Skip to main content
SpringerLink
Log in

Differential expression of sialylglycoconjugates and sialidase activity in distinct morphological stages of Fonsecaea pedrosoi

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

The expression of sialoglycoconjugates in Fonsecaea pedrosoi conidia, mycelia, and sclerotic cells was analyzed using influenza A and C virus strains, sialidase treatment, and lectin binding. Conidium and mycelium whole cells were recognized by Limax flavus (LFA), Maackia amurensis (MAA), and Sambucus nigra (SNA) lectins, denoting the presence of surface sialoglycoconjugates containing α2,3- and α2,6-sialylgalactosyl sequences. Sialidase-treated conidia reacted more intensively with peanut agglutinin (PNA), confirming the occurrence of sialyl-galactosyl linkages. Conidial cells agglutinated in the presence of influenza A and C virus strains, which confirmed the results obtained from lectin-binding experiments and revealed the presence of sialoglycoconjugates bearing 9-O-acetyl-N-acetylneuraminic acid (Neu5,9Ac2) surface structures. Western blotting analysis with peroxidase-labeled LFA demonstrated the occurrence of sialylglycoproteins in protein extracts from conidia and mycelia, with molecular masses corresponding to 56 and 40 kDa. An additional band of 77 kDa was detected in conidial extracts, suggesting an association between sialic acid expression and morphogenesis. Synthesis of sialic acids was correlated with sialidase expression, since both conidial and mycelial morphological stages presented secreted and cell-associated enzyme activity. Sialoglycoconjugates were not detected in F. pedrosoi sclerotic cells from in vitro and in vivo sources, which also do not express sialidase activity. The surface sialyl residues in F. pedrosoi are apparently involved in the fungal interaction with immune effector cells, since sialidase-treated conidia were less resistant to phagocytosis by human neutrophils from healthy individuals. These findings suggest that sialic acid expression in F. pedrosoi varies according to the morphological transition and may protect infecting propagules against immune destruction by host cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1a–h
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • 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 61:1395–1399

    CAS  PubMed  Google Scholar 

  • Alviano CS, Pereira MEA, De Souza W, Oda LM, Travassos LR (1982) Sialic acids are surface components of Sporothrix schenckii yeast forms. FEMS Microbiol Lett 15:223–227

    Article  CAS  Google Scholar 

  • Alviano CS, Farbiarz SR, De Souza W, Angluster J, Travassos LR (1991) Characterization of Fonsecaea pedrosoi melanin. J Gen Microbiol 137:837–844

    CAS  PubMed  Google Scholar 

  • Alviano CS, Travassos LR, Angluster J, de Souza W (1992) Effect of environmental factors on Fonsecaea pedrosoi morphogenesis with emphasis on sclerotic cells induced by propranolol. Mycopathologia 119:17–23

    CAS  PubMed  Google Scholar 

  • Alviano CS, Travassos LR, Schauer R (1999) Sialic acids in fungi: a minireview. Glycoconj J 16:545–554

    CAS  PubMed  Google Scholar 

  • Alviano DS, Kneipp LF, Lopes AH, Travassos LR, Meyer-Fernandes JR, Rodrigues ML, Alviano CS (2003). Differentiation of Fonsecaea pedrosoi mycelial forms into sclerotic cells is induced by platelet-activating factor. Res Microbiol 154:689–695.

    Article  CAS  PubMed  Google Scholar 

  • Angata T, Varki A (2002) Chemical diversity in the sialic acids and related α-keto acids: An evolutionary perspective. Chem Rev 102:439–469

    Article  CAS  PubMed  Google Scholar 

  • Arduino RC, Jacques-Palaz K, Murray BE, Rakita RM (1994) Resistance of Enterococcus faecium to neutrophil-mediated phagocytosis. Infect Immun 62:5587–5594

    CAS  PubMed  Google Scholar 

  • Bouali A, Robert R, Tronchin G, Senet JM (1987) Characterization of binding of human fibrinogen to the surface of germ tubes and mycelium of Candida albicans. J Gen Microbiol 133:545–551

    CAS  PubMed  Google Scholar 

  • Bouchara JP, Tronchin G, Annaix V, Robert R, Senet JM (1990) Laminin receptors on Candida albicans germ tubes. Infect Immun 58:48–54

    CAS  PubMed  Google Scholar 

  • Butterfield W, Jong SC (1987) Effect of carbon source on conidiogenesis in Fonsecaea dermatitidis, agent of chromomycosis. Mycopathologia 58:59–62

    Google Scholar 

  • Castro LGM, Pimentel ERA, Lacaz CS (2003) Treatment of chromoblastomycosis by cryosurgery with liquid nitrogen: 15 years’experience. Int J Dermatol 42:408–412

    Article  PubMed  Google Scholar 

  • Couceiro JNSS, 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 29:155–165

    Article  CAS  PubMed  Google Scholar 

  • Esquenazi D, Rozental S, Alviano CS, Travassos LR, Schauer R (2003) Sialic acids are absent from the dermatophytes Trichophyton mentagrophytes and Trichophyton rubrum. Mycoses 46:1–6

    Article  PubMed  Google Scholar 

  • Esterre P, Peyrol S, Sainte-Marie D, Pradinaud R, Grimaud JA (1993) Granulomatous reaction and tissue remodeling in the cutaneous lesion of chromoblastomycosis. Virchows Archiv A Patho Anat 422:285–291

    CAS  Google Scholar 

  • Farbiarz SR, De Carvalho TU, Alviano CS, De Souza W (1990) Fine structure and cytochemistry of the interaction between Fonsecaea pedrosoi and mouse resident macrophages. J Med Vet Mycol 28:373–383

    CAS  PubMed  Google Scholar 

  • Farbiarz SR, Carvalho TU, Alviano CS, De Souza W (1992) Inhibitory effect of melanin on the interaction of Fonsecaea pedrosoi with mammalian cells in vitro. J Med Vet Mycol 30:265–273

    CAS  PubMed  Google Scholar 

  • Hamilton AJ, Jeavons L, Hobby P, Hay RJ (1992) A 34 to 38 kilodalton Cryptococcus neoformans glycoprotein produced as an exoantigen bearing a glycosylated species-specific epitope. Infect Immun 60:143–149

    CAS  PubMed  Google Scholar 

  • Hamza SH, Mercado PJ, Skelton HG, Smith KJ (2003) An unusual dematiaceous fungal infection of the skin caused by Fonsecaea pedrosoi: a case report and review of the literature. J Cutan Pathol 30:340–343

    Article  PubMed  Google Scholar 

  • Hulb U, Ishida H, Kiso M, Hasegawa A, Schauer R (2000) Studies on the specificity and sensitivity of the Influenza C virus binding assay for 9-O-acetylated sialic acids and its application to human melanomas. J Biochem 127:1021–1031

    PubMed  Google Scholar 

  • Jedrzejas MJ (2001) Pneumococcal virulence factors: structure and function. Microbiol Mol Biol Rev 65:187–207

    Article  CAS  PubMed  Google Scholar 

  • Jost BH, Songer JG, Billington SJ (2001) Cloning, expression, and characterization of a neuraminidase gene from Arcanobacterium pyogenes. Infect Immun 69:4430–4437

    Article  CAS  PubMed  Google Scholar 

  • Krug G, Roggentin P, Schauer R, Brasch J (1997) Dermatophyten bilden in vitro keine sialidase. Mycoses 40:17–21

    CAS  Google Scholar 

  • Kwon-Chung KJ, Bennet JE (1992) Chromoblastomycosis. In: Medical Mycology. Lea & Febiger, Philadelphia, pp 337–355

  • Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685

    PubMed  Google Scholar 

  • Limongi CL, Alviano CS, De Souza W, Rozental S (2001) Isolation and partial characterization of an adhesin from Fonsecaea pedrosoi. Med Mycol 39:429–437

    CAS  PubMed  Google Scholar 

  • Lowry OH, Rosebrogh NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  Google Scholar 

  • McGinnis MR, Hilger EA (1987) Infections caused by black fungi. Arch Dermatol 123:1300–1302

    Article  CAS  PubMed  Google Scholar 

  • Mendoza L, Karuppayil SM, Szaniszlo PJ (1993) Calcium regulates in vitro dimorphism in chromoblastomycotic fungi. Mycoses 36:157–164

    CAS  PubMed  Google Scholar 

  • Oda LM, Kubelka CF, Alviano CS, Travassos LR (1983) Ingestion of yeast forms of Sporotrix schenckii by mouse peritoneal macrophages. Infect Immun 39:497–504

    CAS  PubMed  Google Scholar 

  • Oliveira LG, Resende MA, Lopes CF, Cisalpino EO (1973) Isolamento e identificação dos agentes da cromomicose em Belo Horizonte. Rev Soc Bras Med Trop 7:1 (in Portuguese).

    Google Scholar 

  • Orskov F, Orskov I, Sutton A, Schenckman R, Lin W, Egan W, Hoff EG, Robbins JB (1979) Form variation in Escherichia coli K1 determined by O-acetylation of the capsular polysaccharide. J Exp Med 152:1375–1392

    Google Scholar 

  • Potier M, Mameli L, Bélisle M, Dallaire L, Melançon SB (1979) Fluorometric assay of neuraminidase with a sodium (4-methylumbelliferyl-α-D-N-acetylneuraminate) substrate. Anal Biochem 94:287–296

    CAS  PubMed  Google Scholar 

  • Reuter G, Schauer R (1994) Determination of sialic acids. Methods Enzymol 230:168–199

    CAS  PubMed  Google Scholar 

  • Rivitti EA, Aoki V (1999) Deep fungal infections in tropical countries. Clin Dermatol 17:171–190

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues ML, Rozental S, Couceiro JNSS, Angluster J, Alviano CS, Travassos LR (1997) Identification of N-acetylneuraminic acid and its 9-O-acetylated derivative on the cell surface of Cryptococcus neoformans: influence on fungal phagocytosis. Infect Immun 65:4937–4942

    CAS  PubMed  Google Scholar 

  • Rodrigues ML, Alviano CS, Travassos LR (1999) Pathogenicity of Cryptococcus neoformans: virulence factors and immunological mechanisms. Microbes Infect 1:293–301

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues ML, Dobroff ASS, Couceiro JNSS, Alviano CS, Schauer R, Travassos LR (2003) Sialylglycoconjugates and sialyltransferases activity in the fungus Cryptococcus neoformans. Glycoconjugate J 19:165–173

    Article  Google Scholar 

  • Rogers GN, Herrier G, Paulson JC, Klenk HD (1986) Influenza C virus uses 9-O-acetylneuraminic as a high affinity receptor determinant for attachment to cells. J Biol Chem 261:5947–5951

    CAS  PubMed  Google Scholar 

  • Roggentin P, Krug G, Schauer R, Brasch J (1999) Lack of sialidase activity in Candida albicans and Candida glabrata. Mycoses 42:33–36

    Article  CAS  Google Scholar 

  • Rosen T, Overholt M (1996) Persistent viability of the medlar body. Int J Dermatol 35:96–98

    CAS  PubMed  Google Scholar 

  • Royal GC Jr, Nandedkar AK, Sampson CC, Faggett T (1984) Neuraminidase production by Candida albicans. J Natl Med Assoc 76:143–145

    CAS  PubMed  Google Scholar 

  • Rozental S, Alviano CS, De Souza W (1996) Fine structure and cytochemical study of the interaction between Fonsecaea pedrosoi and rat polymorphonuclear leukocyte. J Med Vet Mycol 34:323–330

    CAS  PubMed  Google Scholar 

  • Schauer R, Kamerling JP (1997) Chemistry, biochemistry and biology of sialic acids. In: Montreuil J, Vliegenthart JFG, Schachter H (eds) Glycoproteins II, vol 29b. New Comprehensive Biochemistry, Elsevier Science, Amsterdam, pp 243–402

  • Schnitzler N, Peltroche-Llacsahuanga H, Bestier N, Zündorf J, Lütticken R, Haase G (1999) Effect of melanin and carotenoids of Exophiala (Wangiella) dermatitidis on phagocytosis, oxidative burst, and killing by human neutrophils. Infect Immun 67:94–101

    CAS  PubMed  Google Scholar 

  • Silva JP, de Souza W, Rozental S (1999) Chromoblastomycosis: a retrospective study of 325 cases on Amazonic region (Brazil). Mycopathologia 143:171–175

    Article  CAS  Google Scholar 

  • Silva JP, Alviano DS, Alviano CS, De Souza W, Travassos LR, Diniz JAP, Rozental S (2002) Comparison of Fonsecaea pedrosoi sclerotic cells obtained in vivo and in vitro: ultrastructure and antigenicity. FEMS Immunol Med Microbiol 33:63–69

    Article  PubMed  Google Scholar 

  • Soares RMA, Angluster J, de Souza W, Alviano CS (1995) Carbohydrate and lipid components of hyphae and conidia of human pathogen Fonsecaea pedrosoi. Mycopathologia 132:71–77

    CAS  PubMed  Google Scholar 

  • Soares RMA, Costa e Silva-Filho F, 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 144:309–314

    CAS  PubMed  Google Scholar 

  • Soares RMA, Soares RMA, Alviano DS, Angluster J, De Souza W, Alviano CS, Travassos lr (2000) Identification of sialic acids on the cell surface of Candida albicans. Biochim Biophys Acta 1474:262–268

    Article  CAS  PubMed  Google Scholar 

  • 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 24:145–153

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Uchida Y, Tsukada Y, Sugimori T (1974) Production of microbial neuraminidases induced by colominic acid. Biochim Biophys Acta 350:425–431

    Article  CAS  PubMed  Google Scholar 

  • 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 61:4675–4681

    CAS  PubMed  Google Scholar 

  • Warren L (1959) The thiobarbituric assay of sialic acids. J Biol Chem 234:1971–1975

    CAS  PubMed  Google Scholar 

  • Wasylnka JA, Simmer MI, Moore MM (2001) Differences in sialic acid density in pathogenic and non-pathogenic Aspergillus species. Microbiology 147:869–877

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank Fátima Regina de Vasconcelos Goulart for technical assistance. This work was supported by Programa de Apoio a Núcleos de Excelência (PRONEX), Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ), Fundação Universitária José Bonifácio (FUJB) and Fundação Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES).

Author information

Authors and Affiliations

  1. Instituto de Microbiologia Professor Paulo de Góes, Universidade Federal do Rio de Janeiro, Centro de Ciências da Saúde-Bloco I, Ilha do Fundão, 21941-590, Rio de Janeiro, RJ, Brazil

    Daniela S. Alviano, Marcio L. Rodrigues, Catia A. Almeida, André L. S. Santos, José N. S. S. Couceiro, Rosangela M. A. Soares & Celuta S. Alviano

  2. Disciplina de Biologia Celular, Universidade Federal de São Paulo, 04023–062, São Paulo, SP, Brazil

    Luiz R. Travassos

Authors
  1. Daniela S. Alviano
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marcio L. Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Catia A. Almeida
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. André L. S. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José N. S. S. Couceiro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Rosangela M. A. Soares
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luiz R. Travassos
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Celuta S. Alviano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Celuta S. Alviano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alviano, D.S., Rodrigues, M.L., Almeida, C.A. et al. Differential expression of sialylglycoconjugates and sialidase activity in distinct morphological stages of Fonsecaea pedrosoi . Arch Microbiol 181, 278–286 (2004). https://doi.org/10.1007/s00203-004-0653-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-004-0653-9

Keywords

Search

Navigation