Comparative transcriptome analysis of Paracoccidioides brasiliensis during in vitro adhesion to type I collagen and fibronectin: Identification of potential adhesins

Research in Microbiology

Volumn 163, Issue 3, 2012, Pages 182-191

  Bailão, Alexandre Melo ^a   Nogueira, Sarah Veloso ^a   Rondon Caixeta Bonfim, Sheyla Maria ^a   De Castro, Kelly Pacheco ^a   De Fátima da Silva, Julhiany ^b   Mendes Giannini, Maria José Soares ^b   Pereira, Maristela ^a   De Almeida Soares, Célia Maria ^a  

^a FEDERAL UNIVERSITY OF GOIÁS   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Adhesin; Cooper transporter; Enolase; Paracoccidioides brasiliensis; RDA

Indexed keywords

ADHESIN; COLLAGEN TYPE 1; ENOLASE; FIBRONECTIN; TRANSCRIPTOME;

ARTICLE; BIOGENESIS; CELL TRANSPORT; DNA LIBRARY; ENERGY; EXPRESSED SEQUENCE TAG; EXTRACELLULAR MATRIX; HOST CELL; IMMUNOFLUORESCENCE; MACROPHAGE; METABOLISM; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACOCCIDIOIDES BRASILIENSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION;

CELL ADHESION; COLLAGEN TYPE I; DNA, COMPLEMENTARY; EXPRESSED SEQUENCE TAGS; FIBRONECTINS; GENE EXPRESSION PROFILING; HUMANS; PARACOCCIDIOIDES; REAL-TIME POLYMERASE CHAIN REACTION;

FUNGI; PARACOCCIDIOIDES BRASILIENSIS;

EID: 84859439614     PISSN: 09232508     EISSN: 17697123     Source Type: Journal    
DOI: 10.1016/j.resmic.2012.01.004     Document Type: Article

References (43)

1. Albuquerque P.C., Nakayasu E.S., Rodrigues M.L., Frases S., Casadevall A., Zancope-Oliveira R.M., Almeida I.C., Nosanchuk J.D. Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell. Microbiol. 2008, 10:1695-1710.
2. Andreotti P.F., da Silva J.L.M., Bailão A.M., Soares C.M.A., Bernard G., Soares C.P., Mendes-Giannini M.J. Isolation and partial characterization of a 30 kDa adhesin from Paracoccidioides brasiliensis. Microbes Infect. 2005, 7:875-881.
3. Bailão A.M., Schrank A., Borges C.L., Dutra V., Molinari-Madlum E.E.W.I., Felipe M.S.S., Mendes-Giannini M.J.S., Martins W.S., Pereira M., Soares C.M.A. Differential gene expression by Paracoccidioides brasiliensis in host interaction conditions: representational difference analysis identifies candidate gene associated with fungal pathogenesis. Microbes Infect. 2006, 8:2686-2697.
4. Barbosa M.S., Báo S.N., Andreotti P.F., Faria F.P., Felipe M.S., Feitosa L.S., Mendes-Giannini M.J.S., Soares C.M.A. 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, 74:382-389.
5. Batista W.L., Matsuo A.L., Ganiko L., Barros T.F., Veiga T.R., Freymuller E., Puccia R. The PbMDJ1 gene belongs to a conserved MDJ1/LON locus in thermodimorphic pathogenic fungi and encodes a heat shock protein that localizes to both the mitochondria and cell wall of Paracoccidioides brasiliensis. Eukaryot. Cell 2006, 5:379-390.
6. Bookout A.L., Cummins C.L., Mangelsdorf D.J., Pesola J.M., Kramer M.F. High-throughput real-time quantitative reverse transcription PCR. Curr. Protoc. Mol. Biol. 2006, 15. 15.8.
7. Carneiro C.R.W., Postol E., Nomizo R., Reis L.F.L., Brentani R.R. Identification of enolase as a laminin-binding protein on the surface of Staphylococcus aureus. Microbes Infect 2004, 6:604-608.
8. Castaldo C., Vastano V., Siciliano R.A., Candela M., Vici M., Muscariello L., Marasco R., Sacco M. Surface displaced alpha-enolase of Lactobacillus plantarum is a fibronectin binding protein. Microb. Cell Fact. 2009, 16:8-14.
9. Castro N.S., Barbosa M.S., Maia Z.A., Bao S.N., Felipe M.S.S., Santana J.M., Mendes-Giannini M.J.S., Pereira M., Soares C.M.A. Characterization of Paracoccidioides brasiliensis PbDfg5p, a cell-wall protein implicated in filamentous growth. Yeast 2008, 25:141-154.
10. Chen B., Zhang A., Xu Z., Li R., Chen H., Jin M. Large-scale identification of bacteria-host crosstalk by affinity chromatography: capturing the interactions of Streptococcus suis proteins with host cells. J. Proteome Res. 2011, 10:5163-5174.
11. Conesa A., Göts S., García-Gómez J.M., Terol J., Talón M., Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676.
12. Costa M., Borges C.L., Bailão A.M., Meirelles G.V., Mendonça Y.A., Dantas S.F.M., de Faria F.P., Felipe M.S.S., Molinari-Madlun E.E.W.I., Mendes-Giannini M.J.S., Fiúza R.B., Martins W.S., Pereira M., Soares C.M.A. Transcriptome profiling of Paracoccidioides brasiliensis yeast-phase cells recovered from infected mice brings new insights into fungal response upon host interaction. Microbiology 2007, 153:4194-4207.
13. Crowe J.D., Sievwright I.K., Auld G.C., Moore N.R., Gow N.A., Booth N.A. Candida albicans binds human plasminogen: identification of eight plasminogen-binding proteins. Mol. Microbiol. 2003, 47:1637-1651.
14. Dantas S.F., Vieira de Rezende T.C., Bailão A.M., Taborda C.P., Santos R.S., Pacheco K.C., Soares C.M.A. Identification and characterization of antigenic proteins potentially expressed during the infectious process of Paracoccidioides brasiliensis. Microbes Infect. 2009, 11:895-903.
15. Donofrio F.C., Calil A.C., Miranda E.T., Almeida A.M., Bernard G., Soares C.P., Nogueira S.V., Soares C.M.A., Mendes-Giannini M.J. Enolase from Paracoccidioides brasiliensis: isolation and identification as a fibronectin-binding protein. J. Med. Microbiol. 2009, 58:706-713.
16. Dunsmore S.E., Rannels D.E. Extracellular matrix biology in the lung. Am. J. Physiol. 1996, 270:L3-27.
17. Esgleas M., Li Y., Handock M.A., Harel J., Dubreuil J.D., Gottschalk M. Isolation and characterization of alpha-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 2008, 154:2668-2679.
18. Ewing B., Green P. Base-calling of automated sequencer traces using phred II. Error probabilities. Genome Res. 1998, 8:186-194.
19. Feng Y., Pan X., Sun W., Wang C., Zhang H., Li X., Ma Y., Shao Z., Ge J., Zheng F., Gao G.F., Tang J. Streptococcus suis enolase functions as a protective antigen displayed on the bacterial cell surface. J. Infect. Dis. 2009, 200:1583-1592.
20. Gonzaléz A., Goméz B.L., Diez S., Hernández O., Restrepo A., Hamilton A.J., Cano L.E. Purification and partial characterization of a Paracoccidioides brasiliensis protein with capacity to bind to extracellular matrix proteins. Infect. Immun. 2005, 73:2486-2495.
21. Gonzaléz A., Caro E., Muñoz C., Hamilton A.J., Cano L.E. Paracoccidioides brasiliensis conidia recognize fibronectin and fibrinogen which subsequently participate in adherence to human type II alveolar cells: involvement of a specific adhesin. Microb. Pathog. 2008, 44:389-401.
22. Götz S., García-Gómez J.M., Terol J., Williams T.D., Nagaraj S.H., Nueda M.J., Robles M., Talón M., Dopazo J., Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008, 36:3420-3435.
23. Hanna S.A., Monteiro da Silva J.L., Giannini M.J. Adherence and intracellular parasitism of Paracoccidioides brasiliensis in Vero cells. Microbes Infect. 2000, 2:877-884.
24. Hernández O., Almeida A.J., Gonzalez A., Garcia A.M., Tamayo D., Cano L.E., Restrepo A., McEwen J.G. A 32-kilodalton hydrolase plays an important role in Paracoccidioides brasiliensis adherence to host cells and influences pathogenicity. Infect. Immun. 2010, 78:5280-5286.
25. Huang X., Madan A. CAP3: a DNA sequence assembly program. Genome Res. 1999, 9:868-877.
26. Huesca M., Goodwin A., Bhagwansingh A., Hoffman P., Lingwood C.A. Characterization of an acidic-pH-inducible stress protein (hsp70), a putative sulfatide binding adhesin, from Helicobacter pylori. Infect. Immun. 1998, 66:4061-4067.
27. Klotz S.A., Pendrak M.L., Hein R.C. Antibodies to alpha5beta1 and alpha(v)beta3 integrins react with Candida albicans alcohol dehydrogenase. Microbiology 2001, 147:3159-3164.
28. Long K.H., Gomez F.J., Morris R.E., Newman S.L. Identification of heat shock protein 60 as the ligand on Histoplasma capsulatum that mediates binding to CD18 receptors on human macrophages. J. Immunol. 2003, 170:487-494.
29. Lyons A.J., Jones J. Cell adhesion molecules, the extracellular matrix and oral squamous carcinoma. Int. J. Oral Maxillofac. Surg. 2007, 36:671-679.
30. Marchais V., Kempf M., Licznar P., Lefrançois C., Bouchara J.P., Robert R., Cottin J. DNA array analysis of Candida albicans gene expression in response to adherence to polystyrene. FEMS Microbiol. Lett. 2005, 245:25-32.
31. Neto B.R.S., Silva J.F., Mendes-Giannini M.J., Lenzi H.L., Soares C.M.A., Pereira M. The malate synthase of Paracoccidioides brasiliensis is a linked surface protein that behaves as an anchorless adhesin. BMC Microbiol. 2009, 9:272.
32. Nogueira S.V., Fonseca F.L., Rodrigues M.L., Mundodi V., Abi-Chacra E.A., Winters M.S., Alderete J.F., Soares C.M.A. Paracoccidioides brasiliensis enolase is a surface protein that binds plasminogen and mediates interaction of yeast forms with host cells. Infect. Immun. 2010, 78:4040-4050.
33. Penalver M.C., O'Connor J.E., Martinez J.P., Gil M.L. Binding of human fibronectin to Aspergillus fumigatus conidia. Infect. Immun. 1996, 64:1146-1153.
34. Pereira L.A., Báo S.N., Barbosa M.S., Silva J.L., Felipe M.S., Santana J.M., Mendes-Giannini M.J.S., Soares C.M.A. Analysis of the Paracoccidioides brasiliensis triosephosphate isomerase suggests the potential for adhesin function. FEMS Yeast Res. 2007, 7:1381-1388.
35. Ramana J., Gupta D. FaaPred: a SVM-based prediction method for fungal adhesins and adhesin-like proteins. PLoS One 2010, 5:e9695.
36. Restrepo A., McEwen J.G., Castaneda E. The habitat of Paracoccidioides brasiliensis: how far from solving the riddle?. Med. Mycol. 2001, 39:233-241.
37. Ruoslahti E. Fibronectin and its receptors. Annu. Rev. Biochem. 1988, 57:375-413.
38. San-Blas G., Niño-Vega G., Iturriaga T. Paracoccidioides brasiliensis and paracoccidioidomycosis: molecular approaches to morphogenesis, diagnosis, epidemiology, taxonomy and genetics. Med. Mycol. 2002, 40:225-242.
39. Silva M.G., Schrank A., Bailao E.F.L.C., Bailao A.M., Borges C.L., Staats C.C., Parente J.A., Pereira M., et al. The homeostasis of iron, copper and zinc in Paracoccidioides brasiliensis, Cryptococcus neoformans var. grubi, and Cryptococcus gatii: a comparative analysis. Front. Microbiol. 2011, 2:1-12.
40. Sohn K., Senyurek I., Fertey J., Konigsdorfer A., Joffroy C., Hauser N., Zelt G., Brunner H., Rupp S. An in vitro assay to study the transcriptional response during adherence of Candida albicans to different human epithelia. FEMS Yeast Res. 2006, 6:1085-1093.
41. Vicentini A.P., Gesztesi J.L., Franco M.F., Souza W., Moraes J.Z., Travassos L.R., Lopes J.D. Binding of Paracoccidioides brasiliensis to laminin through surface glycoprotein gp43 leads to enhancement of fungal pathogenesis. Infect. Immun. 1994, 4:1465-1469.
42. Waterman S.R., Hacham M., Hu G., Zhu X., Park Y.D., Shin S., Panepinto J., Valyi-Nagy T., Beam C., Husain S., Singh N., Williamson P.R. Role of a CUF1/CTR4 copper-regulatory axis in the virulence of Cryptococcus neoformans. J. Clin. Invest. 2007, 117:794-802.
43. Zakikhany K., Naglik J.R., Schmidt-Westhausen A., Holland G., Schaller M., Hube B. In vivo transcript profiling of Candida albicans identifies a gene essential for interepithelial dissemination. Cell. Microbiol. 2007, 9:2938-2954.