1887

Abstract

Infection by , which causes the life-threatening disease invasive aspergillosis, begins with the inhalation of conidia that adhere to and germinate in the lung. Previous studies have shown that conidia express high levels of the negatively charged 9-carbon sugar sialic acid, and that sialic acid appears to mediate the binding of conidia to basal lamina proteins. However, despite the ability of sialic acid to inhibit adherence of conidia, the exact mechanism by which this binding occurs remains unresolved. Utilizing various free sialic acids and other carbohydrates, sialic acid derivatives, sialoglycoconjugates, glycoproteins, -keto acid related compounds and amino acids we have found that the binding of conidia to type IV collagen and fibrinogen was inhibited by (i) glycoproteins (in a sialic acid-independent manner), and (ii) free sialic acids, glucuronic acid and -keto acid related compounds. However, inhibition by the latter was found to be the result of a shift in pH from neutral (pH 7.4) to acidic (less than pH 4.6) induced by the relatively high concentrations of free sialic acids, glucuronic acid and -keto acid related compounds used in the binding assays. This suggests that previous reports describing inhibition of conidia binding by free sialic acid may actually be due to a pH shift similar to that shown here. As previously reported, we found that conidia express only -acetylneuraminic acid, the most common sialic acid found in nature. However, appears to do so by an alternative mechanism to that seen in other organisms. We report here that (i) does not incorporate sialic acid obtained from the environment, (ii) does not synthesize and incorporate sialic acid from exogenous -acetylmannosamine, and (iii) lacks homologues of known sialic acid biosynthesizing enzymes.

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2009-09-01
2020-07-11
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References

  1. Alviano C. S., Travassos L. R., Schauer R.. 1999; Sialic acids in fungi: a minireview. Glycoconj J16:545–554
    [Google Scholar]
  2. Angata T., Varki A.. 2002; Chemical diversity in the sialic acids and related α-keto acids: an evolutionary perspective. Chem Rev102:439–469
    [Google Scholar]
  3. Arnaout M. A., Goodman S. L., Xiong J. P.. 2002; Coming to grips with integrin binding to ligands. Curr Opin Cell Biol14:641–651
    [Google Scholar]
  4. Bouchara J. P., Sanchez M., Chevailler A., Marotleblond A., Lissitzky J. C., Tronchin G., Chabasse D.. 1997; Sialic acid-dependent recognition of laminin and fibrinogen by Aspergillus fumigatus conidia. Infect Immun65:2717–2724
    [Google Scholar]
  5. Bromley I. M., Donaldson K.. 1996; Binding of Aspergillus fumigatus spores to lung epithelial cells and basement membrane proteins: relevance to the asthmatic lung. Thorax51:1203–1209
    [Google Scholar]
  6. Crocker P. R.. 2002; Siglecs: sialic-acid-binding immunoglobulin-like lectins in cell-cell interactions and signalling. Curr Opin Struct Biol12:609–615
    [Google Scholar]
  7. Denning D. W.. 1998; Invasive aspergillosis. Clin Infect Dis26:781–803
    [Google Scholar]
  8. Gil M. L., Penalver M. C., Lopez-Ribot J. L., O'Connor J. E., Martinez J. P.. 1996; Binding of extracellular matrix proteins to Aspergillus fumigatus conidia. Infect Immun64:5239–5247
    [Google Scholar]
  9. Hamilton A. J., Jeavons L., Youngchim S., Vanittanakom N., Hay R. J.. 1998; Sialic acid-dependent recognition of laminin by Penicillium marneffei conidia. Infect Immun66:6024–6026
    [Google Scholar]
  10. Hamilton A. J., Jeavons L., Youngchim S., Vanittanakom N.. 1999; Recognition of fibronectin by Penicillium marneffei conidia via a sialic acid-dependent process and its relationship to the interaction between conidia and laminin. Infect Immun67:5200–5205
    [Google Scholar]
  11. Hara S., Yamaguchi M., Takemori Y., Furuhata K., Ogura H., Nakamura M.. 1989; Determination of mono- O-acetylated N-acetylneuraminic acids in human and rat sera by fluorometric high-performance liquid chromatography. Anal Biochem179:162–166
    [Google Scholar]
  12. Hostetter M. K.. 1999; Integrin-like proteins in Candida spp. and other microorganisms. Fungal Genet Biol28:135–145
    [Google Scholar]
  13. Keppler O. T., Horstkorte R., Pawlita M., Schmidt C., Reutter W.. 2001; Biochemical engineering of the N-acyl side chain of sialic acid: biological implications. Glycobiology11:11R–18R
    [Google Scholar]
  14. Latge J. P.. 1999; Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev12:310–350
    [Google Scholar]
  15. Latge J. P.. 2001; The pathobiology of Aspergillus fumigatus. Trends Microbiol9:382–389
    [Google Scholar]
  16. Lehmann F., Tiralongo E., Tiralongo J.. 2006; Sialic acid-specific lectins: occurrence, specificity and function. Cell Mol Life Sci63:1331–1354
    [Google Scholar]
  17. Manavathu E. K., Abraham O. C., Chandrasekar P. H.. 2001; Isolation and in vitro susceptibility to amphotericin B, itraconazole and posaconazole of voriconazole-resistant laboratory isolates of Aspergillus fumigatus. Clin Microbiol Infect7:130–137
    [Google Scholar]
  18. Mawhinney T. P., Chance D. L.. 1994; Hydrolysis of sialic acids and O-acetylated sialic acids with propionic acid. Anal Biochem223:164–167
    [Google Scholar]
  19. Mosquera J., Denning D. W.. 2002; Azole cross-resistance in Aspergillus fumigatus. Antimicrob Agents Chemother46:556–557
    [Google Scholar]
  20. Penalver M. C., O'Connor J. E., Martinez J. P., Gil M. L.. 1996; Binding of human fibronectin to Aspergillus fumigatus conidia. Infect Immun64:1146–1153
    [Google Scholar]
  21. Pereira-Chioccola V. L., Schenkman S.. 1999; Biological role of Trypanosoma cruzi trans-sialidase. Biochem Soc Trans27:516–518
    [Google Scholar]
  22. Reuter G., Schauer R.. 1994; Determination of sialic acids. Methods Enzymol230:168–199
    [Google Scholar]
  23. Ringenberg M., Lichtensteiger C., Vimr E.. 2001; Redirection of sialic acid metabolism in genetically engineered Escherichia coli. Glycobiology11:533–539
    [Google Scholar]
  24. Rodrigues M. L., Rozental S., Couceiro J. N., Angluster J., Alviano C. S., Travassos L. R.. 1997; Identification of N-acetylneuraminic acid and its 9- O-acetylated derivative on the cell surface of Cryptococcus neoformans: influence on fungal phagocytosis. Infect Immun65:4937–4942
    [Google Scholar]
  25. Rodrigues M. L., Dobroff A. S., Couceiro J. N., Alviano C. S., Schauer R., Travassos L. R.. 2002; Sialylglycoconjugates and sialyltransferase activity in the fungus Cryptococcus neoformans. Glycoconj J19:165–173
    [Google Scholar]
  26. Schauer R., Kamerling J. P.. 1997; Chemisty, biochemistry and biology of sialic acids. In Glycoproteins II pp243–402 Edited by Montreuil J., Vliegenthart J. F. G., Schachter H. Amsterdam: Elsevier;
    [Google Scholar]
  27. Schilling B., Goon S., Samuels N. M., Gaucher S. P., Leary J. A., Bertozzi C. R., Gibson B. W.. 2001; Biosynthesis of sialylated lipooligosaccharides in Haemophilus ducreyi is dependent on exogenous sialic acid and not mannosamine. Incorporation studies using N-acylmannosamine analogues, N-glycolylneuraminic acid, and 13C-labeled N-acetylneuraminic acid. Biochemistry40:12666–12677
    [Google Scholar]
  28. Shen Y., Kohla G., Lrhorfi A. L., Sipos B., Kalthoff H., Gerwig G. J., Kamerling J. P., Schauer R., Tiralongo J.. 2004; O-Acetylation and de- O-acetylation of sialic acids in human colorectal carcinoma. Eur J Biochem271:281–290
    [Google Scholar]
  29. Soares R. M., Alviano C. S., Angluster J., Travassos L. R.. 1993; Identification of sialic acids on the cell surface of hyphae and yeast forms of the human pathogen Paracoccidioides brasiliensis. FEMS Microbiol Lett108:31–34
    [Google Scholar]
  30. Soares R. M. A., de A. Soares R. M., Alviano D. S., Angluster J., Alviano C. S., Travassos L. R.. 2000; Identification of sialic acids on the cell surface of Candida albicans Biochim Biophys Acta; 1474;262–268
    [Google Scholar]
  31. Stevens D. A., Kan V. L., Judson M. A., Morrison V. A., Dummer S., Denning D. W., Bennett J. E., Walsh T. J., Patterson T. F., Pankey G. A.. 2000; Practice guidelines for diseases caused by Aspergillus. Infectious Diseases Society of America. Clin Infect Dis30:696–709
    [Google Scholar]
  32. Tanner M. E.. 2005; The enzymes of sialic acid biosynthesis. Bioorg Chem33:216–228
    [Google Scholar]
  33. Tronchin G., Esnault K., Renier G., Filmon R., Chabasse D., Bouchara J. P.. 1997; Expression and identification of a laminin-binding protein in Aspergillus fumigatus conidia. Infect Immun65:9–15
    [Google Scholar]
  34. Tronchin G., Esnault K., Sanchez M., Larcher G., Marot-Leblond A., Bouchara J. P.. 2002; Purification and partial characterization of a 32-kilodalton sialic acid-specific lectin from Aspergillus fumigatus. Infect Immun70:6891–6895
    [Google Scholar]
  35. Varki A., Angata T.. 2006; Siglecs – the major subfamily of I-type lectins. Glycobiology16:1R–27R
    [Google Scholar]
  36. Vimr E. R., Kalivoda K. A., Deszo E. L., Steenbergen S. M.. 2004; Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev68:132–153
    [Google Scholar]
  37. Warris A., Weemaes C. M., Verweij P. E.. 2002; Multidrug resistance in Aspergillus fumigatus. N Engl J Med347:2173–2174
    [Google Scholar]
  38. Warwas M. L., Watson J. N., Bennet A. J., Moore M. M.. 2007; Structure and role of sialic acids on the surface of Aspergillus fumigatus conidiospores. Glycobiology17:401–410
    [Google Scholar]
  39. Wasylnka J. A., Moore M. M.. 2000; Adhesion of Aspergillus species to extracellular matrix proteins: evidence for involvement of negatively charged carbohydrates on the conidial surface. Infect Immun68:3377–3384
    [Google Scholar]
  40. Wasylnka J. A., Moore M. M.. 2002; Uptake of Aspergillus fumigatus conidia by phagocytic and nonphagocytic cells in vitro: quantitation using strains expressing green fluorescent protein. Infect Immun70:3156–3163
    [Google Scholar]
  41. Wasylnka J. A., Simmer M. I., Moore M. M.. 2001; Differences in sialic acid density in pathogenic and non-pathogenic Aspergillus species. Microbiology147:869–877
    [Google Scholar]
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