Glycoconjugate Journal

, Volume 16, Issue 9, pp 545–554 | Cite as

Sialic acids in fungi

  • Celuta S. Alviano
  • Luiz R. Travassos
  • Roland Schauer
Article

Abstract

The increasing number of reports on the presence of sialic acids in fungi (N-acetyl, N-glycolyl-and 5,9-N,O-diacetyl neuraminic acids) based on direct and indirect evidence warrants the present review. Formerly suggested as sialidase-sensitive sources of anionic groups at the cell surface of fungal species grown in chemically defined media (e.g., Fonsecaea pedrosoi), sialic acids have also been found in Sporothrix schenckii, Paracoccidioides brasiliensis, Cryptococcus neoformans and recently, in Candida albicans. Methods used involved adequate hydrolysis and extraction procedures, HTPLC, gas-chromatography, colorimetry, mass spectroscopy, sialidase-sensitive lectin and influenza virus binding. Apart from protecting fungal cells against phagocytosis (S. schenckii, C. neoformans) and playing a cellular structural role (F. pedrosoi), other biological functions of sialic acids are still being investigated.

fungi sialic acids anionic groups N-acetylneuraminic acid O-acetylated sialic acids fungal pathogenesis BSM, bovine sumandibular gland mucin CIH, colloidal iron hydroxide CMP, cytidine monophosphate EI, electron impact ER, endoplasmic reticulum FITC, fluorescein isothiocyanate Gal, Galactose GalNAc, N-acetyl-D-galactosamine GLC, Gas-liquid chromatography HPTLC, High-performance thin-layer chromatography LFA, Limax flavus agglutinin LPA, Limulus polyphemus agglutinin MAA, Maackia amurensis agglutinin MoAb, Monoclonal antibody MS, Mass-spectrometry Neu5Ac, N-Acetylneuraminic acid Neu5,9Ac2, 5-N-Acetyl-9-O-acetylneuraminic acid Neu5Gc, N-glycolylneuraminic acid PNA, peanut agglutinin SNA, Sambucus nigra agglutinin WGA, wheat germ agglutinin 

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References

  1. 1.
    Schauer R (1982) Chemistry,metabolism and biological functions of sialic acids. Adv Carbohydr Chem Biochem 40: 131–234.Google Scholar
  2. 2.
    Schauer R, Kamerling JP (1997) Chemistry, biochemistry and biology of sialic acids. In Glycoproteins II (Montreuil J, Vliegenthart JFG, Schachter H, eds) pp 243–402. Amsterdam: Elsevier.Google Scholar
  3. 3.
    Kelm S, Schauer R (1997) Sialic acids in molecular and cellular interactions. Int Rev Cytol 175: 137–240.Google Scholar
  4. 4.
    Harvey BE, Toth CA, Wagner HE, Stule GD Jr, Thomas P (1992) Sialyltransferase activity and hepatic tumor growth in a nude mouse model of colorectal cancer metastases. Cancer Res 52: 1775–79.Google Scholar
  5. 5.
    Miyagi T, Sato K, Hata K, Tamiguchi S (1994) Metastatic potential of transformed rat 3Y1 cell lines is inversely correlated with lysosomal-type sialidase activity. FEBS Lett 349: 255–59.Google Scholar
  6. 6.
    Varki A (1992) Diversity in the sialic acids.Glycobiology 2: 25–40.Google Scholar
  7. 7.
    Corfield AP, Schauer R (1982) Occurrence of sialic acids. In Sialic Acids—Chemistry, Metabolism and Function (Schauer R, ed) pp 5–50.Wien: Springer.Google Scholar
  8. 8.
    Kraub JH, Reuter G, Schauer R, Weckesser J, Mayer H (1988) Sialic acid-containing lipopolysaccharides of purple nonsulfur bacteria. Arch Microbiol 150: 584–89.Google Scholar
  9. 9.
    Alviano CS, Pereira MEA, Souza W, Oda LM, Travassos LR (1982) Sialic acids are surface components of Sporothrix schenckii yeast forms. FEMS Microbiol Lett 15: 223–27.Google Scholar
  10. 10.
    Oda LM, Kubelka CF, Alviano CS, Travassos LR (1983) Ingestion of yeast forms of Sporothrix schenckii by mouse peritoneal macrophages. Infect Immun 39: 497–504.Google Scholar
  11. 11.
    Hamilton AJ, Jeavons L, Hobby P, Hay RJ (1992)A34-to 38-kilodalton Cryptococcus neoformans glycoprotein produced as an exoantigen bearing a glycosylated species-specific epitope. Infect Immun 60: 143–49.Google Scholar
  12. 12.
    Rodrigues ML, Rozental S, Coceiro JNSS, Angluster J, Alviano CS, Travassos LR (1997)Indentification of N-acetylneuraminic acid and its 9-O-acetylated derivative on the cell surface of Cryptococcus neoformans: Influence on fungal phagocytosis. Infect Immun 65: 4937–42.Google Scholar
  13. 13.
    Souza ET, Silva-Filho FC, De Souza W, Alviano CS, Angluster J, Travassos LR (1986) Identification of sialic acids on the cell surface of hyphae and conidia of the human pathogen Fonsecaea pedrosoi. J Med Vet Mycol 24: 145–53.Google Scholar
  14. 14.
    Soares RMA, Alviano CS, Angluster J, Travassos LR (1993) Identification of sialic acids on the cell surface of hyphae and yeast forms of the human pathogen Paracoccidioides brasiliensis. FEMS Microbiol Lett 108: 31–4.Google Scholar
  15. 15.
    Soares RMA, Silva-Filho FC, Rozental S, Angluster J, De Souza W, Alviano CS, Travassos LR (1998) Anionogenic groups and surface sialoglycoconjugate structures of yeast forms of the human pathogen Paracoccidioides brasiliensis. Microbiology 144: 309–14.Google Scholar
  16. 16.
    Alaei S, Larcher C, Ebenbichler C, Prodinger WN, Janatova J, Dierich MP (1993) Isolation and biochemical characterization of the iC3b receptor of Candida albicans. Infect Immun 61: 1395–99.Google Scholar
  17. 17.
    Wadsworth E, Prasad SC, Calderone R (1993) Analysis of mannoproteins from blastoconidia and hyphae of Candida albicans with a common epitope recognized by anticomplement receptor type 2 antibodies. Infect Immun 61: 4675–81.Google Scholar
  18. 18.
    Jones L, Hobden C, O'shea P (1995) Use of a real-time fluorescent probe to study the electrostatic properties of the cell surface of Candida albicans.Mycol Res 99: 969–76.Google Scholar
  19. 18a.
    Soares RMA, Soares RMA, Alviano DS, Angluster J, Alviano CS, Travassos LR (2000) Identification of sialic acids on the cell surface of Candida albicans. Biochim Biophys Acta, in press.Google Scholar
  20. 19.
    Benhamou N, Ouellette GB (1987) Ultrastructural characterization of an extracellular fibrillar sheath on cells of Ascocalyx abietina, the scleroderris canker agent of conifers. Can J Bot 65: 154–67.Google Scholar
  21. 20.
    De Stefano JA, Cushion MT, Puvanesarajah V, Walzer PD (1990) Analysis of Pneumocystis carinii cyst wall. II. Sugar composition. J Protozool 37: 436–41.Google Scholar
  22. 21.
    De Stefano JA, Trinkle LS, Walzer PD, Cushion MT (1992) Flow cytometric analyses of lectin binding to Pneumocystis carinii surface carbohydrates. J Parasitol 78: 271–80.Google Scholar
  23. 22.
    Gasic GJ, Berwicz L, Sorrentino M (1968) Positive and negative colloidal iron as cell surface electron stains. Lab Invest 18: 63–71.Google Scholar
  24. 23.
    Burry RW, Wood JG (1979) Contributions of lipids and proteins to the surface charge of membranes. An electron microscopy study with cationized and anionized ferritin. J Cell Biol 82: 726–41.Google Scholar
  25. 24.
    Eylar EH, Maddoff MA, Brody OV, Oncley JL (1962) The contribution of sialic acid to the surface charge of the erythrocyte. J Biol Chem 237: 1992–200.Google Scholar
  26. 25.
    Furchgott RF, Ponder E (1941) Electrophoretic studies on human red blood cells. J Gen Physiol 24: 447–57.Google Scholar
  27. 26.
    Matta MAV, Alviano CS, Angluster J, De Souza W. Silva-Filho FC, Esteves MJG (1993) Surface charge and hydrophobicity of wild and mutant Crithidia fasciculata. Cell Bioph 20: 69–79.Google Scholar
  28. 27.
    James AM (1979) Molecular aspects of biological surfaces. Chem Soc Rev 8: 389–418.Google Scholar
  29. 28.
    Schauer R (1985) Sialic acids and their role as biological masks. Trends Biochem Sci 10: 357–60.Google Scholar
  30. 29.
    Benchimol M, De Souza W, Travassos LR (1979) Distribution of anionic groups at the cell surface of different Sporothrix schenckii cell types. Infect Immun 24: 912–19.Google Scholar
  31. 30.
    Nosanchuk JD, Casadevall A(1997) Cellular charge of Cryptococcus neoformans: contributions from the capsular polysaccharide, melanin, and monoclonal antibody binding. Infect Immun 65: 1836–41.Google Scholar
  32. 31.
    Sharon N, Lis H (1990) Legume lectins—a large family of homologous proteins. FASEB J 4: 3198–208.Google Scholar
  33. 32.
    Mandal C, Mandal C (1990) Sialic acid binding lectins. Experientia 46: 433–41.Google Scholar
  34. 33.
    Goldstein IJ, Poretz RD (1986) In The Lectins: Properties, Functions and Applications in Biology and Medicine (Liener IE, Sharon N, Goldstein LI, eds) pp 35–244. New York: Academic Press Inc.Google Scholar
  35. 34.
    Knibbs RN, Goldstein IJ, Ratcliffe RM, Shibuya N (1991) Characterization of the carbohydrate binding specificity of the leukoagglutinating lectin from Maackia amurensis. Comparison with other sialic acid-specific lectins. J Biol Chem 266: 83–8.Google Scholar
  36. 35.
    Couceiro JN, Paulson JC, Baum LG (1993) Influenza virus strains selectively recognize sialyloligosaccharides on human respiratory epithelium; the role of the host cell in selection of hemagglutinin receptor specificity. Virus Res 29: 155–65.Google Scholar
  37. 36.
    Lampio A (1988) Exposure of major glycolipids in human Pk and p erythrocytes. Glycoconj J 5: 513–20.Google Scholar
  38. 37.
    Varki A (1997) Sialic acids as ligands in recognition phenomena. FASEB J. 4: 248–55.Google Scholar
  39. 38.
    Muchmore EA, Varki A (1987) Selective inactivation of influenza C esterase: a probe for detecting 9-O-acetylated sialic acids. Science 236: 1293–95.Google Scholar
  40. 39.
    Rogers GN, Herrler G, Paulson JC, Klenk HD (1986) Influenza C virus uses 9-O-acetyl-N-acetylneuraminic acid as a high affinity receptor determinant for attachment to cells. J Biol Chem 261: 5947–51.Google Scholar
  41. 40.
    Zimmer G, Reuter G, Schauer R (1992) Use of influenza C virus Sialic acids in fungi 553 for detection of 9-O-acetylated sialic acids on immobilized glycoconjugates by esterase activity. Eur J Biochem 204: 209–15.Google Scholar
  42. 41.
    Matta MAV, Aleksitch V, Angluster J, Alviano CS, De Souza W, Andrade AFB, Esteves MJG (1995) Occurrence of N-acetyl-and N-O-diacetyl-neuraminic acid derivatives in wild and mutant Crithidia fasciculata. Parasitol Res 81: 426–33.Google Scholar
  43. 42.
    Ørskov F, Ørskov I, Sutton A, Schenckman R, Lin W, Egan W, Hoff GE, Robbins JB (1979) Form variation in Escherichia coli K1 determined by O-acetylation of the capsular polysaccharide. J Exp Med 152: 1375–92.Google Scholar
  44. 43.
    Varki A, Kornfeld S (1980) An autosomal dominant gene regulates the extent of 9-O-acetylation of murine erythrocyte sialic acids. A probable explanation for the variation in capacity to activate the human alternate complement pathway. J Exp Med 152: 532–44.Google Scholar
  45. 44.
    Schauer R, Kelm S, Reuter G, Roggentin P, Shaw L (1995) Chemistry and biology of sialic acids. In Biology of the Sialic Acids (Rosenberg A, ed) pp 7–67. New York: Plenum Press.Google Scholar
  46. 45.
    Varki A, Diaz S (1984) The release and purification of sialic acids from glycoconjugates: methods to minimize the loss and migration of O-acetyl groups. Anal Biochem 137: 236–47.Google Scholar
  47. 46.
    Reuter G, Schauer R (1994) Determination of sialic acids. Methods Enzymol 130: 168–99.Google Scholar
  48. 47.
    Engstler M, Reuter G, Schauer R (1992) Purification and characterization of a novel sialidase in procyclic culture forms of Trypanosoma brucei. Mol Biochem Parasitol 54: 21–30.Google Scholar
  49. 48.
    Warren, L (1959) The thiobarbituric acid assay of sialic acids. J Biol Chem 234: 1971–75.Google Scholar
  50. 49.
    Kornfeld R, Kornfeld S (1985) Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem. 54: 631–64.Google Scholar
  51. 50.
    Gemmill R, Trimble, RB (1999) Overview of N-and O-linked oligosaccharide structures found in various yeast species. Biochim Biophys Acta 1426: 227–37.Google Scholar
  52. 51.
    Fukazawa Y, Kagaya K, Shinoda T (1995) Cell wall polysaccharides of pathogenic yeasts. Curr Top Med Mycol 6: 189–219.Google Scholar
  53. 52.
    Gemmill TR, Trimble RB (1996) Schizosaccharomyces pombe produces novel pyruvate-containing N-linked oligosaccharides. J Biol Chem 271: 25945–49.Google Scholar
  54. 53.
    Schenkman S, Jiang MS, Hart GW, Nussenzweig V (1991) A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell 65: 1117–25.Google Scholar
  55. 54.
    Lee H, Kelm S, Michalski J-C, Schauer R (1990) Influence of sialic acids on the galactose-recognizing receptor of rat peritoneal macrophages. Biol Chem Hoppe-Seyler 371: 307–16.Google Scholar
  56. 55.
    Bratosin D, Mazurier J, Debray H, Lecocq M, Boilly B, Alonso C, Moisei M, Motas C, Montreuil J (1995) Flow cytofluorimetric analysis of young and senescent human erythrocytes probed with lectins.Evidence that sialic acids control their life span. Glycoconjugate J 12: 258–67.Google Scholar
  57. 56.
    Wickes BL, Mayorga ME, Edman U, Edman JC (1996) Dimorphism and haploid fruiting in Cryptococcus neoformans: association with the a-mating type. Proc Natl Acad Sci USA 93: 7327–31.Google Scholar
  58. 57.
    Ahmad F, McPhie P (1980) The intrinsic viscosity of glycoproteins. Int J Biochem 11: 91–6.Google Scholar
  59. 58.
    Bouali A, Robert R, Tronchim G, Senet JM (1987) Characterization of binding of hyman fibrinogen to the surface of germtubes and mycelium of Candida albicans. J Gen Microbiol 133: 545–51.Google Scholar
  60. 59.
    Bouchara JP, Tronchin G, Annaix V, Robert R, Senet JM (1990) Laminin receptors on Candida albicans germ tubes. Infect Immun 58: 48–54.Google Scholar
  61. 60.
    Tronchin G, Bouchara JP, Robert R, Senet JM (1988) Adherence of Candida albicans germ tubes to plastic: ultrastructural and molecular studies of fibrillar adhesins. Infect Immun 56: 1987–1993.Google Scholar

Copyright information

© Kluwer Academic Publishers 1999

Authors and Affiliations

  • Celuta S. Alviano
    • 1
  • Luiz R. Travassos
    • 2
  • Roland Schauer
    • 3
  1. 1.Instituto de Microbiologia Professor Paulo de GóesUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Disciplina de Biologia CelularUniversidade Federal de São PauloSão PauloBrazil
  3. 3.Biochemisches InstitutChristian-Albrechts-UniversitäKielGermany

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