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. 1987 Oct;55(10):2364–2369. doi: 10.1128/iai.55.10.2364-2369.1987

Role of sialic acid in saliva-mediated aggregation of Pseudomonas aeruginosa isolated from cystic fibrosis patients.

K Komiyama 1, B F Habbick 1, S K Tumber 1
PMCID: PMC260714  PMID: 3115896

Abstract

The mechanism of saliva-mediated aggregation of Pseudomonas aeruginosa in subjects with and without cystic fibrosis (CF) was investigated. Virtually all saliva from CF patients that we tested strongly agglutinated the Pseudomonas cells and was heat stable to 56 degrees C, whereas saliva from subjects without CF had a decreased aggregating ability and was heat sensitive. When saliva was treated with neuraminidase and proteases, and also when P. aeruginosa cells were treated with mixed gangliosides, there was a decrease in aggregating activities. However, neither the addition of the acid-hydrolyzed ganglioside nor the treatment of the P. aeruginosa cells by sugars had any effect on subsequent aggregating activities. Therefore, the release of sialic acid by enzymatic treatments of saliva, as well as the blockage of the sialic acid-binding sites on the cell wall by mixed gangliosides, resulted in the parallel loss of saliva-mediated aggregating activity of P. aeruginosa. The level of free sialic acid released by endogenous neuraminidase was higher in the saliva from CF patients than in that from the non-CF subjects examined. The increased aggregation of P. aeruginosa mediated by saliva from patients with CF seems to be directly related to the sialic acid content present, suggesting that this acid molecule acts as the salivary receptor for P. aeruginosa.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ayars G. H., Altman L. C., Fretwell M. D. Effect of decreased salivation and pH on the adherence of Klebsiella species to human buccal epithelial cells. Infect Immun. 1982 Oct;38(1):179–182. doi: 10.1128/iai.38.1.179-182.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Beachey E. H. Bacterial adherence: adhesin-receptor interactions mediating the attachment of bacteria to mucosal surface. J Infect Dis. 1981 Mar;143(3):325–345. doi: 10.1093/infdis/143.3.325. [DOI] [PubMed] [Google Scholar]
  3. Bratthall D., Carlén A. Salivary agglutinin and secretory IgA reactions with oral streptococci. Scand J Dent Res. 1978 Dec;86(6):430–443. doi: 10.1111/j.1600-0722.1978.tb00650.x. [DOI] [PubMed] [Google Scholar]
  4. Diaz E., Mosovich L. L., Neter E. Serogroups of Pseudomonas aeruginosa and the immune response of patients with cystic fibrosis. J Infect Dis. 1970 Mar;121(3):269–274. doi: 10.1093/infdis/121.3.269. [DOI] [PubMed] [Google Scholar]
  5. Ellen R. P., Bratthall D., Borgström M., Howley T. P. Actinomyces viscosus and Actinomyces naeslundii agglutinins in human saliva. Scand J Dent Res. 1983 Aug;91(4):263–273. doi: 10.1111/j.1600-0722.1983.tb00815.x. [DOI] [PubMed] [Google Scholar]
  6. Ellen R. P., Fillery E. D., Seckington K. Infrequent polysaccharide cohesion among Actinomyces viscosus and Actinomyces naeslundii fresh isolates of human origin. J Periodontal Res. 1983 Jan;18(1):50–55. doi: 10.1111/j.1600-0765.1983.tb00334.x. [DOI] [PubMed] [Google Scholar]
  7. Gahnberg L., Olsson J., Krasse B., Carlén A. Interference of Salivary immunoglobulin A antibodies and other salivary fractions with adherence of Streptococcus mutans to hydroxyapatite. Infect Immun. 1982 Aug;37(2):401–406. doi: 10.1128/iai.37.2.401-406.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Golub E. E., Thaler M., Davis C., Malamud D. Bacterial aggregating activity in human saliva: simultaneous determination of free and bound cells. Infect Immun. 1979 Dec;26(3):1028–1034. doi: 10.1128/iai.26.3.1028-1034.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hoiby N. Pseudomonas aeruginosa infection in cystic fibrosis. Relationship between mucoid strains of Pseudomonas aeruginosa and the humoral immune response. Acta Pathol Microbiol Scand B Microbiol Immunol. 1974 Aug;82(4):551–558. [PubMed] [Google Scholar]
  10. Johanson W. G., Jr, Woods D. E., Chaudhuri T. Association of respiratory tract colonization with adherence of gram-negative bacilli to epithelial cells. J Infect Dis. 1979 Jun;139(6):667–673. doi: 10.1093/infdis/139.6.667. [DOI] [PubMed] [Google Scholar]
  11. Kashket S., Donaldson C. G. Saliva-induced aggregation of oral streptococci. J Bacteriol. 1972 Dec;112(3):1127–1133. doi: 10.1128/jb.112.3.1127-1133.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Komiyama K., Habbick B. F., Gibbons R. J. Interbacterial adhesion between Pseudomonas aeruginosa and indigenous oral bacteria isolated from patients with cystic fibrosis. Can J Microbiol. 1987 Jan;33(1):27–32. doi: 10.1139/m87-005. [DOI] [PubMed] [Google Scholar]
  13. Komiyama K., Habbick B. F., Martin T., Tumber S. K. Characterization by pyocine typing and serotyping of oral and sputum strains of Pseudomonas aeruginosa isolated from cystic fibrosis patients. Can J Microbiol. 1987 Mar;33(3):221–225. doi: 10.1139/m87-038. [DOI] [PubMed] [Google Scholar]
  14. Komiyama K., Tynan J. J., Habbick B. F., Duncan D. E., Liepert D. J. Pseudomonas aeruginosa in the oral cavity and sputum of patients with cystic fibrosis. Oral Surg Oral Med Oral Pathol. 1985 Jun;59(6):590–594. doi: 10.1016/0030-4220(85)90187-2. [DOI] [PubMed] [Google Scholar]
  15. Lam J., Chan R., Lam K., Costerton J. W. Production of mucoid microcolonies by Pseudomonas aeruginosa within infected lungs in cystic fibrosis. Infect Immun. 1980 May;28(2):546–556. doi: 10.1128/iai.28.2.546-556.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lamblin G., Boersma A., Klein A., Roussel P., van Halbeek H., Vliegenthart J. F. Primary structure determination of five sialylated oligosaccharides derived from bronchial mucus glycoproteins of patients suffering from cystic fibrosis. The occurrence of the NeuAc alpha(2----3)Gal beta(1----4)[Fuc alpha(1----3)] GlcNAc beta(1----.) structural element revealed by 500-MHz 1H NMR spectroscopy. J Biol Chem. 1984 Jul 25;259(14):9051–9058. [PubMed] [Google Scholar]
  17. Levine M. J., Herzberg M. C., Levine M. S., Ellison S. A., Stinson M. W., Li H. C., van Dyke T. Specificity of salivary-bacterial interactions: role of terminal sialic acid residues in the interaction of salivary glycoproteins with Streptococcus sanguis and Streptococcus mutans. Infect Immun. 1978 Jan;19(1):107–115. doi: 10.1128/iai.19.1.107-115.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Liljemark W. F., Bloomquist C. G., Ofstehage J. C. Aggregation and adherence of Streptococcus sanguis: role of human salivary immunoglobulin A. Infect Immun. 1979 Dec;26(3):1104–1110. doi: 10.1128/iai.26.3.1104-1110.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lindahl M., Faris A., Wadstrom T. Colonization factor antigen on enterotoxigenic Escherichia coli is a sialic-specific lectin. Lancet. 1982 Jul 31;2(8292):280–280. doi: 10.1016/s0140-6736(82)90368-3. [DOI] [PubMed] [Google Scholar]
  20. Lindemann R. A., Newman M. G., Kaufman A. K., Le T. V. Oral colonization and susceptibility testing of Pseudomonas aeruginosa oral isolates from cystic fibrosis patients. J Dent Res. 1985 Jan;64(1):54–57. doi: 10.1177/00220345850640011001. [DOI] [PubMed] [Google Scholar]
  21. Malamud D., Appelbaum B., Kline R., Golub E. E. Bacterial aggregating activity in human saliva: comparisons of bacterial species and strains. Infect Immun. 1981 Mar;31(3):1003–1006. doi: 10.1128/iai.31.3.1003-1006.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Marks M. I. The pathogenesis and treatment of pulmonary infections in patients with cystic fibrosis. J Pediatr. 1981 Feb;98(2):173–179. doi: 10.1016/s0022-3476(81)80631-2. [DOI] [PubMed] [Google Scholar]
  23. McBride B. C., Gisslow M. T. Role of sialic acid in saliva-induced aggregation of Streptococcus sanguis. Infect Immun. 1977 Oct;18(1):35–40. doi: 10.1128/iai.18.1.35-40.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pier G. B. Pulmonary disease associated with Pseudomonas aeruginosa in cystic fibrosis: current status of the host-bacterium interaction. J Infect Dis. 1985 Apr;151(4):575–580. doi: 10.1093/infdis/151.4.575. [DOI] [PubMed] [Google Scholar]
  25. Ramphal R., Pyle M. Adherence of mucoid and nonmucoid Pseudomonas aeruginosa to acid-injured tracheal epithelium. Infect Immun. 1983 Jul;41(1):345–351. doi: 10.1128/iai.41.1.345-351.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Ramphal R., Pyle M. Evidence for mucins and sialic acid as receptors for Pseudomonas aeruginosa in the lower respiratory tract. Infect Immun. 1983 Jul;41(1):339–344. doi: 10.1128/iai.41.1.339-344.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ramphal R., Pyle M. Further characterization of the tracheal receptor for Pseudomonas aeruginosa. Eur J Clin Microbiol. 1985 Apr;4(2):160–162. doi: 10.1007/BF02013590. [DOI] [PubMed] [Google Scholar]
  28. Ramphal R., Small P. M., Shands J. W., Jr, Fischlschweiger W., Small P. A., Jr Adherence of Pseudomonas aeruginosa to tracheal cells injured by influenza infection or by endotracheal intubation. Infect Immun. 1980 Feb;27(2):614–619. doi: 10.1128/iai.27.2.614-619.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Reddy M. S., Levine M. J., Prakobphol A. Oligosaccharide structures of the low-molecular-weight salivary mucin from a normal individual and one with cystic fibrosis. J Dent Res. 1985 Jan;64(1):33–36. doi: 10.1177/00220345850640010601. [DOI] [PubMed] [Google Scholar]
  30. Rosan B., Appelbaum B., Golub E., Malamud D., Mandel I. D. Enhanced saliva-mediated bacterial aggregation and decreased bacterial adhesion in caries-resistant versus caries-susceptible individuals. Infect Immun. 1982 Dec;38(3):1056–1059. doi: 10.1128/iai.38.3.1056-1059.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Rosan B., Malamud D., Appelbaum B., Golub E. Characteristic differences between saliva-dependent aggregation and adhesion of streptococci. Infect Immun. 1982 Jan;35(1):86–90. doi: 10.1128/iai.35.1.86-90.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Schloemer R. H., Wagner R. R. Sialoglycoprotein of vesicular stomatitis virus: role of the neuraminic acid in infection. J Virol. 1974 Aug;14(2):270–281. doi: 10.1128/jvi.14.2.270-281.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Sobeslavsky O., Prescott B., Chanock R. M. Adsorption of Mycoplasma pneumoniae to neuraminic acid receptors of various cells and possible role in virulence. J Bacteriol. 1968 Sep;96(3):695–705. doi: 10.1128/jb.96.3.695-705.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Valenti W. M., Trudell R. G., Bentley D. W. Factors predisposing to oropharyngeal colonization with gram-negative bacilli in the aged. N Engl J Med. 1978 May 18;298(20):1108–1111. doi: 10.1056/NEJM197805182982002. [DOI] [PubMed] [Google Scholar]
  35. WARREN L. The thiobarbituric acid assay of sialic acids. J Biol Chem. 1959 Aug;234(8):1971–1975. [PubMed] [Google Scholar]
  36. Weerkamp A. H., McBride B. C. Adherence of Streptococcus salivarius HB and HB-7 to oral surfaces and saliva-coated hydroxyapatite. Infect Immun. 1980 Oct;30(1):150–158. doi: 10.1128/iai.30.1.150-158.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wood R. E., Boat T. F., Doershuk C. F. Cystic fibrosis. Am Rev Respir Dis. 1976 Jun;113(6):833–878. doi: 10.1164/arrd.1976.113.6.833. [DOI] [PubMed] [Google Scholar]
  38. Woods D. E., Bass J. A., Johanson W. G., Jr, Straus D. C. Role of adherence in the pathogenesis of Pseudomonas aeruginosa lung infection in cystic fibrosis patients. Infect Immun. 1980 Dec;30(3):694–699. doi: 10.1128/iai.30.3.694-699.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Woods D. E., Straus D. C., Johanson W. G., Jr, Bass J. A. Role of fibronectin in the prevention of adherence of Pseudomonas aeruginosa to buccal cells. J Infect Dis. 1981 Jun;143(6):784–790. doi: 10.1093/infdis/143.6.784. [DOI] [PubMed] [Google Scholar]
  40. Woods D. E., Straus D. C., Johanson W. G., Jr, Berry V. K., Bass J. A. Role of pili in adherence of Pseudomonas aeruginosa to mammalian buccal epithelial cells. Infect Immun. 1980 Sep;29(3):1146–1151. doi: 10.1128/iai.29.3.1146-1151.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. van Heyningen W. E., Mellanby J. A note on the specific fixation, specific deactivation and non-specific inactivation of bacterial toxins by gangliosides. Naunyn Schmiedebergs Arch Pharmacol. 1973;276(3-4):297–302. doi: 10.1007/BF00499883. [DOI] [PubMed] [Google Scholar]

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