sputum of patients with bronchitis and cystic fibrosis. Arch Biochem Biophys 177, 95-104.[CrossRef]
    [Google Scholar]
  5. Bocker, T., Lindhorst, T. K., Thiem, J. & Vill, V. ( 1992; ). Synthesis and properties of sulfated alkyl glycosides. Carbohydr Res 230, 245-256.[CrossRef]
    [Google Scholar]
  6. Buret, A. & Cripps, A. W. ( 1993; ). The immunoevasive activities of Pseudomonas aeruginosa. Relevance for cystic fibrosis. Am Rev Respir Dis 148, 793-805.[CrossRef]
    [Google Scholar]
  7. Chace, K. C., Leahy, D. S., Martin, R., Carubelli, R., Flux, M. & Sachdev, G. P. ( 1983; ). Respiratory mucous secretions in patients with cystic fibrosis: relationship between levels of highly sulfated mucin component and severity of the disease. Clinica Chimica Acta 132, 143-155.[CrossRef]
    [Google Scholar]
  8. Chance, D. L. & Mawhinney, T. P. ( 1996; ). Disulfated oligosaccharides derived from tracheobronchial mucous glycoproteins of a patient suffering from cystic fibrosis. Carbohydr Res 295, 157-177.[CrossRef]
    [Google Scholar]
  9. Cheng, P. W., Boat, T. F., Cranfill, K., Yankaskas, J. R. & Boucher, R. C. ( 1989; ). Increased sulfation of glycoconjugates by cultured nasal epithelial cells from patients with cystic fibrosis. J Clin Invest 84, 68-72.[CrossRef]
    [Google Scholar]
  10. Clarke, P. & Slater, J. H. ( 1986; ). Evolution of enzyme structure and function in Pseudomonas. In The Bacteria: A Treatise on Structure and Function, vol. X, The Biology of Pseudomonas, pp. 71-143. Edited by J. R. Sokatch. New York: Academic Press.
  11. Cybulski, Z., Michalska, W. & Pietkiewicz, K. ( 1993; ). Epidemiological estimation of Pseudomonas aeruginosa strains isolated from different environments. Acta Microbiol Pol 42, 259-65.
    [Google Scholar]
  12. Davril, M., Degroote, S., Humbert, P., Galabert, C., Dumur, V., Lafitte, J.-J., Lamblin, G. & 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.[CrossRef]
    [Google Scholar]
  13. Fitzgerald, J. W. & Dodgson, K. S. ( 1971a; ). Sulphur utilization during growth of Pseudomonas fluorescens on potassium d-glucose-6-O-sulfate. Biochem J 121, 521-528.
    [Google Scholar]
  14. Fitzgerald, J. W. & Dodgson, K. S. ( 1971b; ). Carbon and sulphur utilization during growth of Pseudomonas fluorescens on potassium d-glucose-6-O-sulfate as the sole sulphur source. Biochem J 122, 277-283.
    [Google Scholar]
  15. Gerken, T. A. & Gupta, R. ( 1993; ). Mucus in cystic fibrosis. In Cystic Fibrosis, pp. 53-90. Edited by P. B. Davis. New York: Marcel Dekker.
  16. Gupta, R. & Jentoft, N. ( 1992; ). The structure of tracheobronchial mucins from cystic fibrosis and control patients. J Biol Chem 267, 3160-3167.
    [Google Scholar]
  17. Holloway, B. W., Krishnapillai, V. & Morgan, A. F. ( 1979; ). Chromosomal genetics of Pseudomonas. Microbiol Rev 43, 73-102.
    [Google Scholar]
  18. Jansen, H. J., Hart, C. A., Rhodes, J. M., Saunders, J. R. & Smalley, J. W. ( 1999; ). A novel mucin-sulphatase activity found in Burkholderia cepacia and Pseudomonas aeruginosa. J Med Microbiol 48, 551-557.[CrossRef]
    [Google Scholar]
  19. Koneman, E. W., Allen, S. D., Janda, W. M., Schreckenberger, P. C. & Winn, W. C., Jr (1992). Color Atlas and Textbook of Diagnostic Microbiology, 4th edn. Philadelphia: J. B. Lippincott.
  20. Lloyd, A. G. ( 1960; ). Studies on sulphatases: preparation of substrates for the assay of glycosulphatase. Biochem J 75, 478-482.
    [Google Scholar]
  21. Loutit, J. S. & Tompkins, L. S. ( 1991; ). Restriction enzyme and Southern hybridization analyses of Pseudomonas aeruginosa strains from patients with cystic fibrosis. J Clin Microbiol 29, 2897-2900.
    [Google Scholar]
  22. Mawhinney, T. P. & Chance, D. L. ( 1994; ). Structural elucidation by fast atom bombardment mass spectrometry of multisulfated oligosaccharides isolated from human respiratory mucous glycoproteins. J Carbohydr Chem 13, 825-840.[CrossRef]
    [Google Scholar]
  23. Mawhinney, T. P., Adelstein, E., Morris, D. A., Mawhinney, A. M. & Barbero, G. J. ( 1987; ). Structure determination of five sulfated oligosaccharides derived from tracheobronchial mucus glycoprotein. J Biol Chem 262, 2994-3001.
    [Google Scholar]
  24. Mawhinney, T. P., Adelstein, E., Gayer, D. A., Landrum, D. C. & Barbero, G. J. ( 1992a; ). Structural analysis of monosulfated side-chain oligosaccharides isolated from human tracheobronchial mucous glycoproteins. Carbohydr Res 223, 187-207.[CrossRef]
    [Google Scholar]
  25. Mawhinney, T. P., Landrum, D. C., Gayer, D. A. & Barbero, G. J. ( 1992b; ). Sulfated sialyl-oligosaccharides derived from tracheobronchial mucous glycoproteins of a patient suffering from cystic fibrosis. Carbohydr Res 235, 179-197.[CrossRef]
    [Google Scholar]
  26. Nelson, J. W., Tredgett, M. W., Sheenhan, J. K., Thornton, D. J., Notman, D. & Govan, J. R. W. ( 1990; ). Mucinophilic and chemotactic properties of Pseudomonas aeruginosa in relation to pulmonary colonization with cystic fibrosis. Infect Immun 58, 1489-1495.
    [Google Scholar]
  27. Prizont, R. & Reed, W. ( 1991; ). Differences in blood group B-specific mucinase activity between virulent and avirulent Shigella flexneri 2a strains. Microb Pathog 11, 129-135.[CrossRef]
    [Google Scholar]
  28. Roussel, P., Lamblin, G., Degrand, P., Walker-Nasir, E. & Jeanloz, R. W. ( 1975; ). Heterogeneity of carbohydrate chains of sulfated bronchial glycoproteins isolated from a patient suffering from cystic fibrosis. J Biol Chem 250, 2114-2118.
    [Google Scholar]
  29. Scharfman, A., Van Brussel, E., Houdret, N., Lamblin, G. & Roussel, P. ( 1996; ). Interactions between glycoconjugates from human respiratory airways and Pseudomonas aeruginosa. Am J Respir Crit Care Med 154, S163-169.[CrossRef]
    [Google Scholar]
  30. Schneider, D. R. & Parker, C. D. ( 1982; ). Purification and characterization of the mucinase of Vibrio cholerae. J Infect Dis 145, 474-482.[CrossRef]
    [Google Scholar]
  31. Slomiany, B. L., Murty, V. L., Piotrowski, J., Liau, Y. H., Sundaram, P. & Slomiany, A. ( 1992; ). Glycosulfatase activity of Helicobacter pylori toward gastric mucin. Biochem Biophys Res Commun 183, 506-513.[CrossRef]
    [Google Scholar]
  32. Slomiany, B. L., Murty, V. L., Piotrowski, J., Liau, Y. H. & Slomiany, A. ( 1993; ). Glycosulfatase activity of Porphyromonas gingivalis a bacterium associated with periodontal disease. Biochem Mol Biol Int 29, 973-980.
    [Google Scholar]
  33. Smith, A. W., Chahal, B. & French, G. L. ( 1994; ). The human gastric pathogen Helicobacter pylori has a gene encoding an enzyme first classified as a mucinase in Vibrio cholerae. Mol Microbiol 13, 153-160.[CrossRef]
    [Google Scholar]
  34. Tally, E. A. ( 1963; ). The Koenigs–Knorr reaction for disaccharide synthesis. Methods Carbohydr Chem 2, 337-340.
    [Google Scholar]
  35. Vieu, J. F., Lepers, J. P., Chamoiseau, G., Billon, C. & Klein, B. ( 1987; ). Epidemiology of Pseudomonas aeruginosa in Mauritania: study of 239 strains of various origins. Bull Soc Pathol Exot Filiales 80, 771–780 (in French).
    [Google Scholar]
  36. Voelker, D. H. & Orton, P. Z. (1993). Univariate inferential tests. In Cliffs Quick Review Statistics, pp. 85–108. Lincoln, NE: Cliffs Notes.
  37. Whistler, R. L., Spencer, W. W. & BeMiller, J. N. ( 1963; ). Sulfates, d-glucose 3-sulfate and 6-sulfate. In Methods in Carbohydrate Chemistry, vol. II, Reactions of Carbohydrates, pp. 298-303. Edited by R. L. Whistler & M. L. Wolfrom. New York: Academic Press.
  38. Widdicombe, J. ( 1995; ). Relationships among the composition of mucus, epithelial lining liquid, and adhesion of microorganisms. Am J Respir Crit Care Med 151, 2088-2093.[CrossRef]
    [Google Scholar]
  39. Woodward, H., Horsey, B., Bhavanadan, V. P. & Davidson, E. A. ( 1982; ). Isolation, purification, and properties of respiratory mucus glycoproteins. Biochemistry 21, 694-701.[CrossRef]
    [Google Scholar]
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