Differential gene expression analysis of Paracoccidioides brasiliensis during keratinocyte infection

Journal of Medical Microbiology

Volumn 60, Issue 3, 2011, Pages 269-280

  Da Silva, Roberta Peres ^a   Matsumoto, Marcelo Teruyuki ^a   Braz, Jaqueline Derissi ^a   Voltan, Aline Raquel ^a   De Oliveira, Haroldo Cesar ^a   Soares, Christiane Pienna ^a   Giannini, Maria José Soares Mendes ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; CYTOKINE; FUNGAL PROTEIN; GLUTAMINE FRUCTOSE 6 PHOSPHATE AMINOTRANSFERASE; MESSENGER RNA; PENR2 PROTEIN; PROTEASOME; RDS1 PROTEIN; UBIQUITIN CONJUGATING ENZYME; UNCLASSIFIED DRUG; ZINC TRANSPORTER;

ARTICLE; CARBON METABOLISM; CELL ADHESION; CELL CULTURE; CELL INVASION; CELL PROLIFERATION; CELL STRESS; CULTURE MEDIUM; CYTOSKELETON; DRUG TARGETING; FUNGUS ISOLATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; KERATINOCYTE; NONHUMAN; PARACOCCIDIOIDES BRASILIENSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN METABOLISM; SOUTH AMERICAN BLASTOMYCOSIS; STRESS; YEAST;

CELLS, CULTURED; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; HUMANS; KERATINOCYTES; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, FLUORESCENCE; PARACOCCIDIOIDES; PROTEOME;

EID: 79951902253     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.022467-0     Document Type: Article

References (86)

1. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389-3402. (Pubitemid 27359211)
2. Andreotti, P. F., Monteiro da Silva, J. L., Bailão, A. M., Soares, C. M., Benard, G., Soares, C. P. & Mendes-Giannini, M. J. (2005). Isolation and partial characterization of a 30 kDa adhesin from Paracoccidioides brasiliensis. Microbes Infect 7, 875-881.
3. Bailão, A. M., Schrank, A., Borges, C. L., Dutra, V., Walquíria Inês Molinari-Madlum, E. E., Soares Felipe, M. S., Soares Mendes- Giannini, M. J., Martins, W. S., 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, 2686-2697.
4. Bailão, A. M., Shrank, A., Borges, C. L., Parente, J. A., Dutra, V., Felipe, M. S., Fiúza, R. B., Pereira, M. & de Almeida Soares, C. M. (2007). The transcriptional profile of Paracoccidioides brasiliensis yeast cells is influenced by human plasma. FEMS Immunol Med Microbiol 51, 43-57.
5. Bajorek, M., Finley, D. & Glickman, M. H. (2003). Proteasome disassembly and downregulation is correlated with viability during stationary phase. Curr Biol 13, 1140-1144. (Pubitemid 36815263)
6. Barelle, C. J., Priest, C. L., MacCallum, D. M., Gow, N. A., Odds, F. C. & Brown, A. J. (2006). Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell Microbiol 8, 961-971. (Pubitemid 43670837)
7. Benard, G. & Franco, M. (2007). Paracoccidioidomycosis. In Topley & Wilson's Microbiology and Microbial Infections: Medical Mycology, 10th edn, pp. 541-549. Edited by W. G. Merz & R. J. Hay. London: Hodder Arnold.
8. Benard, G. & Mendes-Giannini,M. J. S. (2009). Paracoccidioidomycosis. In Feigin & Cherry's Textbook of Pediatric Infectious Diseases, 6th edn, pp. 2762-2776. Edited by R. D. Feigin, J. D. Cherry, G. J. Demmler-Harrison & S. L. Kaplan. Philadelphia: Saunders Elsevier.
9. Berlett, B. S. & Stadtman, E. R. (1997). Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272, 20313-20316. (Pubitemid 27355575)
10. Bignell, E., Negrete-Urtasun, S., Calcagno, A. M., Haynes, K., Arst, H. N., Jr & Rogers, T. (2005). The Aspergillus pH-responsive transcription factor PacC regulates virulence. Mol Microbiol 55, 1072-1084. (Pubitemid 40299178)
11. Bird, A. J., Zhao, H., Luo, H., Jensen, L. T., Srinivasan, C., Evans- Galea, M., Winge, D. R. & Eide, D. J. (2000). A dual role for zinc fingers in both DNA binding and zinc sensing by the Zap1 transcriptional activator. EMBO J 19, 3704-3713. (Pubitemid 30462128)
12. Bochtler, M., Ditzel, L., Groll, M., Hartmann, C. & Huber, R. (1999). The proteasome. Annu Rev Biophys Biomol Struct 28, 295-317. (Pubitemid 29319261)
13. Costa, D. L., Dias-Melicio, L. A., Acorci, M. J., Bordon, A. P., Tavian, E. G., Peraçoli, M. T. & Soares, A. M. (2007). Effect of interleukin-10 on the Paracoccidioides brasiliensis killing by gamma-interferon activated human neutrophils. Microbiol Immunol 51, 73-80. (Pubitemid 46155188)
14. Coux, O., Tanaka, K. & Goldberg, A. L. (1996). Structure and functions of the 20S and 26S proteasomes. Annu Rev Biochem 65, 801-847. (Pubitemid 26255262)
15. Cox, G. M., Harrison, T. S., McDade, H. C., Taborda, C. P., Heinrich, G., Casadevall, A. & Perfect, J. R. (2003). Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Infect Immun 71, 173-180. (Pubitemid 36026018)
16. da Silva, M. B., Marques, A. F., Nosanchuk, J. D., Casadevall, A., Travassos, L. R. & Taborda, C. P. (2006). Melanin in the dimorphic fungal pathogen Paracoccidioides brasiliensis: effects on phagocytosis, intracellular resistance and drug susceptibility. Microbes Infect 8, 197-205. (Pubitemid 43139308)
17. Demasi, M., Silva, G. M. & Netto, L. E. (2003). 20 S proteasome from Saccharomyces cerevisiae is responsive to redox modifications and is S-glutathionylated. J Biol Chem 278, 679-685. (Pubitemid 36043622)
18. Derengowski, L. S., Tavares, A. H., Silva, S., Procopio, L. S., Felipe, M. S. & Silva-Pereira, I. (2008). Upregulation of glyoxylate cycle genes upon Paracoccidioides brasiliensis internalization by murine macrophages and in vitro nutritional stress condition. MedMycol 46, 125-134. (Pubitemid 351372331)
19. Dias, A. L., Brigagao, M. R., Colepicolo, P., Siqueira, A. M., Silva, E. G. & Paula, C. R. (2006). Superoxide dismutase in Cryptococcus neoformans varieties gattii, grubii, and neoformans. Mem Inst Oswaldo Cruz 101, 107-109.
20. Dutra, V., Nakazato, L., Broetto, L., Silveira Schrank, I., Henning Vainstein, M. & Schrank, A. (2004). Application of representational difference analysis to identify sequence tags expressed by Metarhizium anisopliae during the infection process of the tick Boophilus microplus cuticle. Res Microbiol 155, 245-251. (Pubitemid 38624171)
21. Ebel, F., Schwienbacher, M., Beyer, J., Heesemann, J., Brakhage, A. A. & Brock, M. (2006). Analysis of the regulation, expression, and localisation of the isocitrate lyase from Aspergillus fumigatus, a potential target for antifungal drug development. Fungal Genet Biol 43, 476-489. (Pubitemid 43729189)
22. Eide, D. J. (2009). Homeostatic and adaptive responses to zinc deficiency in Saccharomyces cerevisiae. J Biol Chem 284, 18565-18569.
23. Ewing, B., Hillier, L., Wendi, M. C. & Green, P. (1998). Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res 8, 175-185. (Pubitemid 28177229)
24. Fan, W., Kraus, P. R., Boily, M. J. & Heitman, J. (2005). Cryptococcus neoformans gene expression during murine macrophage infection. Eukaryot Cell 4, 1420-1433. (Pubitemid 41176696)
25. Finlay, B. B. & Falkow, S. (1988). Comparison of the invasion strategies used by Salmonella cholerae-suis, Shigella flexneri and Yersinia enterocolitica to enter cultured animal cells: endosome acidification is not required for bacterial invasion or intracellular replication. Biochimie 70, 1089-1099. (Pubitemid 18261779)
26. Fradin, C., De Groot, P., Maccallum, D., Schaller, M., Klis, F., Odds, F. C. & Hube, B. (2005). Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol Microbiol 56, 397-415. (Pubitemid 40516780)
27. Franco, M. (1987). Host-parasite relationships in paracoccidioidomycoses. J Med Vet Mycol 25, 5-18.
28. Franco, M. V., Goes, A. M. & Koury, M. C. (1997). Model of in vitro granulomatous hypersensitivity in human paracoccidioidomycosis. Mycopathologia 137, 129-136. (Pubitemid 27461757)
29. Giulivi, C., Pacifici, R. E. & Davies, K. J. (1994). Exposure of hydrophobic moieties promotes the selective degradation of hydrogen peroxide-modified hemoglobin by the multicatalytic proteinase complex, proteasome. Arch Biochem Biophys 311, 329-341. (Pubitemid 24220152)
30. Goulart, L., Rosa e Silva, L. K., Chiapello, L., Silveira, C., Crestani, J., Masih, D. & Vainstein, M. H. (2010). Cryptococcus neoformans and Cryptococcus gattii genes preferentially expressed during rat macrophage infection. Med Mycol 48, 932-941.
31. Green, P. (2009). PHRAP documentation. University of Washington, Seattle, WA, USA. http://www.phrap.org/phrap.docs/phrap.html.
32. Hamilton, A. J. & Gomez, B. L. (2002). Melanins in fungal pathogens. J Med Microbiol 51, 189-191.
33. Hanna, S. A., Monteiro da Silva, J. L. & Mendes-Giannini, M. J. S. (2000). Adherence and intracellular parasitism of Paracoccidioides brasiliensis in Vero cells. Microbes Infect 2, 877-884.
34. Hu, G., Cheng, P. Y., Sham, A., Perfect, J. R. & Kronstad, J. W. (2008). Metabolic adaptation in Cryptococcus neoformans during early murine pulmonary infection. Mol Microbiol 69, 1456-1475.
35. Huang, X. & Madan, A. (1999). CAP3: a DNA sequence assembly program. Genome Res 9, 868-877. (Pubitemid 29488446)
36. Hubank, M. & Schatz, D. G. (1994). Identifying differences in mRNA expression by representational difference analysis of cDNA. Nucleic Acids Res 22, 5640-5648.
37. Hynes, M. J., Murray, S. L., Duncan, A., Khew, G. S. & Davis, M. A. (2006). Regulatory genes controlling fatty acid catabolism and peroxisomal functions in the filamentous fungus Aspergillus nidulans. Eukaryot Cell 5, 794-805. (Pubitemid 43841389)
38. Kaminagakura, E., Bonan, P. R., Lopes, M. A., Almeida, O. P. & Scully, C. (2006). Cytokeratin expression in pseudoepitheliomatous hyperplasia of oral paracoccidioidomycosis. Med Mycol 44, 399-404. (Pubitemid 44173323)
39. Kim, M. J., Kil, M., Jung, J. H. & Kim, J. (2008). Roles of zinc-responsive transcription factor Csr1 in filamentous growth of the pathogenic yeast Candida albicans. J Microbiol Biotechnol 18, 242-247.
40. Krappmann, S., Bignell, E. M., Reichard, U., Rogers, T., Haynes, K. & Braus, G. H. (2004). The Aspergillus fumigatus transcriptional activator CpcA contributes significantly to the virulence of this fungal pathogen. Mol Microbiol 52, 785-799. (Pubitemid 38621748)
41. Kraus, P. R., Boily, M., Giles, S. S., Stajich, J. E., Allen, A. & Cox, G. M. (2004). Identification of Cryptococcus neoformans temperature-regulated genes with a genomic-DNA microarray. Eukaryot Cell 3, 1249-1260. (Pubitemid 39385233)
42. Kumamoto, C. A. & Vinces, M. D. (2005). Contributions of hyphae and hypha-co-regulated genes to Candida albicans virulence. Cell Microbiol 7, 1546-1554. (Pubitemid 41511912)
43. Kurokawa, C. S., Lopes, C. R., Sugizaki, M. F., Kuramae, E. E., Franco, M. F. & Peracoli, M. T. (2005). Virulence profile of ten Paracoccidioides brasiliensis isolates: association with morphologic and genetic patterns. Rev Inst Med Trop Sao Paulo 47, 257-262. (Pubitemid 41568600)
44. Laporte, D., Salin, B., Daignan-Fornier, B. & Sagot, I. (2008). Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J Cell Biol 181, 737-745. (Pubitemid 351786980)
45. Lawen, A. (2007). Another piece of the puzzle of apoptotic cytochrome c release. Mol Microbiol 66, 553-556.
46. Lee, A., Toffaletti, D. L., Tenor, J., Soderblom, E. J., Thompson, J. W., Moseley, M. A., Price, M. & Perfect, J. R. (2010). Survival defects of Cryptococcus neoformans mutants exposed to human cerebrospinal fluid result in attenuated virulence in an experimental model of meningitis. Infect Immun 78, 4213-4225.
47. Lengeler, K. B., Davidson, R. C., D'Souza, C., Harashima, T., Shen, W., Wang, P., Pan, X., Waugh, M. & Heitman, J. (2000). Signal transduction cascades regulating fungal development and virulence. Microbiol Mol Biol Rev 64, 746-785. (Pubitemid 32475930)
48. Lenzi, H. L., Calich, V. L. G., Mendes-Giannini, M. J. S., Xidieh, C. F., Miyaji, M., Mota, E. M., Machado, M. P. & Restrepo, A. (2000). Two patterns of extracellular matrix expression in experimental paracoccidioidomycosis. Med Mycol 38, S115-S119.
49. Lieu, H. Y., Song, H. S., Yang, S. N., Kim, J. H., Park, Y. D., Kim, H. J., Kim, H. Y. & Park, C. S. (2006). Identification of proteins affected by iron in Saccharomyces cerevisiae using proteome analysis. J Microbiol Biotechnol 16, 946-951.
50. T method. Methods 25, 402-408.
51. Lorenz, M. C. & Fink, G. R. (2001). The glyoxylate cycle is required for fungal virulence. Nature 412, 83-86. (Pubitemid 32851514)
52. Ludin, K. M., Hilti, N. & Schweingruber, M. E. (1995). Schizosaccharomyces pombe rds1, an adenine-repressible gene regulated by glucose, ammonium, phosphate, carbon dioxide and temperature. Mol Gen Genet 248, 439-445.
53. McKinney, J. D., Höner zu Bentrup, K., Muñoz-Elías, E. J., Miczak, A., Chen, B., Chan, W. T., Swenson, D., Sacchettini, J. C., Jacobs, W. R., Jr & Russell, D. G. (2000). Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406, 735-738.
54. Mendes-Giannini, M. J. S., Ricci, L. C., Uemura, M. A., Toscano, E. & Arns, C. W. (1994). Infection and apparent invasion of Vero cells by Paracoccidioides brasiliensis. J Med Vet Mycol 32, 189-197. (Pubitemid 24232760)
55. Mendes-Giannini, M. J. S., Hanna, S. A., Monteiro da Silva, J. L., Andreotti, P. F., Benard, G., Lenzi, H. L. & Soares, C. P. (2004). Invasion of epithelial mammalian cells by Paracoccidioides brasiliensis leads to cytoskeletal rearrangement and apoptosis of the host cell. Microbes Infect 6, 882-891.
56. Mendes-Giannini, M. J., Monteiro da Silva, J. L., de Fátima da Silva, J., Donofrio, F. C., Miranda, E. T., Andreotti, P. F. & Soares, C. P. (2008). Interactions of Paracoccidioides brasiliensis with host cells: recent advances. Mycopathologia 165, 237-248.
57. Moreno, M. A., Ibrahim-Granet, O., Vicentefranqueira, R., Amich, J., Ave, P., Leal, F., Latgé, J. P. & Calera, J. A. (2007). The regulation of zinc homeostasis by the ZafA transcriptional activator is essential for Aspergillus fumigatus virulence. Mol Microbiol 64, 1182-1197. (Pubitemid 46849011)
58. Morgan-Kiss, R. M. & Cronan, J. E. (2004). The Escherichia coli fadK (ydiD) gene encodes an anerobically regulated short chain acyl-CoA synthetase. J Biol Chem 279, 37324-37333. (Pubitemid 39195440)
59. Moscardi-Bacchi,M., Soares, A., Mendes, R., Marques, S. & Franco, M. (1989). In situ localization of T lymphocyte subsets in human paracoccidioidomycosis. J Med Vet Mycol 27, 149-158.
60. Muñoz-Elías, E. J. & McKinney, J. D. (2005). Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat Med 11, 638-644. (Pubitemid 40868304)
61. Narasipura, S.D., Ault, J. G.,Behr,M. J.,Chaturvedi, V. & Chaturvedi, S. (2003). Characterization of Cu,Zn superoxide dismutase (SOD1) gene knockout mutant of Cryptococcus neoformans var. gattii: role in biology and virulence. Mol Microbiol 47, 1681-1694. (Pubitemid 36363348)
62. Narasipura, S. D., Chaturvedi, V. & Chaturvedi, S. (2005). Characterization of Cryptococcus neoformans variety gattii SOD2 reveals distinct roles of the two superoxide dismutases in fungal biology and virulence. Mol Microbiol 55, 1782-1800. (Pubitemid 40445213)
63. Olivas, I., Royuela, M., Romero, B., Monteiro, M. C., Minguez, J. M., Laborda, F. & De Lucas, J. R. (2008). Ability to grow on lipids accounts for the fully virulent phenotype in neutropenic mice of Aspergillus fumigatus null mutants in the key glyoxylate cycle enzymes. Fungal Genet Biol 45, 45-60. (Pubitemid 350101284)
64. Pereira, C., Camougrand, N., Manon, S., Sousa, M. J. & Côrte-Real, M. (2007). ADP/ATP carrier is required for mitochondrial outer membrane permeabilization and cytochrome c release in yeast apoptosis. Mol Microbiol 66, 571-582. (Pubitemid 47621847)
65. Qazi, S. N., Counil, E., Morrissey, J., Rees, C. E., Cockayne, A., Winzer, K., Chan, W. C., Williams, P. & Hill, P. J. (2001). agr expression precedes escape of internalized Staphylococcus aureus from the host endosome. Infect Immun 69, 7074-7082. (Pubitemid 32995468)
66. Radisky, D. & Kaplan, J. (1999). Regulation of transition metal transport across the yeast plasma membrane. J Biol Chem 274, 4481-4484.
67. Ramírez, M. A. & Lorenz, M. C. (2009). The transcription factor homolog CTF1 regulates b-oxidation in Candida albicans. Eukaryot Cell 8, 1604-1614.
68. Ratledge, C. & Dover, L. G. (2000). Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54, 881-941.
69. Rosa e Silva, L. K., Staats, C. C., Goulart, L. S., Morello, L. G., Pelegrinelli Fungaro, M. H., Schrank, A. & Vainstein, M. H. (2008). Identification of novel temperature-regulated genes in the human pathogen Cryptococcus neoformans using representational difference analysis. Res Microbiol 159, 221-229.
70. Rosenshine, I., Duronio, V. & Finlay, B. B. (1992). Tyrosine protein kinase inhibitors block invasin-promoted bacterial uptake by epithelial cells. Infect Immun 60, 2211-2217.
71. Rude, T. H., Toffaletti, D. L., Cox, G. M. & Perfect, J. R. (2002). Relationship of the glyoxylate pathway to the pathogenesis of Cryptococcus neoformans. Infect Immun 70, 5684-5694.
72. Rutherford, J. C. & Bird, A. J. (2004). Metal-responsive transcription factors that regulate iron, zinc, and copper homeostasis in eukaryotic cells. Eukaryot Cell 3, 1-13. (Pubitemid 38237293)
73. San-Blas, G., Niño-Vega, G. & Iturriaga, T. (2002). Paracoccidioides brasiliensis and paracoccidioidomycosis: molecular approaches to morphogenesis, diagnosis, epidemiology, taxonomy and genetics. Med Mycol 40, 225-242. (Pubitemid 34752321)
74. Sanger, F., Nicklen, S. & Coulson, A. R. (1977). DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci U S A 74, 5463-5467.
75. Scully, C. & de Almeida, O. P. (1992). Orofacial manifestations of the systemic mycoses. J Oral Pathol Med 21, 289-294.
76. Sengupta, M. & Datta, A. (2003). Two membrane proteins located in the Nag regulon of Candida albicans confer multidrug resistance. Biochem Biophys Res Commun 301, 1099-1108. (Pubitemid 36279226)
77. Silva, G. M., Netto, L. E., Discola, K. F., Piassa-Filho, G. M., Pimenta, D. C., Bárcena, J. A. & Demasi, M. (2008). Role of glutaredoxin 2 and cytosolic thioredoxins in cysteinyl-based redox modification of the 20S proteasome. FEBS J 275, 2942-2955. (Pubitemid 351678681)
78. Singh, B. & Datta, A. (1979). Regulation of N-acetylglucosamine uptake in yeast. Biochim Biophys Acta 557, 248-258.
79. Singh, P., Ghosh, S. & Datta, A. (2001). Attenuation of virulence and changes in morphology in Candida albicans by disruption of the N-acetylglucosamine catabolic pathway. Infect Immun 69, 7898-7903. (Pubitemid 33086623)
80. Swanson, J. A. & Baer, S. C. (1995). Phagocytosis by zippers and triggers. Trends Cell Biol 5, 89-93.
81. Taborda, C. P., Silva, M. B., Nosanchuk, J. D. & Travassos, L. R. (2008). Melanin as a virulence factor of Paracoccidioides brasiliensis and other dimorphic pathogenic fungi: a minireview. Mycopathologia 165, 331-339. (Pubitemid 351585238)
82. Traba, J., Satrústegui, J. & Del Arco, A. (2009). Transport of adenine nucleotides in the mitochondria of Saccharomyces cerevisiae: interactions between the ADP/ATP carriers and the ATP-Mg/Pi carrier. Mitochondrion 9, 79-85.
83. Tuder, R. M., el Ibrahim, R., Godoy, C. E. & De Brito, T. (1985). Pathology of the human pulmonary paracoccidioidomycosis. Mycopathologia 92, 179-188.
84. Ullrich, O., Reinheckel, T., Sitte, N., Hass, R., Grune, T. & Davies, K. J. (1999). Poly-ADP ribose polymerase activates nuclear proteasome to degrade oxidatively damaged histones. Proc Natl Acad Sci U S A 96, 6223-6228. (Pubitemid 29256647)
85. Vázquez-Boland, J. A., Kuhn, M., Berche, P., Chakraborty, T., Domínguez-Bernal, G., Goebel, W., González-Zorn, B., Wehland, J. & Kreft, J. (2001). Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14, 584-640. (Pubitemid 32642752)
86. Zhao, H. & Eide, D. J. (1997). Zap1p, a metalloregulatory protein involved in zinc-responsive transcriptional regulation in Saccharomyces cerevisiae. Mol Cell Biol 17, 5044-5052. (Pubitemid 27357603)