Paracoccidioides brasiliensis enolase is a surface protein that binds plasminogen and mediates interaction of yeast forms with host cells

Infection and Immunity

Volumn 78, Issue 9, 2010, Pages 4040-4050

  Nogueira, Sarah Veloso ^a   Fonseca, Fernanda L ^b   Rodrigues, Marcio L ^b   Mundodi, Vasanth ^a,c   Abi Chacra, Erika A ^b   Winters, Michael S ^d   Alderete, John F ^c   De Almeida Soares, Célia Maria ^a  

^a FEDERAL UNIVERSITY OF GOIÁS   (Brazil)

^b FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c WASHINGTON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENOLASE; FIBRONECTIN; GLUTATHIONE TRANSFERASE; HYBRID PROTEIN; LYSINE; PLASMIN; PLASMINOGEN; PROTEIN ANTIBODY; RECOMBINANT PROTEIN; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING COMPETITION; CELL ADHESION; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOPLASM; EPITHELIUM CELL; ESCHERICHIA COLI; FEMALE; FIBRINOLYSIS; HOST CELL; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PARACOCCIDIOIDES BRASILIENSIS; PATHOGENESIS; PHAGOCYTE; PLASMINOGEN ACTIVATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN IMMOBILIZATION; REAL TIME POLYMERASE CHAIN REACTION; SOUTH AMERICAN BLASTOMYCOSIS; UPREGULATION; YEAST CELL; ANIMAL; BAGG ALBINO MOUSE; IMMUNOLOGY; METABOLISM; PARACOCCIDIOIDES; PHYSIOLOGY; RABBIT;

ANIMALS; FEMALE; FIBRINOLYSIS; HUMANS; MICE; MICE, INBRED BALB C; PARACOCCIDIOIDES; PARACOCCIDIOIDOMYCOSIS; PHOSPHOPYRUVATE HYDRATASE; PLASMINOGEN; RABBITS;

EID: 77956640401     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00221-10     Document Type: Article

References (53)

1. Agarwal, S., P. Kulshreshtha, D. Bambah Mukku, and R. Bhatnagar. 2008. α-Enolase binds to human plasminogen on the surface of Bacillus anthracis. Biochim. Biophys. Acta 1784:986-994.
2. Angiolella, L., M. Facchin, A. Stringaro, B. Maras, N. Simonetti, and A. Cassone. 1996. Identification of a glucan-associated enolase as a main cell wall protein of Candida albicans and an indirect target of lipopeptide antimycotics. J. Infect. Dis. 173:684-690.
3. Barbosa, F. M., F. L. Fonseca, C. Holandino, C. S. Alviano, L. Nimrichter, and M. L. Rodrigues. 2006. Glucuronoxylomannan-mediated interaction of Cryptococcus neoformans with human alveolar cells results in fungal internalization and host cell damage. Microbes Infect. 8:493-502.
4. Barbosa, M. S., S. N. Báo, P. F. Andreotti, F. P. Faria, M. S. Felipe, L. S. Feitosa, M. J. S. Mendes-Giannini, and C. M. A. Soares. 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. 74:382-389.
5. Batista, W. L., A. L. Matsuo, L. Ganiko, T. F. Barros, T. R. Veiga, E. Freymuller, and R. Puccia. 2006. 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 5:379-390.
6. Bergmann, S., M. Rohde, G. S. Chhatwal, and S. Hammerschmidt. 2001. α-Enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol. Microbiol. 40:1273-1287.
7. Bookout, A. L., C. L. Cumming, D. J. Mangelsdorf, J. M. Pesola, and M. F. Kramer. 2006. High-throughput real-time quantitative reverse transcription PCR, p. 15.8.1-15.8.28. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology. John Wiley & Sons, Hoboken, NJ.
8. Bradford, M. M. 1976. A dye binding assay for protein. Anal. Biochem. 72:248-254.
9. Castellino, F. J., and V. A. Ploplis. 2005. Structure and function of the plasminogen/plasmin system. Thromb. Haemost. 93:647-654.
10. Castro, N. D. S., M. S. Barbosa, Z. A. Maia, S. N. Bao, M. S. Felipe, J. M. Santana, M. J. S. Mendes-Giannini, M. Pereira, and C. M. A. Soares. 2008. Characterization of Paracoccidioides brasiliensis PbDfg5p, a cell-wall protein implicated in filamentous growth. Yeast 25:141-154.
11. Chaka, W., J. Scharringa, A. F. Verheul, J. Verhoef, A. G. Van Strijp, and I. M. Hoepelman. 1995. Quantitative analysis of phagocytosis and killing of Cryptococcus neoformans by human peripheral blood mononuclear cells by flow cytometry. Clin. Diagn. Lab. Immunol. 2:753-759.
12. Coltri, K. C., A. S. Casabona-Fortunato, M. L. Gennari-Cardoso, C. F. Pinzan, L. P. Ruas, V. S. Mariano, R. Martinez, J. C. Rosa, A. Panunto-Castelo, and M. C. Roque-Barreira. 2006. Paracoccin, a GlcNAc-binding lectin from Paracoccidioides brasiliensis, binds to laminin and induces TNF-alpha production by macrophages. Microbes Infect. 8:704-713.
13. Cork, A. J., S. Jergic, S. Hammerschmidt, B. Kobe, V. Pancholi, J. L. Benesch, C. V. Robinson, N. E. Dixon, J. A. Aquilina, and M. J. Walker. 2009. Defining the structural basis of human plasminogen binding by streptococcal surface enolase. J. Biol. Chem. 284:17129-17137.
14. Costa, M., C. L. Borges, A. M. Bailão, G. V. Meirelles, Y. A. Mendonça, S. F. I. M. Dantas, F. P. Faria, M. S. S. Felipe, E. E. W. I. Molinari-Madlum, M. J. S. M. Giannini, R. B. Fiúza, W. S. Martins, M. Pereira, and C. M. A. Soares. 2007. Transcriptome profiling of Paracoccidioides brasiliensis yeast-phase cells recovered from infected mice brings new insights into fungal response upon host interaction. Microbiology 153:4194-4207.
15. Crowe, J. D., I. K. Sieywright, G. C. Auld, N. R. Moore, N. A. Gow, and N. A. Booth. 2003. Candida albicans binds human plasminogen: identification of eight plasminogen-binding proteins. Mol. Microbiol. 47:1637-1651.
16. Dantas, S. F., T. C. Vieira de Rezende, A. M. Bailão, C. P. Taborda, R. S. Santos, K. C. Pacheco, and C. M. A. Soares. 2009. Identification and characterization of antigenic proteins potentially expressed during the infectious process of Paracoccidioides brasiliensis. Microbes Infect. 11:895-903.
17. Donofrio, F. C., A. C. Calil, E. T. Miranda, A. M. Almeida, G. Benard, C. P. Soares, S. V. Nogueira, C. M. A. Soares, and M. J. Mendes-Giannini. 2009. Enolase from Paracoccidioides brasiliensis: isolation and identification as a fibronectin-binding protein. J. Med. Microbiol. 58:706-713.
18. dos Reis Almeida, F. B., L. L. de Oliveira, M. Valle de Sousa, M. C. Barreira, and E. S. Hanna. 2010. Paracoccin from Paracoccidioides brasiliensis; purification through affinity with chitin and identification of N-acetyl-beta-D-glucosaminidase activity. Yeast 27:67-76.
19. Eroles, P., M. Sentandreu, M. V. Elorza, and R. Sentandreu. 1997. The highly immunogenic enolase and Hsp70p are adventitious Candida albicans cell wall proteins. Microbiology 143:313-320.
20. Esgleas, M., Y. Li, M. A. Handock, J. Harel, J. D. Dubreuil, and M. Gottschalk. 2008. Isolation and characterization of alpha-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 154:2668-2679.
21. Fox, D., and A. G. Smulian. 2001. Plasminogen-binding activity of enolase in the opportunistic pathogen Pneumocystis carinii. Med. Mycol. 39:495-507.
22. Franco, M. 1987. Host-parasite relationships in paracoccidioidomycosis. J. Med. Vet. Mycol. 25:5-18.
23. Ganiko, L., R. Puccia, V. S. Mariano, O. A. Sant'Anna, E. Freymuller, M. C. Roque-Barreira, and L. R. Travassos. 2007. Paracoccin, an N-acetyl-glucosamine-binding lectin of Paracoccidioides brasiliensis, is involved in fungal growth. Microbes Infect. 9:695-703.
24. Hanna, S. A., J. L. Monteiro da Silva, and M. J. Mendes-Giannini. 2000. Adherence and intracellular parasitism of Paracoccidioides brasiliensis in Vero cells. Microbes Infect. 2:877-884.
25. Jong, A. Y., S. H. M. Chen, M. F. Stins, K. S. Kim, T. L. Tuan, and S. H. Huang. 2003. Binding of Candida albicans enolase to plasmin(ogen) results in enhanced invasion of human brain microvascular endothelial cells. J. Med. Microbiol. 52:615-622.
26. Kesimer, M., N. Kilic, R. Mehrotra, D. J. Thornton, and J. K. Sheehan. 2009. Identification of salivary mucin MUC7 binding proteins from Streptococcus gordonii. BMC Microbiol. 9:163.
27. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
28. Lima, O. C., C. C. Figueiredo, J. O. Previato, L. Mendonça- Previato, V. Morandi, and L. M. L. Bezerra. 2001. Involvement of fungal cell wall components in adhesion of Sporothrix schenckii to human fibronectin. Infect. Immun. 69:6874-6880.
29. Linder, T. E., R. L. Daniels, D. J. Lim, and T. F. DeMaria. 1994. Effect of intranasal inoculation of Streptococcus pneumoniae on the structure of the surface carbohydrates of the chinchilla eustachian tube and middle ear mucosa. Microb. Pathog. 16:435-441.
30. López-Villar, E., L. Monteoliva, M. R. Larsen, E. Sachon, M. Shabaz, M. Pardo, J. Pla, C. Gil, P. Roepstorff, and C. Nombela. 2006. Genetic and proteomic evidences support the localization of yeast enolase in the cell surface. Proteomics 6(Suppl. 1):S107-S118.
31. Mendes-Giannini, M. J. S., S. A. Hanna, J. L. da Silva, P. F. Andretti, L. R. Vicentini, G. Bernard, H. L. Lenzi, and C. P. Soares. 2004. Invasion of epithelial mammalian cells by Paracoccidioides brasiliensis leads to cytoskeletal rearrangement and apoptosis of the host cell. Microbes Infect. 6:882-891.
32. Miles, L. A., C. M. Dahberg, J. Plescia, J. Felez, K. Kato, and E. F. Plow. 1991. Role of cell-surface lysines in plasminogen binding to cells: identification of alpha-enolase as a candidate plasminogen receptor. Biochemistry 30:1682-1691.
33. Mundodi, V., A. S. Kucknoor, and J. F. Alderete. 2008. Immunogenic and plasminogen-binding surface-associated α-enolase of Trichomonas vaginalis. Infect. Immun. 76:523-531.
34. Neto, B. R. D. S., J. F. Silva, M. J. Mendes-Giannini, H. L. Lenzi, C. M. A. Soares, and M. Pereira. 2009. The malate synthase of Paracoccidioides brasiliensis is a linked surface protein that behaves as an anchorless adhesin. BMC Microbiol. 9:272.
35. Nimrichter, L., M. L. Rodrigues, E. G. Rodrigues, and L. R. Travassos. 2005. The multitude of targets for the immune system and drug therapy in the fungal cell wall. Microbes Infect. 7:789-798.
36. Nosanchuk, J. D., J. N. Steenbergen, L. Shi, G. S. Deepe, Jr., and A. Casadevall. 2003. Antibodies to a cell surface histone-like protein protect against Histoplasma capsulatum. J. Clin. Invest. 112:1164-1175.
37. O'Farrell, P. H. 1975. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250:4007-4021.
38. Pancholi, V., and V. A. Fischetti. 1998. Alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J. Biol. Chem. 273:14503-14515.
39. Patti, J. L., B. L. Allen, M. J. McGavin, and M. Hook. 1994. MSCRAMM-mediated adherence of microorganisms to host tissues. Annu. Rev. Microbiol. 48:585-617.
40. Peñalver, M. C., J. E. O'Connor, J. P. Martinez, and M. L. Gil. 1996. Binding of human fibronectin to Aspergillus fumigatus conidia. Infect. Immun. 64:1146-1153.
41. Pereira, L. A., S. N. Báo, M. S. Barbosa, J. L. Silva, M. S. Felipe, J. M. Santana, M. J. S. Mendes-Giannini, and C. M. A. Soares. 2007. Analysis of the Paracoccidioides brasiliensis triosephosphate isomerase suggests the potential for adhesin function. FEMS Yeast Res. 7:1381-1388.
42. Pitarch, A., M. Sánchez, C. Nombela, and C. Gil. 2002. Sequential fractionation and two-dimensional gel analysis unravels the complexity of the dimorphic fungus Candida albicans cell wall proteome. Mol. Cell Proteomics 1:967-982.
43. Plow, E. F., T. Redlitz, L. A. Miles, and J. L. Hoover-Plow. 1995. The cell biology of the plasminogen system. FASEB J. 9:939-945.
44. Restrepo, A., J. G. McEwen, and E. Castañeda. 2001. The habitat of Paracoccidioides brasiliensis: how far from solving the riddle? Med. Mycol. 39:233-241.
45. Rodrigues, M. L., E. S. Nakayasu, D. L. Oliveira, L. Nimrichter, J. D. Nosanchuk, I. C. Almeida, and A. Casadevall. 2008. Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence. Eukaryot. Cell 7:58-67.
46. San-Blas, G., G. Nino-Veja, and T. Iturriaga. 2002. Paracoccidioides brasiliensis and paracoccidioidomycosis: molecular approaches to morphogenesis, diagnosis, epidemiology, taxonomy and genetics. Med. Mycol. 40:225-242.
47. Stie, J., G. Bruni, and D. Fox. 2009. Surface-associated plasminogen binding of Cryptococcus neoformans promotes extracellular matrix invasion. PLoS One 3:e5780.
48. Vassalli, J. D., A. P. Sappino, and D. Belin. 1991. The plasminogen activator/plasmin system. J. Clin. Invest. 88:1067-1072.
49. Vicentini, A. P., J. L. Gesztesi, M. F. Franco, W. Souza, J. Z. Moraes, L. R. Travassos, and J. D. Lopes. 1994. Binding of Paracoccidioides brasiliensis to laminin through surface glycoprotein gp43 leads to enhancement of fungal pathogenesis. Infect. Immun. 4:1465-1469.
50. Vieira, M. L., S. A. Vasconcellos, A. P. Gonçales, Z. M. de Morais, and A. L. Nascimento. 2009. Plasminogen acquisition and activation at the surface of leptospira species lead to fibronectin degradation. Infect. Immun. 77:4092-4101.
51. Walker, M. J., J. D. McArthur, F. Mckay, and M. Ranson. 2005. Is plasminogen deployed as a Streptococcus pyogenes virulence factor? Trends Microbiol. 13:308-313.
52. Westerlund, B., and T. K. Korhonen. 1993. Bacterial proteins binding to the mammalian extracellular matrix. Mol. Microbiol. 4:687-694.
53. Zaas, A. K., G. Liao, J. W. Chien, C. Weinberg, D. Shore, S. S. Giles, K. A. Marr, J. Usuka, L. H. Burch, L. Pereira, J. R. Perfect, G. Peltz, and D. A. Schwartz. 2008. Plasminogen alleles influence susceptibility to invasive aspergillosis. PLoS Genet. 4:e1000101.