, Volume 165, Issue 4–5, pp 237–248 | Cite as

Interactions of Paracoccidioides brasiliensis with host cells: recent advances

  • Maria José Soares Mendes-GianniniEmail author
  • Juliana Leal Monteiro da Silva
  • Julhiany de Fátima da Silva
  • Fabiana Cristina Donofrio
  • Elaine Toscano Miranda
  • Patrícia Ferrari Andreotti
  • Christiane Pienna Soares


Host-fungal interactions are inherently complex and dynamic. In order to identify new microbial targets and develop more effective anti-fungal therapies, it is important to understand the cellular and molecular mechanisms of disease. Paracoccidioidomycosis provokes a variety of clinical symptoms, and Paracoccidioides brasiliensis can reach many tissues, but primarily attacks the lungs. The ability of the pathogen to interact with the host surface structures is essential to further colonization, invasion, and growth. Epithelial cells may represent the first host barrier or the preferential site of entry of the fungus. For this reason, interactions between P. brasiliensis and Vero/A549 epithelial cells were evaluated, with an emphasis on the adherence, induction of cytoskeletal alterations, and differential signaling activity of the various surface molecules. The adhesion to and invasion of epithelial cells by P. brasiliensis may represent strategies employed to thwart the initial host immune response, and may help in the subsequent dissemination of the pathogen throughout the body.


Paracoccidioides brasiliensis Host-fungal interaction Adhesion Cytoskeleton Apoptosis Virulence factors 



We thank Dr. Henrique Leonel Lenzi, for the Confocal images (Depto. de Patologia, Instituto Oswaldo Cruz-Fiocruz, Rio de Janeiro, RJ. Brazil).


  1. 1.
    Benard G, Franco M. Paracoccidioidomycosis. In: Merz WG, Hay RJ editors. Topley Wilson’s medical mycology. 10, 13th ed. London: Hodder Arnold; 2005.Google Scholar
  2. 2.
    Franco M. Host-parasite relationships in paracoccidioidomycoses. J Med Vet Mycol. 1986;25:5–18.CrossRefGoogle Scholar
  3. 3.
    Kurokawa CS, Lopes CR, Sugizaki MF, Kuramae EE, Franco MF, Peracoli MT. Virulence profile of ten Paracoccidioides brasiliensis isolates: association with morphologic and genetic patterns. Rev Inst Med Trop Sao Paulo. 2005;47:257–62.PubMedGoogle Scholar
  4. 4.
    Franco CS, Lacaz A, Restrepo-Moreno G, Del Negro, editors. Paracoccidioidomycosis. Boca Raton: CRC Press; 1994.Google Scholar
  5. 5.
    Dranginis AM, Rauceo JM, Coronado JE, Lipke PN. A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol Mol Biol Rev. 2007;71:282–94.PubMedCrossRefGoogle Scholar
  6. 6.
    Cutler JE, Deepe GS, Klein BS. Advances in combating fungal diseases: vaccines on the threshold. Nat Rev Microbiol. 2007;5:13–28.PubMedCrossRefGoogle Scholar
  7. 7.
    Zhang P, Sandland GJ, Feng Z, Xu D, Minchella DJ. Evolutionary implications for interactions between multiple strains of host and parasite. J Theor Biol. 2007;14:541–55.Google Scholar
  8. 8.
    McClelland EE, Bernhardt P, Casadevall A. Estimating the relative contributions of virulence factors for pathogenic microbes. Infect Immun 2006;74:1500–04.PubMedCrossRefGoogle Scholar
  9. 9.
    Rappleye CA, Goldman WE. Defining virulence genes in the dimorphic fungi. Annu Rev Microbiol. 2006;60:281–303.PubMedCrossRefGoogle Scholar
  10. 10.
    Mendes-Giannini MJ, Soares CP, Monteiro da Silva JL, Andreotti PF. Interaction of pathogenic fungi with host cells: Molecular and cellular approaches. FEMS Immunol Med Microbiol. 2005;45:383–94.PubMedCrossRefGoogle Scholar
  11. 11.
    Filler SG, Sheppard DC. Fungal invasion of normally non-phagocytic host cells. PLoS Pathog. 2006;2:e129.PubMedCrossRefGoogle Scholar
  12. 12.
    Bailão AM, Schrank A, Borges CL, Dutra V, Molinari-Madlum EE, Soares Felipe MS, Soares Mendes-Giannini MJ, Martins WS, Pereira M, Soares CM. Differential gene expression by Paracoccidioides brasiliensis in host interaction conditions: representational difference analysis identifies candidate genes associated with fungal pathogenesis. Microb Infect. 2006;8:2686–97.CrossRefGoogle Scholar
  13. 13.
    Bastos KP, Bailão AM, Borges CL, Faria FP, Felipe MS, Silva MG, Martins WS, Fiúza RB, Pereira M, Soares CM. The transcriptome analysis of early morphogenesis in Paracoccidioides brasiliensis mycelium reveals novel and induced genes potentially associated to the dimorphic process. BMC Microbiol. 2007;7:29.PubMedCrossRefGoogle Scholar
  14. 14.
    Felipe MS, Andrade RV, Arraes FB, Nicola AM, Maranhão AQ, Torres FA, Silva-Pereira I, Poças-Fonseca MJ, Campos EG, Moraes LM, Andrade PA, Tavares AH, Silva SS, Kyaw CM, Souza DP, Pereira M, Jesuíno RS, Andrade EV, Parente JA, Oliveira GS, Barbosa MS, Martins NF, Fachin AL, Cardoso RS, Passos GA, Almeida NF, Walter ME, Soares CM, Carvalho MJ, Brígido MM. Transcriptional profiles of the human pathogenic fungus Paracoccidioides brasiliensis in mycelium and yeast cells. J Biol Chem. 2005;280:24706–14.PubMedCrossRefGoogle Scholar
  15. 15.
    Goldmann GH, Dos Reis Marques E, Duarte Ribeiro DC, de Souza Bernardes LA, Quiapin AC, Vitorelli PM, Savoldi M, Semighini CP, de Oliveira RC, Nunes LR, Travassos LR, Puccia R, Batista WL, Ferreira LE, Moreira JC, Bogossian AP, Tekaia F, Nobrega MP, Nobrega FG, Goldman MH. Expressed sequence tag analysis of the human pathogen Paracoccidioides brasiliensis yeast phase: identification of putative homologues of Candida albicans virulence and pathogenicity genes. Eukaryot Cell. 2003;2:34–48.CrossRefGoogle Scholar
  16. 16.
    Tavares AH, Silva SS, Dantas A, Campos EG, Andrade RV, Maranhão AQ, Brígido MM, Passos-Silva DG, Fachin AL, Teixeira SM, Passos GA, Soares CM, Bocca AL, Carvalho MJ, Silva-Pereira I, Felipe MS. Early transcriptional response of Paracoccidioides brasiliensis upon internalization by murine macrophages. Microb Infect. 2007;9:583–90.CrossRefGoogle Scholar
  17. 17.
    Almeida AJ, Carmona JA, Cunha C, Carvalho A, Rappleye CA, Goldman WE, Hooykaas PJ, Leão C, Ludovico P, Rodrigues F. Towards a molecular genetic system for the pathogenic fungus Paracoccidioides brasiliensis. Fungal Genet Biol. 2007.Google Scholar
  18. 18.
    Borges-Walmsley MI, Chen D, Shu X, Walmsley AR. The pathobiology of Paracoccidioides brasiliensis. Trends Microbiol. 2002;10:80–87.PubMedCrossRefGoogle Scholar
  19. 19.
    Mendes-Giannini MJS, Taylor ML, Bouchara JB, Burger E, Calich VLG, Escalante ED, Hanna SA, Lenzi HL, Machado MP, Miyaji M, Monteiro Da Silva JL, Mota EM, Restrepo A, Restrepo S, Tronchin G, Vincenzi LR, Xidieh CF, Zenteno E. Pathogenesis II: fungal responses to host responses: interaction of host cells with fungi. Med Mycol. 2000;38:113–23.PubMedGoogle Scholar
  20. 20.
    Gonzalez A, Lenzi HL, Motta EM, Caputo L, Sahaza JH, Cock AM, Ruiz AC, Restrepo A, Cano LE. Expression of adhesion molecules in lungs of mice infected with Paracoccidioides brasiliensis conidia. Microb Infect. 2005;7:666–73.Google Scholar
  21. 21.
    Verstrepen KJ, Klis FM. Flocculation, adhesion and biofilm formation in yeasts. Mol Microbiol. 2006;60:5–15.PubMedCrossRefGoogle Scholar
  22. 22.
    Mendes-Giannini MJS, Hanna SA, Monteiro Da Silva JL, Andreotti PF, Benard G, Lenzi HL, Soares CP. Invasion of epithelial mammalian cells by Paracoccidioides brasiliensis leads to cytoskeletal rearrangement and apoptosis of the host cell. Microb Infect. 2004;6:882–91.CrossRefGoogle Scholar
  23. 23.
    Monteiro da Silva JL. Adesão e invasão de Paracoccidioides brasiliensis em cultura de células: envolvimento do citoesqueleto, evento de sinalização e ocorrência de apoptose [Tese]. Araraquara, São Paulo: Universidade Estadual Paulista; 2004. p. 134.Google Scholar
  24. 24.
    Furtado JS, Brito T, Freymuller E. The structure and reproduction of Paracoccidioides brasiliensis in human tissue. Sabouraudia. 1967;5:226–9.PubMedGoogle Scholar
  25. 25.
    De Brito T, Furtado JS, Castro RM, Manini M. Intraepithelial parasitism as an infection mechanism in human paracoccidioidomycosis. Vir Arch Path Anat. 1973;361:129–38.Google Scholar
  26. 26.
    Hanna SA. Estudo dos mecanismos e fatores de virulência de Paracoccidioides brasiliensis em culturas de células [Dissertação]. Rio Claro, São Paulo: Universidade Estadual Paulista; 1995. p. 166.Google Scholar
  27. 27.
    Uemura MA. Evidências da participação dos mecanismos de adesão e invasão celular na patogenicidade do Paracoccidioides brasiliensis [Dissertação]. Campinas, São Paulo: Universidade Estadual de Campinas; 1996. p. 99.Google Scholar
  28. 28.
    Hanna AS, Monteiro Da Silva JL, Mendes-Giannini MJS. Adherence and intracellular parasitism of Paracoccidioides brasiliensis in Vero cells. Microb Infect. 2000;2:1–8.Google Scholar
  29. 29.
    Mendes-Giannini MJS, Ricci LC, Uemura M, Toscano E, Arns CW. Infection and apparent invasion of Vero cells by Paracoccidioides brasiliensis. J Med Vet Mycol. 1994;32:189–95.PubMedCrossRefGoogle Scholar
  30. 30.
    Hahn RC, Macedo AM, Fontes CJ, Batista RD, Santos NL, Hamdan JS. Randomly amplified polymorphic DNA as a valuable tool for epidemiological studies of Paracoccidioides brasiliensis. J Clin Microbiol. 2003;7:2849–54.CrossRefGoogle Scholar
  31. 31.
    Mendes-Giannini MJS, Ricci LC, Uemura MA, Toscano E, Arns CW. Invasion of Vero cells by Paracoccidioides brasiliensis. Rev Arg Micol. 1992;15:29–36.Google Scholar
  32. 32.
    Tuder RM, El Ibrahim R, Godoy CE, De Brito T. Pathology of the human pulmonary paracoccidioidomycosis. Mycopathologia. 1985;92:179–88.PubMedCrossRefGoogle Scholar
  33. 33.
    Kroegel C, Costabel U. Immune functions of constitutive pulmonary cells: the salt in the soup. Eur Respir J. 1994;7:2106–7.PubMedCrossRefGoogle Scholar
  34. 34.
    Monteiro Da Silva JL, Andreotti PF, Mendes-Giannini MJS. Interação de Paracoccidioides brasiliensis com células endoteliais. Revista de Ciências Farmacêuticas Básica e Aplicada 2005;26:149–56.Google Scholar
  35. 35.
    Barbosa MS, Bao SN, Andreotti PF, De Faria FP, Felipe MS, Dos Santos Feitosa L, Mendes-Giannini MJ, Soares CM. Glyceraldehyde-3-phosphate dehydrogenase of Paracoccidioides brasiliensis is a cell surface protein involved in fungal adhesion to extracellular matrix proteins and interaction with cells. Infect Immun. 2006;74:382–9.PubMedCrossRefGoogle Scholar
  36. 36.
    Moreira AP, Campanelli AP, Cavassani KA, Souto JT, Ferreira BR, Martinez R, Rossi MA, Silva JS. Intercellular adhesion molecule-1 is required for the early formation of granulomas and participates in the resistance of mice to the infection with the fungus Paracoccidoides brasiliensis. Am J Pathol. 2006;169:1270–81.PubMedCrossRefGoogle Scholar
  37. 37.
    Ofek I, Kahane I, Sharon N. Toward anti-adhesion therapy for microbial diseases. Trends Microbiol. 1996;4:297–9.PubMedCrossRefGoogle Scholar
  38. 38.
    Mendes-Giannini MJ, Andreotti PF, Vincenzi LR, Monteiro Da Silva JL, Lenzi HL, Benard G, Zancope-Oliveira R, De Matos Guedes HL, Soares CP. Binding of extracellular matrix proteins to Paracoccidioides brasiliensis. Microb Infect. 2006;8:1550–9.CrossRefGoogle Scholar
  39. 39.
    Vicentini AP, Gesztesi JL, Franco MF, De Souza W, De Moraes JZ, Travassos LR, Lopes JD. Binding of Paracoccidioides brasiliensis to laminin through surface glycoprotein gp43 leads to enhancement of fungal pathogenesis. Infect Immun. 1994;62:1465–9.PubMedGoogle Scholar
  40. 40.
    Andreotti PF, Monteiro Da Silva JL, Bailão AM, De Almeida Soares CM, Benard G, Soares CP, Mendes-Giannini MJS. Isolation and partial characterization of a 30 kDa adhesin from Paracoccidioides brasiliensis. Microb Infect. 2005;7:875–81.CrossRefGoogle Scholar
  41. 41.
    Gonzalez A, Gomez B, Diez S, Hernandez O, Restrepo A, Hamilton AJ, Cano LE. Purification and partial characterization of a Paracoccidioides brasiliensis proteins with capacity to bind to extracellular matrix proteins. Infect Immun. 2005;73:2486–95.PubMedCrossRefGoogle Scholar
  42. 42.
    Coltri KC, Casabona-Fortunato AS, Gennari-Cardoso ML, Pinzan CF, Ruas LP, Mariano VS, Martinez R, Rosa JC, Panunto-Castelo A, Roque-Barreira MC. Paracoccin, a GlcNAc-binding lectin from Paracoccidioides brasiliensis, binds to laminin and induces TNF-alpha production by macrophages. Microb Infect. 2006;3:704–13.CrossRefGoogle Scholar
  43. 43.
    Donofrio FC. Isolamento e caracterização parcial de adesina de Paracoccidioides brasiliensis ligante de fibronectina. [Dissertação]. Araraquara, São Paulo: Universidade Estadual Paulista; 2007. p. 108.Google Scholar
  44. 44.
    Silva JF, Andreotti PF, Monteiro da Silva JL, Soares CM, Mendes-Giannini, MJS. Proteomic analysis of Paracoccidioides brasiliensis adhesins correlated with adhesion profile. Salvador, 36nd SBBq, 2007. Abstract No: W-50.Google Scholar
  45. 45.
    Castaneda E, Brummer E, Pappagianis D, Stevens DA. Chronic pulmonary and disseminated paracoccdioidomycosis in mice: quantitation of progression and chronicity. J Med Vet Mycol. 1987;23:377–87.CrossRefGoogle Scholar
  46. 46.
    San-Blas G, San-Blas F, Ormaechea E, Serrano LE. Cell wall analysis of adenine requiring mutant of the yeast like form of Paracoccidioides brasiliensis strain IVICPb9. Sabouraudia. 1977;15:297–303.PubMedGoogle Scholar
  47. 47.
    Sundstrom P, Cutler JE, Staab JF. Reevaluation of the role of HWP1 in systemic candidiasis by use of Candida albicans strains with selectable marker URA3 targeted to the ENO1 locus. Infect Immun. 2002;70:3281–3.PubMedCrossRefGoogle Scholar
  48. 48.
    Zhao X, Oh SH, Cheng G, Green CB, Nuessen JA, Yeater K, Leng RP, Brown AJ, Hoyer LL. ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin: functional comparisons between Als3p and Als1p. Microbiology. 2004;15:2415–28.CrossRefGoogle Scholar
  49. 49.
    Cormack BP, Ghori N, Falkow S. An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science. 1999;285:578–82.PubMedCrossRefGoogle Scholar
  50. 50.
    Brandhorst T, Wuthrich M, Finkel-Jimenez B, Klein B. A C-terminal EGF-like domain governs BAD1 localization to the yeast surface and fungal adherence to phagocytes, but is dispensable in immune modulation and pathogenicity of Blastomyces dermatitidis. Mol Microbiol. 2003;48:53–65.PubMedCrossRefGoogle Scholar
  51. 51.
    Hung CY, Yu JJ, Seshan KR, Reichard U, Cole GT. A parasitic phase-specific adhesin of Coccidioides immitis contributes to the virulence of this respiratory fungal pathogen. Infect Immun. 2002;70:3443–56.PubMedCrossRefGoogle Scholar
  52. 52.
    Sundstrom P. Adhesins in Candida albicans. Curr Opin Microbiol. 1999;4:353–7.CrossRefGoogle Scholar
  53. 53.
    Brandhorst TT, Wuthrich M, Warner T, Klein B. Targeted gene disruption reveals an adhesin indispensable for pathogenicity of Blastomyces dermatitidis. J Exp Med. 1999;189:1207–16.PubMedCrossRefGoogle Scholar
  54. 54.
    Klein BS. Molecular basis of pathogenicity in Blastomyces dermatitidis: the importance of adhesion. Curr Opin Microbiol. 2000;4:339–43.CrossRefGoogle Scholar
  55. 55.
    Pizarro-Cerda J, Cossart P. Bacterial adhesion and entry into host cells. Cell 2006;124:715–27.PubMedCrossRefGoogle Scholar
  56. 56.
    Phan QT, Myers CL, Fu Y, Sheppard DC, Yeaman MR, Welch WH, Ibrahim AS, Edwards JE, Filler SG. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 2007;20:e64.CrossRefGoogle Scholar
  57. 57.
    Finlay BB, Falkow S. Common themes in microbial pathogenicity revisited. Microbiol Mol Biol Rev. 1997;61:136–69.PubMedGoogle Scholar
  58. 58.
    Swanson JA, Watts C. Macropinocytosis. Trends Cell Biol. 1995;5:424–8.PubMedCrossRefGoogle Scholar
  59. 59.
    Swanson JA, Baer SC. Phagocytosis by zyppers and triggers. Trends Cell Biol. 1995;5:89–93.PubMedCrossRefGoogle Scholar
  60. 60.
    Goldberg MB, Sansonetti PJ. Shigella subversion of the cellular cytoskeleton a strategy of epithelial colonization. Infect Immun. 1993;61:4941–6.PubMedGoogle Scholar
  61. 61.
    Hayward RD, Koronabis V. Direct nucleation and bundling of actin by the SipC protein of invasive Salmonella. Embo J. 1999;18:4926–34.PubMedCrossRefGoogle Scholar
  62. 62.
    Rosenshine I, Duronio V, Finlay BB. Tyrosine protein kinase inhibitors block invasin-promoted bacterial uptake by epithelial cells. Infect Immun. 1992;60:2211–7.PubMedGoogle Scholar
  63. 63.
    Tsarfaty I, Sandovsky-Losica H, Mittelman L, Berdicevsky I, Segal E. Cellular actin is affected by interaction with Candida albicans. FEMS Microbiol Lett. 2000;189:225–32.PubMedCrossRefGoogle Scholar
  64. 64.
    Wasylnka JA, Moore MM. Uptake of Aspergillus fumigatus conidia by phagocytic and nonphagocytic cells in vitro: quantitation using strains expressing green fluorescent protein. Infect Immun. 2002;70:3156–63.PubMedCrossRefGoogle Scholar
  65. 65.
    Kogan TV, Jadoun J, Mittelman L, Hirschberg K, Osherov N. Involvement of secreted Aspergillus fumigatus proteases in disruption of the actin fiber cytoskeleton and loss of focal adhesion sites in infected A549 lung pneumocytes. J Infect Dis. 2004;11:1965–73.CrossRefGoogle Scholar
  66. 66.
    Mendes-Giannini MJS, Moraes RA, Ricci TA. Proteolytic activity of the 43,000 molecular weight antigen secreted by Paracoccidioides brasiliensis. Rev Inst Med Trop. 1990;32:384–5.Google Scholar
  67. 67.
    Puccia R, Carmona AK, Gesztesi JL, Juliano L, Travassos LR. Exocellular proteolytic activity of Paracoccidioides brasiliensis: cleavage of components associated with the basement membrane. Med Mycol. 1998;36:354–8.Google Scholar
  68. 68.
    Bayles KW, Wesson CA, Liou LE, Fox LK, Bohach A, Trumble WR. Intracellular Staphylococcus aureus escapes the endosome and induces apoptosis in epithelial cells. Infect Immun. 1998;66:336–42.PubMedGoogle Scholar
  69. 69.
    Lewis K. Programmed death in bacteria. Microbiol Mol Biol Rev. 2000;64:503–14.PubMedCrossRefGoogle Scholar
  70. 70.
    Cacere CR, Romano CC, Mendes-Giannini MJS, Duarte AJ, Benard G. The role of apoptosis in the antigen-specific T cell hyporesponsiveness of paracoccidioidomycosis patients. Clin Immunol. 2002;105:215–22.PubMedCrossRefGoogle Scholar
  71. 71.
    Souto PC, Brito VN, Gameiro J, da Cruz-Hofling MA, Verinaud L. Programmed cell death in thymus during experimental paracoccidioidomycosis. Med Microbiol Immunol. 2003;192:225–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Danelishvili L, Mc Garvey JLY, Bermudez LE. Mycobacterium tuberculosis infection causes different levels of apoptosis and necrosis in humam macrophages and alveolar epithelial cells. Cell Microbiol. 2003;5:649–60.PubMedCrossRefGoogle Scholar
  73. 73.
    Lenzi HL, Calich VLG, Mendes-Giannini MJS, Xidieh CF, Miyaji M, Mota EM, Machado MP, Restrepo A. Two patterns of extracellular matrix expression in experimental paracoccidioidomycosis. Med Mycol. 2000;38:115–9.Google Scholar
  74. 74.
    Allen HL, Deepe GS Jr. Apoptosis modulates protective immunity to the pathogenic fungus Histoplasma capsulatum. J Clin Invest. 2005;10:2875–85.CrossRefGoogle Scholar
  75. 75.
    Berkova N, Lair-Fulleringer S, Femenia F, Huet D, Wagner MC, Gorna K, Tournier F, Ibrahim-Granet O, Guillot J, Chermette R, Boireau P, Latge JP. Aspergillus fumigatus conidia inhibit tumour necrosis factor- or staurosporine-induced apoptosis in epithelial cells. Int Immunol. 2006;18:139–50.PubMedCrossRefGoogle Scholar
  76. 76.
    Cock AM, Cano LE, Vélez D, Aristizábal BH, Trujillo J, Restrepo A. Fibrotic sequelae in pulmonary paracoccidioidomycosis: histopathological aspects in BALB/c mice infected with viable and non-viable Paracoccidioides brasiliensis propagules. Rev Inst Med Trop Sao Paulo. 2000;42:59–66.PubMedGoogle Scholar
  77. 77.
    Fine A, Anderson NL, Rothstein TL, Williams MC, Gochuico BR. Fas expression in pulmonary alveolar type II cells. Am J Physiol. 1997;273:64–71.Google Scholar
  78. 78.
    Hagimoto N, Kuwano K, Kawasaki M, Yoshimi M, Kaneko Y, Kunitake R, Maeyama T, Tanaka T, Hara N. Induction of interleukin-8 secretion and apoptosis in bronchiolar epithelial cells by Fas ligation. Am J Respir Cell Mol Biol. 1999;21:436–45.PubMedGoogle Scholar
  79. 79.
    Lengeler KB, Davidson RC, D’souza C, Harashima T, Shen W, Wang P, Pan X, Waugh M, Heitman J. Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev. 2000;64:746–85.PubMedCrossRefGoogle Scholar
  80. 80.
    Marques ER, Ferreira ME, Drummond RD, Felix JM, Menossi M, Savoldi M, Travassos LR, Puccia R, Batista WL, Carvalho KC, Goldman MH, Goldman GH. Identification of genes preferentially expressed in the pathogenic yeast phase of Paracoccidioides brasiliensis, using suppression subtraction hybridization and differential macroarray analysis. Mol Genet Genomics. 2004;271:667–777.PubMedCrossRefGoogle Scholar
  81. 81.
    De Carvalho MJ, Amorim Jesuino RS, Daher BS, Silva-Pereira I, de Freitas SM, Soares CM, Felipe MS. Functional and genetic characterization of calmodulin from the dimorphic and pathogenic fungus Paracoccidioides brasiliensis. Fungal Genet Biol. 2003;39:204–10.PubMedCrossRefGoogle Scholar
  82. 82.
    El-Rady, Shearer Jr G. Isolation and characterization of a calmodulin-encoding cDNA from the pathogenic fungus Histoplasma capsulatum. J Med Vet Mycol. 1996;34:163–9.PubMedCrossRefGoogle Scholar
  83. 83.
    Saporito SM, Sypherd PS. The isolation and characterization of a calmodulin encoding gene (CMD1) form the dimorphic fungus Candida albicans. Gene 1991;106:43–9.PubMedCrossRefGoogle Scholar
  84. 84.
    Monteiro da Silva JL, Andreotti PF, Benard G, Soares CP, Miranda ET, Mendes-Giannini MJ. Epithelial cells treated with genistein inhibit adhesion and endocytosis of Paracoccidioides brasiliensis. Antonie Van Leeuwenhoek. 2007;92:129–35.CrossRefGoogle Scholar
  85. 85.
    Toscano EM. Influência da gp43 kDa de P. brasiliensis em eventos de sinalização celular [Tese]. Araraquara, São Paulo: Universidade Estadual Paulista; 2006. p. 125.Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Maria José Soares Mendes-Giannini
    • 1
    Email author
  • Juliana Leal Monteiro da Silva
    • 1
  • Julhiany de Fátima da Silva
    • 1
  • Fabiana Cristina Donofrio
    • 1
  • Elaine Toscano Miranda
    • 1
  • Patrícia Ferrari Andreotti
    • 1
  • Christiane Pienna Soares
    • 1
  1. 1.Departamento de Análises Clínicas, Faculdade de Ciências FarmacêuticasUNESPAraraquaraBrazil

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