Advertisement

Transcriptomics of the Host–Pathogen Interaction in Paracoccidioidomycosis

  • Patrícia Albuquerque
  • Hugo Costa Paes
  • Aldo Henrique Tavares
  • Larissa Fernandes
  • Anamélia Lorenzetti Bocca
  • Ildinete Silva-Pereira
  • Maria Sueli Soares Felipe
  • André Moraes Nicola
Chapter

Abstract

Due to a lack of molecular tools that enable gain- and loss-of-function studies, much research with the fungi of the Paracoccidioides genus has consisted of gene expression studies. These have addressed the direct interaction of these fungi with the mammalian host or their response to environmental stimuli of interest to the study of their adaptability to said host, such as the temperature shift that triggers dimorphic transition. In this chapter, we present a review of findings of host–pathogen interaction studies and what evidence they found of mechanisms whereby Paracoccidioides is able to overcome differences in environment and establish disease, and of how the host responds to the pathogen. In the first part, which deals with the pathogen response, expression studies have identified metabolic pathways genes thereof are upregulated when the fungi are exposed to different organs, as well as blood and derivatives, of mice and humans. Of note, these studies have suggested an important role, in the adaptation to host tissues, of a metabolic shift away from glycolysis and aerobic respiration and towards fermentative and non-aerobic ways of obtaining energy. With regard to the remarkable preference of the genus for male hosts, studies of the response of Paracoccidioides to oestradiol have suggested a role of Rho GTPases in the process. As for the second part, dealing with the host response to the fungus, despite the paucity of data, the few large-scale studies available offer evidence to support the model whereby Th1-driven immune responses are protective and disease is associated with Th2 and Th17 responses, in keeping with small-scale studies. Overall, gene expression studies have supplied a large amount of data that lack direct experimental confirmation but which keep revealing new research avenues.

Keywords

Yeast Cell Wall Dimorphic Fungus Cell Wall Biogenesis Osmotic Stress Response Dimorphic Transition 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Bailao AM, Schrank A, Borges CL, Dutra V, Walquiria Ines Molinari-Madlum EE, Soares Felipe MS, Soares Mendes-Giannini MJ, Martins WS, Pereira M, Maria de Almeida Soares C (2006) Differential gene expression by Paracoccidioides brasiliensis in host interaction conditions: representational difference analysis identifies candidate genes associated with fungal pathogenesis. Microbes Infect 8(12–13):2686–2697. doi:10.1016/j.micinf.2006.07.019PubMedCrossRefGoogle Scholar
  2. Bailao AM, Shrank A, Borges CL, Parente JA, Dutra V, Felipe MS, Fiuza RB, Pereira M, de Almeida Soares CM (2007) The transcriptional profile of Paracoccidioides brasiliensis yeast cells is influenced by human plasma. FEMS Immunol Med Microbiol 51(1):43–57. doi:10.1111/j.1574-695X.2007.00277.xPubMedCrossRefGoogle Scholar
  3. Bailao AM, Nogueira SV, Rondon Caixeta Bonfim SM, de Castro KP, de Fatima da Silva J, Mendes Giannini MJ, Pereira M, de Almeida Soares CM (2012) Comparative transcriptome analysis of Paracoccidioides brasiliensis during in vitro adhesion to type I collagen and fibronectin: identification of potential adhesins. Res Microbiol 163(3):182–191. doi:10.1016/j.resmic.2012.01.004PubMedCrossRefGoogle Scholar
  4. Barbosa MS, Bao SN, Andreotti PF, de Faria FP, Felipe MS, dos Santos Feitosa L, Mendes-Giannini MJ, Soares CM (2006) 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 74(1):382–389. doi:10.1128/IAI.74.1.382-389.2006PubMedCentralPubMedCrossRefGoogle Scholar
  5. Bernardino S, Pina A, Felonato M, Costa TA, Frank de Araujo E, Feriotti C, Bazan SB, Keller AC, Leite KR, Calich VL (2013) TNF-α and CD8+ T cells mediate the beneficial effects of nitric oxide synthase-2 deficiency in pulmonary paracoccidioidomycosis. PLoS Negl Trop Dis 7(8):e2325. doi:10.1371/journal.pntd.0002325PubMedCentralPubMedCrossRefGoogle Scholar
  6. Bischoff SC, Krieger M, Brunner T, Dahinden CA (1992) Monocyte chemotactic protein 1 is a potent activator of human basophils. J Exp Med 175(5):1271–1275PubMedCrossRefGoogle Scholar
  7. Bonfim CV, Mamoni RL, Blotta MH (2009) TLR-2, TLR-4 and dectin-1 expression in human monocytes and neutrophils stimulated by Paracoccidioides brasiliensis. Med Mycol 47(7):722–733. doi:10.3109/13693780802641425PubMedCrossRefGoogle Scholar
  8. Bordon-Graciani AP, Dias-Melicio LA, Acorci-Valerio MJ, Araujo JP, Jr, Soares AM (2012) High expression of human monocyte iNOS mRNA induced by Paracoccidioides brasiliensis is not associated with increase in NO production. Microbes Infect/Institut Pasteur 14(12):1049–1053. doi:10.1016/j.micinf.2012.07.009CrossRefGoogle Scholar
  9. Brummer E, Hanson LH, Stevens DA (1988) Gamma-interferon activation of macrophages for killing of Paracoccidioides brasiliensis and evidence for nonoxidative mechanisms. Int J Immunopharmacol 10(8):945–952PubMedCrossRefGoogle Scholar
  10. Brummer E, Hanson LH, Restrepo A, Stevens DA (1989) Intracellular multiplication of Paracoccidioides brasiliensis in macrophages: killing and restriction of multiplication by activated macrophages. Infect Immun 57(8):2289–2294PubMedCentralPubMedGoogle Scholar
  11. Burger E, Nishikaku AS, Gameiro J, Francelin C, Camargo ZP, Verinaud L (2013) Cytokines expressed in the granulomatous lesions in experimental Paracoccidioidomycosis: role in host protective immunity and as fungal virulence factor. Clin Cell Immunol S1:010. doi:10.4172/2155-9899.S1-010Google Scholar
  12. Calich VL, Vaz CA, Burger E (1998) Immunity to Paracoccidioides brasiliensis infection. Res Immun 149(4–5):407–417; discussion 499–500CrossRefGoogle Scholar
  13. Costa M, Borges CL, Bailao AM, Meirelles GV, Mendonca YA, Dantas SF, de Faria FP, Felipe MS, Molinari-Madlum EE, Mendes-Giannini MJ, Fiuza RB, Martins WS, Pereira M, Soares CM (2007) Transcriptome profiling of Paracoccidioides brasiliensis yeast-phase cells recovered from infected mice brings new insights into fungal response upon host interaction. Microbiology 153(Pt 12):4194–4207. doi:10.1099/mic.0.2007/009332-0PubMedCrossRefGoogle Scholar
  14. de Castro LF Ferreira MC da Silva RM Blotta MH Longhi LN Mamoni RL (2013) Characterization of the immune response in human paracoccidioidomycosis. J Infect 67(5):470–485. doi:10.1016/j.jinf.2013.07.019PubMedCrossRefGoogle Scholar
  15. Derengowski LS, Tavares AH, Silva S, Procopio LS, Felipe MS, Silva-Pereira I (2008) Upregulation of glyoxylate cycle genes upon Paracoccidioides brasiliensis internalization by murine macrophages and in vitro nutritional stress condition. Med Mycol 46(2):125–134. doi:10.1080/13693780701670509PubMedCrossRefGoogle Scholar
  16. Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, Luster AD (2002) IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J Immunol 168(7):3195–3204PubMedCrossRefGoogle Scholar
  17. Felipe MS, Andrade RV, Arraes FB, Nicola AM, Maranhao AQ, Torres FA, Silva-Pereira I, Pocas-Fonseca MJ, Campos EG, Moraes LM, Andrade PA, Tavares AH, Silva SS, Kyaw CM, Souza DP, Pereira M, Jesuino 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, Brigido MM, PbGenome N (2005) Transcriptional profiles of the human pathogenic fungus Paracoccidioides brasiliensis in mycelium and yeast cells. J Biol Chem 280(26):24706–24714. doi:10.1074/jbc.M500625200PubMedCrossRefGoogle Scholar
  18. Feriotti C, Loures FV, Frank de Araujo E, da Costa TA, Calich VL (2013) Mannosyl-recognizing receptors induce an M1-like phenotype in macrophages of susceptible mice but an M2-like phenotype in mice resistant to a fungal infection. PLoS One 8(1):e54845. doi:10.1371/journal.pone.0054845PubMedCentralPubMedCrossRefGoogle Scholar
  19. Fernandes VC, Martins EM, Boeloni JN, Coitinho JB, Serakides R, Goes AM (2011) The combined use of Paracoccidioides brasiliensis Pb40 and Pb27 recombinant proteins enhances chemotherapy effects in experimental paracoccidioidomycosis. Microbes Infect/Institut Pasteur 13(12–13):1062–1072. doi:10.1016/j.micinf.2011.06.004CrossRefGoogle Scholar
  20. Ferreira KS, Bastos KR, Russo M, Almeida SR (2007) Interaction between Paracoccidioides brasiliensis and pulmonary dendritic cells induces interleukin-10 production and toll-like receptor-2 expression: possible mechanisms of susceptibility. J Infect Dis 196(7):1108–1115PubMedCrossRefGoogle Scholar
  21. Ferreira MC, de Oliveira RT, da Silva RM, Blotta MH, Mamoni RL (2010) Involvement of regulatory T cells in the immunosuppression characteristic of patients with paracoccidioidomycosis. Infect Immun 78(10):4392–4401. doi:10.1128/IAI.00487-10PubMedCentralPubMedCrossRefGoogle Scholar
  22. Fortes MR, Miot HA, Kurokawa CS, Marques ME, Marques SA (2011) Immunology of paracoccidioidomycosis. An Bras Dermatol 86(3):516–524PubMedCrossRefGoogle Scholar
  23. Fradin C, Kretschmar M, Nichterlein T, Gaillardin C, d’Enfert C, Hube B (2003) Stage-specific gene expression of Candida albicans in human blood. Mol Microbiol 47(6):1523–1543PubMedCrossRefGoogle Scholar
  24. Fradin C, De Groot P, MacCallum D, Schaller M, Klis F, Odds FC, Hube B (2005) Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol Microbiol 56(2):397–415. doi:10.1111/j.1365-2958.2005.04557.xPubMedCrossRefGoogle Scholar
  25. Fukuda Y, Tsai HF, Myers TG, Bennett JE (2013) Transcriptional profiling of Candida glabrata during phagocytosis by neutrophils and in the infected mouse spleen. Infect Immun 81(4):1325–1333. doi:10.1128/IAI.00851-12PubMedCentralPubMedCrossRefGoogle Scholar
  26. Godiska R, Chantry D, Raport CJ, Sozzani S, Allavena P, Leviten D, Mantovani A, Gray PW (1997) Human macrophage-derived chemokine (MDC), a novel chemoattractant for monocytes, monocyte-derived dendritic cells, and natural killer cells. J Exp Med 185(9):1595–1604PubMedCentralPubMedCrossRefGoogle Scholar
  27. Goldman 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 (2003) 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 2(1):34–48PubMedCentralPubMedCrossRefGoogle Scholar
  28. Johnston DA, Eberle KE, Sturtevant JE, Palmer GE (2009) Role for endosomal and vacuolar GTPases in Candida albicans pathogenesis. Infect Immun 77(6):2343–2355. doi:10.1128/IAI.01458-08PubMedCentralPubMedCrossRefGoogle Scholar
  29. Kanetsuna F, Carbonell LM, Moreno RE, Rodriguez J (1969) Cell wall composition of the yeast and mycelial forms of Paracoccidioides brasiliensis. J Bacteriol 97(3):1036–1041PubMedCentralPubMedGoogle Scholar
  30. Katze MG, He Y, Gale M, Jr (2002) Viruses and interferon: a fight for supremacy. Nat Rev Immunol 2(9):675–687. doi:10.1038/nri888PubMedCrossRefGoogle Scholar
  31. Konno FT, Maricato J, Konno AY, Guereschi MG, Vivanco BC, Feitosa Ldos S, Mariano M, Lopes JD (2012) Paracoccidioides brasiliensis GP43-derived peptides are potent modulators of local and systemic inflammatory response. Microbes Infect/Institut Pasteur 14(6):517–527. doi:10.1016/j.micinf.2011.12.012CrossRefGoogle Scholar
  32. Kurokawa CS, Araujo JP, Jr, Soares AM, Sugizaki MF, Peracoli MT (2007) Pro- and anti-inflammatory cytokines produced by human monocytes challenged in vitro with Paracoccidioides brasiliensis. Microbiol Immunol 51(4):421–428PubMedCrossRefGoogle Scholar
  33. Kurth I, Willimann K, Schaerli P, Hunziker T, Clark-Lewis I, Moser B (2001) Monocyte selectivity and tissue localization suggests a role for breast and kidney-expressed chemokine (BRAK) in macrophage development. J Exp Med 194(6):855–861PubMedCentralPubMedCrossRefGoogle Scholar
  34. Liu J, Balasubramanian MK (2001) 1,3-beta-Glucan synthase: a useful target for antifungal drugs. Curr Drug Targets Infect Disord 1(2):159–169PubMedCrossRefGoogle Scholar
  35. Longhi LN, da Silva RM, Fornazim MC, Spago MC, de Oliveira RT, Nowill AE, Blotta MH, Mamoni RL (2012) Phenotypic and functional characterization of NK cells in human immune response against the dimorphic fungus Paracoccidioides brasiliensis. J Immunol 189(2):935–945. doi:10.4049/jimmunol.1102563PubMedCrossRefGoogle Scholar
  36. Lorenz MC, Bender JA, Fink GR (2004) Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 3(5):1076–1087. doi:10.1128/EC.3.5.1076-1087.2004PubMedCentralPubMedCrossRefGoogle Scholar
  37. Loures FV, Pina A, Felonato M, Feriotti C, de Araujo EF, Calich VL (2011) MyD88 signaling is required for efficient innate and adaptive immune responses to Paracoccidioides brasiliensis infection. Infect Immun 79(6):2470–2480. doi:10.1128/IAI.00375-10PubMedCentralPubMedCrossRefGoogle Scholar
  38. Loures FV, Araujo EF, Feriotti C, Bazan SB, Costa TA, Brown GD, Calich VL (2014) Dectin-1 Induces M1 Macrophages and Prominent Expansion of CD8+ IL-17+ Cells in Pulmonary Paracoccidiodomycosis. The J Infect Dis 210:762–773 doi:10.1093/infdis/jiu136Google Scholar
  39. Ma B, Zhu Z, Homer RJ, Gerard C, Strieter R, Elias JA (2004) The C10/CCL6 chemokine and CCR1 play critical roles in the pathogenesis of IL-13-induced inflammation and remodeling. J Immunol 172(3):1872–1881PubMedCrossRefGoogle Scholar
  40. McEwen JG, Garcia AM, Ortiz BL, Botero S, Restrepo A (1995) In search of the natural habitat of Paracoccidioides brasiliensis. Arch Med Res 26(3):305–306PubMedGoogle Scholar
  41. Menino JF, Saraiva M, Gomes-Alves AG, Lobo-Silva D, Sturme M, Gomes-Rezende J, Saraiva AL, Goldman GH, Cunha C, Carvalho A, Romani L, Pedrosa J, Castro AG, Rodrigues F (2013) TLR9 activation dampens the early inflammatory response to Paracoccidioides brasiliensis, impacting host survival. PLoS Negl Trop Dis 7(7):e2317. doi:10.1371/journal.pntd.0002317PubMedCentralPubMedCrossRefGoogle Scholar
  42. Miramon P, Dunker C, Windecker H, Bohovych IM, Brown AJ, Kurzai O, Hube B (2012) Cellular responses of Candida albicans to phagocytosis and the extracellular activities of neutrophils are critical to counteract carbohydrate starvation, oxidative and nitrosative stress. PLoS One 7(12):e52850. doi:10.1371/journal.pone.0052850PubMedCentralPubMedCrossRefGoogle Scholar
  43. Morton CO, Varga JJ, Hornbach A, Mezger M, Sennefelder H, Kneitz S, Kurzai O, Krappmann S, Einsele H, Nierman WC, Rogers TR, Loeffler J (2011) The temporal dynamics of differential gene expression in Aspergillus fumigatus interacting with human immature dendritic cells in vitro. PLoS One 6(1):e16016. doi:10.1371/journal.pone.0016016PubMedCentralPubMedCrossRefGoogle Scholar
  44. Moser B, Clark-Lewis I, Zwahlen R, Baggiolini M (1990) Neutrophil-activating properties of the melanoma growth-stimulatory activity. J Exp Med 171(5):1797–1802PubMedCrossRefGoogle Scholar
  45. Mourao-Sa D, Robinson MJ, Zelenay S, Sancho D, Chakravarty P, Larsen R, Plantinga M, Van Rooijen N, Soares MP, Lambrecht B, Reis e Sousa C (2011) CLEC-2 signaling via Syk in myeloid cells can regulate inflammatory responses. Eur J Immunol 41(10):3040–3053. doi:10.1002/eji.201141641PubMedCrossRefGoogle Scholar
  46. Nagira M, Imai T, Hieshima K, Kusuda J, Ridanpaa M, Takagi S, Nishimura M, Kakizaki M, Nomiyama H, Yoshie O (1997) Molecular cloning of a novel human CC chemokine secondary lymphoid-tissue chemokine that is a potent chemoattractant for lymphocytes and mapped to chromosome 9p13. J Biol Chem 272(31):19518–19524PubMedCrossRefGoogle Scholar
  47. Nevitt T (2011) War-Fe-re: iron at the core of fungal virulence and host immunity. Biometals 24(3):547–558. doi:10.1007/s10534-011-9431-8PubMedCrossRefGoogle Scholar
  48. Nguyen VQ, Sil A (2008) Temperature-induced switch to the pathogenic yeast form of Histoplasma capsulatum requires Ryp1, a conserved transcriptional regulator. Proc Natl Acad Sci U S A 105(12):4880–4885. doi:10.1073/pnas.0710448105PubMedCentralPubMedCrossRefGoogle Scholar
  49. Nicola AM, Andrade RV, Dantas AS, Andrade PA, Arraes FB, Fernandes L, Silva-Pereira I, Felipe MS (2008) The stress responsive and morphologically regulated hsp90 gene from Paracoccidioides brasiliensis is essential to cell viability. BMC Microbiol 8:158. doi:10.1186/1471-2180-8-158PubMedCentralPubMedCrossRefGoogle Scholar
  50. Nogueira SV, Fonseca FL, Rodrigues ML, Mundodi V, Abi-Chacra EA, Winters MS, Alderete JF, de Almeida Soares CM (2010) Paracoccidioides brasiliensis enolase is a surface protein that binds plasminogen and mediates interaction of yeast forms with host cells. Infect Immun 78(9):4040–4050. doi:10.1128/IAI.00221-10PubMedCentralPubMedCrossRefGoogle Scholar
  51. Oarada M, Kamei K, Gonoi T, Tsuzuki T, Toyotome T, Hirasaka K, Nikawa T, Sato A, Kurita N (2009) Beneficial effects of a low-protein diet on host resistance to Paracoccidioides brasiliensis in mice. Nutrition 25(9):954–963. doi:10.1016/j.nut.2009.02.004PubMedCrossRefGoogle Scholar
  52. Parente AF, Bailao AM, Borges CL, Parente JA, Magalhaes AD, Ricart CA, Soares CM (2011) Proteomic analysis reveals that iron availability alters the metabolic status of the pathogenic fungus Paracoccidioides brasiliensis. PLoS One 6(7):e22810. doi:10.1371/journal.pone.0022810PubMedCentralPubMedCrossRefGoogle Scholar
  53. Pina A, de Araujo EF, Felonato M, Loures FV, Feriotti C, Bernardino S, Barbuto JA, Calich VL (2013) Myeloid dendritic cells (DCs) of mice susceptible to paracoccidioidomycosis suppress T cell responses whereas myeloid and plasmacytoid DCs from resistant mice induce effector and regulatory T cells. Infect Immun 81 (4):1064–1077. doi:10.1128/IAI.00736-12PubMedCentralPubMedCrossRefGoogle Scholar
  54. Price MS, Betancourt-Quiroz M, Price JL, Toffaletti DL, Vora H, Hu G, Kronstad JW, Perfect JR (2011) Cryptococcus neoformans requires a functional glycolytic pathway for disease but not persistence in the host. MBio 2(3):e00103–00111. doi:10.1128/mBio.00103-11PubMedCentralPubMedCrossRefGoogle Scholar
  55. Rappleye CA, Eissenberg LG, Goldman WE (2007) Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor. Proc Natl Acad Sci U S A 104(4):1366–1370. doi:10.1073/pnas.0609848104PubMedCentralPubMedCrossRefGoogle Scholar
  56. Reis BS, Fernandes VC, Martins EM, Serakides R, Goes AM (2008) Protective immunity induced by rPb27 of Paracoccidioides brasiliensis. Vaccine 26(43):5461–5469. doi:10.1016/j.vaccine.2008.07.097PubMedCrossRefGoogle Scholar
  57. Restrepo A, Salazar ME, Cano LE, Stover EP, Feldman D, Stevens DA (1984) Estrogens inhibit mycelium-to-yeast transformation in the fungus Paracoccidioides brasiliensis: implications for resistance of females to paracoccidioidomycosis. Infect Immun 46(2):346–353PubMedCentralPubMedGoogle Scholar
  58. Restrepo A, Gómez BL, Tobón A (2012) Paracoccidioidomycosis: Latin America’s own fungal disorder. Curr Fungal Infect Rep 6(4):9. doi:10.1007/s12281-012-0114-xCrossRefGoogle Scholar
  59. Richthammer C, Enseleit M, Sanchez-Leon E, Marz S, Heilig Y, Riquelme M, Seiler S (2012) RHO1 and RHO2 share partially overlapping functions in the regulation of cell wall integrity and hyphal polarity in Neurospora crassa. Mol Microbiol 85(4):716–733. doi:10.1111/j.1365-2958.2012.08133.xPubMedCrossRefGoogle Scholar
  60. Ruiz OH, Gonzalez A, Almeida AJ, Tamayo D, Garcia AM, Restrepo A, McEwen JG (2011) Alternative oxidase mediates pathogen resistance in Paracoccidioides brasiliensis infection. PLoS Negl Trop Dis 5(10):e1353. doi:10.1371/journal.pntd.0001353PubMedCrossRefGoogle Scholar
  61. San-Blas G, Nino-Vega G, Iturriaga T (2002) Paracoccidioides brasiliensis and paracoccidioidomycosis: molecular approaches to morphogenesis, diagnosis, epidemiology, taxonomy and genetics. Med Mycol 40(3):225–242PubMedCrossRefGoogle Scholar
  62. Shankar J, Restrepo A, Clemons KV, Stevens DA (2011a) Hormones and the resistance of women to paracoccidioidomycosis. Clin Microbiol Rev 24(2):296–313. doi:10.1128/CMR.00062-10Google Scholar
  63. Shankar J, Wu TD, Clemons KV, Monteiro JP, Mirels LF, Stevens DA (2011b) Influence of 17beta-estradiol on gene expression of Paracoccidioides during mycelia-to-yeast transition. PLoS One 6(12):e28402. doi:10.1371/journal.pone.0028402Google Scholar
  64. Silva SS, Tavares AH, Passos-Silva DG, Fachin AL, Teixeira SM, Soares CM, Carvalho MJ, Bocca AL, Silva-Pereira I, Passos GA, Felipe MS (2008) Transcriptional response of murine macrophages upon infection with opsonized Paracoccidioides brasiliensis yeast cells. Microbes Infect 10(1):12–20PubMedCrossRefGoogle Scholar
  65. Soares DA, de Andrade RV, Silva SS, Bocca AL, Soares Felipe SM, Petrofeza S (2010) Extracellular Paracoccidioides brasiliensis phospholipase B involvement in alveolar macrophage interaction. BMC Microbiol 10:241. doi:10.1186/1471-2180-10-241PubMedCentralPubMedCrossRefGoogle Scholar
  66. Steenbergen JN, Shuman HA, Casadevall A (2001) Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc Natl Acad Sci U S A 98 (26):15245–15250. doi:10.1073/pnas.261418798PubMedCentralPubMedCrossRefGoogle Scholar
  67. Tamayo D, Munoz JF, Torres I, Almeida AJ, Restrepo A, McEwen JG, Hernandez O (2013) Involvement of the 90 kDa heat shock protein during adaptation of Paracoccidioides brasiliensis to different environmental conditions. Fungal Genet Biol 51:34–41. doi:10.1016/j.fgb.2012.11.005PubMedCrossRefGoogle Scholar
  68. Tavares AH, Silva SS, Dantas A, Campos EG, Andrade RV, Maranhao AQ, Brigido MM, Passos-Silva DG, Fachin AL, Teixeira SM, Passos GA, Soares CM, Bocca AL, Carvalho MJ, Silva-Pereira I, Felipe MS (2007) Early transcriptional response of Paracoccidioides brasiliensis upon internalization by murine macrophages. Microbes Infect 9(5):583–590. doi:10.1016/j.micinf.2007.01.024PubMedCrossRefGoogle Scholar
  69. Tavares AH, Derengowski LS, Ferreira KS, Silva SS, Macedo C, Bocca AL, Passos GA, Almeida SR, Silva-Pereira I (2012) Murine dendritic cells transcriptional modulation upon Paracoccidioides brasiliensis infection. PLoS Negl Trop Dis 6(1):e1459. doi:10.1371/journal.pntd.0001459PubMedCentralPubMedCrossRefGoogle Scholar
  70. Teixeira MM, Theodoro RC, de Carvalho MJ, Fernandes L, Paes HC, Hahn RC, Mendoza L, Bagagli E, San-Blas G, Felipe MS (2009) Phylogenetic analysis reveals a high level of speciation in the Paracoccidioides genus. Mol Phylogenet Evol 52(2):273–283. doi:S1055-7903(09)00135-3 [pii] 10.1016/j.ympev.2009.04.005PubMedCrossRefGoogle Scholar
  71. Thewes S, Kretschmar M, Park H, Schaller M, Filler SG, Hube B (2007) In vivo and ex vivo comparative transcriptional profiling of invasive and non-invasive Candida albicans isolates identifies genes associated with tissue invasion. Mol Microbiol 63(6):1606–1628. doi:10.1111/j.1365-2958.2007.05614.xPubMedCrossRefGoogle Scholar
  72. Torres I, Hernandez O, Tamayo D, Munoz JF, Leitao NP, Jr, Garcia AM, Restrepo A, Puccia R, McEwen JG (2013) Inhibition of PbGP43 expression may suggest that gp43 is a virulence factor in Paracoccidioides brasiliensis. PloS One 8(7):e68434. doi:10.1371/journal.pone.0068434PubMedCentralPubMedCrossRefGoogle Scholar
  73. Torres I, Hernandez O, Tamayo D, Munoz JF, Garcia AM, Gomez BL, Restrepo A, McEwen JG (2014) Paracoccidioides brasiliensis PbP27 gene: knockdown procedures and functional characterization. FEMS Yeast Res 14(2):270–280. doi:10.1111/1567-1364.12099PubMedCrossRefGoogle Scholar
  74. Tristao FS, Rocha FA, Moreira AP, Cunha FQ, Rossi MA, Silva JS (2013) 5-Lipoxygenase activity increases susceptibility to experimental Paracoccidioides brasiliensis infection. Infect Immun 81(4):1256–1266. doi:10.1128/IAI.01209-12PubMedCentralPubMedCrossRefGoogle Scholar
  75. Voltan AR, Sardi Jde C, Soares CP, Pelajo Machado M, Fusco Almeida AM, Mendes-Giannini MJ (2013) Early Endosome Antigen 1 (EEA1) decreases in macrophages infected with Paracoccidioides brasiliensis. Med Mycol 51(7):759–764. doi:10.3109/13693786.2013.777859PubMedCrossRefGoogle Scholar
  76. Yamochi W, Tanaka K, Nonaka H, Maeda A, Musha T, Takai Y (1994) Growth site localization of Rho1 small GTP-binding protein and its involvement in bud formation in Saccharomyces cerevisiae. J Cell Biol 125(5):1077–1093PubMedCrossRefGoogle Scholar
  77. Youseff BH, Holbrook ED, Smolnycki KA, Rappleye CA (2012) Extracellular superoxide dismutase protects Histoplasma yeast cells from host-derived oxidative stress. PLoS Pathog 8(5):e1002713. doi:10.1371/journal.ppat.1002713PubMedCentralPubMedCrossRefGoogle Scholar
  78. Zhang C, Wang Y, Wang J, Zhai Z, Zhang L, Zheng W, Zheng W, Yu W, Zhou J, Lu G, Shim WB, Wang Z (2013) Functional characterization of Rho family small GTPases in Fusarium graminearum. Fungal Genet Biol 61:90–99. doi:10.1016/j.fgb.2013.09.001PubMedCrossRefGoogle Scholar
  79. Zhu J, Yamane H, Paul WE (2010) Differentiation of effector CD4 T cell populations (*). Annu Rev Immunol 28:445–489. doi:10.1146/annurev-immunol-030409-101212PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Patrícia Albuquerque
    • 3
  • Hugo Costa Paes
    • 1
  • Aldo Henrique Tavares
    • 3
  • Larissa Fernandes
    • 3
  • Anamélia Lorenzetti Bocca
    • 1
  • Ildinete Silva-Pereira
    • 1
  • Maria Sueli Soares Felipe
    • 1
  • André Moraes Nicola
    • 2
  1. 1.Universidade de Brasília, Campus Universitário Darcy RibeiroBrasíliaBrazil
  2. 2.Programa de Pós-Graduação em Ciências Genômicas e BiotecnologiaUniversidade Católica de BrasíliaBrasíliaBrazil
  3. 3.Universidade de Brasília, Faculdade de CeilândiaBrasíliaBrazil

Personalised recommendations