Aspergillus fumigatus survival in alkaline and extreme zinc-limiting environments relies on the induction of a zinc homeostasis system encoded by the zrfc and aspf2 genes

Eukaryotic Cell

Volumn 9, Issue 3, 2010, Pages 424-437

  Amich, Jorge ^a   Vicentefranqueira, Rocío ^a   Leal, Fernando ^a   Calera, José Antonio ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALLERGEN ASP F 2, ASPERGILLUS FUMIGATUS; CATION TRANSPORT PROTEIN; COMPLEMENTARY DNA; FUNGAL PROTEIN; PACC PROTEIN, ASPERGILLUS; SACCHAROMYCES CEREVISIAE PROTEIN; TRANSACTIVATOR PROTEIN; TRANSCRIPTION FACTOR; ZINC; ZRT1 PROTEIN, S CEREVISIAE; ZRT2 PROTEIN, S CEREVISIAE;

AMINO ACID SEQUENCE; ARTICLE; ASPERGILLUS FUMIGATUS; CELL PROLIFERATION; CELL SURVIVAL; CHEMICAL STRUCTURE; DOWN REGULATION; DRUG EFFECT; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE STRUCTURE; GENETIC TRANSFECTION; GENETICS; HOMEOSTASIS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PH; PHYLOGENY; PHYSIOLOGY; PROTEIN MOTIF; SACCHAROMYCES CEREVISIAE; SEQUENCE HOMOLOGY; UPREGULATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ASPERGILLUS FUMIGATUS; CATION TRANSPORT PROTEINS; CELL PROLIFERATION; CELL SURVIVAL; DNA, COMPLEMENTARY; DOWN-REGULATION; FUNGAL PROTEINS; GENE COMPONENTS; GENE DELETION; GENE EXPRESSION; GENE EXPRESSION REGULATION, FUNGAL; HOMEOSTASIS; HYDROGEN-ION CONCENTRATION; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFECTION; UP-REGULATION; ZINC;

ASPERGILLUS; ASPERGILLUS FUMIGATUS; FUNGI;

EID: 77649332351     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00348-09     Document Type: Article

References (58)

1. Amich, J., F. Leal, and J. A. Calera. 2009. Repression of the acid ZrfA/ZrfB zinc-uptake system of Aspergillus fumigatus mediated by PacC under neutral, zinc-limiting conditions. Int. Microbiol. 12:39-47.
2. Auld, D. S. 2001. Zinc coordination sphere in biochemical zinc sites. Biometals 14:271-313.
3. Banerjee, B., P. A. Greenberger, J. N. Fink, and V. P. Kurup. 1998. Immunological characterization of Aspf2, a major allergen from Aspergillus fumigatus associated with allergic bronchopulmonary aspergillosis. Infect. Immun. 66:5175-5182.
4. Basta, N. T., J. A. Ryan, and R. L. Chaney. 2005. Trace element chemistry in residual-treated soil: key concepts and metal bioavailability. J. Environ. Qual. 34:49-63.
5. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
6. Bignell, E., S. Negrete-Urtasun, A. M. Calcagno, K. Haynes, H. N. Arst, Jr., and T. Rogers. 2005. The Aspergillus pH-responsive transcription factor PacC regulates virulence. Mol. Microbiol. 55:1072-1084.
7. 2 sensors to regulate transcriptional activation domain function. EMBO J. 22:5137-5146.
8. Calera, J. A., and H. Hass. 2009. Cations (Zn, Fe), p. 107-129. In J. P. Latgé and W. J. Steinbach (ed.), Aspergillus fumigatus and aspergillosis. ASM Press, Washington, DC.
9. Calera, J. A., M. C. Ovejero, R. López-Medrano, M. Segurado, P. Puente, and F. Leal. 1997. Characterization of the Aspergillus nidulans aspnd1 gene demonstrates that the ASPND1 antigen, which it encodes, and several Aspergillus fumigatus immunodominant antigens belong to the same family. Infect. Immun. 65:1335-1344.
10. Cserzö, M., E. Wallin, I. Simon, G. von Heijne, and A. Elofsson. 1997. Prediction of transmembrane alpha-helices in prokaryotic membrane proteins: the dense alignment surface method. Protein Eng. 10:673-676.
11. d'Enfert, C. 1996. Selection of multiple disruption events in Aspergillus fumigatus using the orotidine-5 -decarboxylase gene, pyrG, as a unique transformation marker. Curr. Genet. 30:76-82.
12. Eide, D. J. 2006. Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta 1763:711-722.
13. Espeso, E. A., J. Tilburn, L. Sanchez-Pulido, C. V. Brown, A. Valencia, H. N. Arst Jr., and M. A. Penalva. 1997. Specific DNA recognition by the Aspergillus nidulans three zinc finger transcription factor PacC. J. Mol. Biol. 274: 466-480.
14. Fedorova, N. D., N. Khaldi, V. S. Joardar, R. Maiti, P. Amedeo, M. J. Anderson, J. Crabtree, J. C. Silva, J. H. Badger, A. Albarraq, S. Angiuoli, H. Bussey, P. Bowyer, P. J. Cotty, P. S. Dyer, A. Egan, K. Galens, C. M. Fraser-Liggett, B. J. Haas, J. M. Inman, R. Kent, S. Lemieux, I. Malavazi, J. Orvis, T. Roemer, C. M. Ronning, J. P. Sundaram, G. Sutton, G. Turner, J. C. Venter, O. R. White, B. R. Whitty, P. Youngman, K. H. Wolfe, G. H. Goldman, J. R. Wortman, B. Jiang, D. W. Denning, and W. C. Nierman. 2008. Genomic islands in the pathogenic filamentous fungus Aspergillus fumigatus. PcLoS Genet. 4e1000046.
15. Fushimi, N., C. E. Ee, T. Nakajima, and E. Ichishima. 1999. Aspzincin, a family of metalloendopeptidases with a new zinc-binding motif. J. Biol. Chem. 274:24195-24201.
16. Gitan, R. S., H. Luo, J. Rodgers, M. Broderius, and D. Eide. 1998. Zinc-induced inactivation of the yeast ZRT1 zinc transporter occurs through endocytosis and vacuolar degradation. J. Biol. Chem. 273:28617-28624.
17. Hahne, H. C. H., and W. Kroontje. 1973. Significance of pH and chloride concentration on behaviour of heavy metal pollutants: mercury (II), cadminum (II), zinc (II), and lead (II). J. Environ. Qual. 2:444-450.
18. Jensen, L. T., M. Ajua-Alemanji, and V. C. Culotta. 2003. The Saccharomyces cerevisiae high affinity phosphate transporter encoded by PHO84 also functions in manganese homeostasis. J. Biol. Chem. 278:42036-42040.
19. Kenward, A. G., L. J. Bartolotti, and C. S. Burns. 2007. Copper and zinc promote interactions between membrane-anchored peptides of the metal binding domain of the prion protein. Biochemistry 46:4261-4271.
20. Lamb, T. M., and A. P. Mitchell. 2003. The transcription factor Rim101p governs ion tolerance and cell differentiation by direct repression of the regulatory genes NRG1 and SMP1 in Saccharomyces cerevisiae. Mol. Cell. Biol. 23:677-686.
21. Lamb, T. M., W. Xu, A. Diamond, and A. P. Mitchell. 2001. Alkaline response genes of Saccharomyces cerevisiae and their relationship to the RIM101 pathway. J. Biol. Chem. 276:1850-1856.
22. Li, W., and A. P. Mitchell. 1997. Proteolytic activation of Rim1p, a positive regulator of yeast sporulation and invasive growth. Genetics 145:63-73.
23. Lyons, T. J., A. P. Gasch, L. A. Gaither, D. Botstein, P. O. Brown, and D. J. Eide. 2000. Genome-wide characterization of the Zap1p zinc-responsive regulon in yeast. Proc. Natl. Acad. Sci. USA 97:7957-7962.
24. Martínez, C. E., and H. L. Motto. 2000. Solubility of lead, zinc and copper added to mineral soils. Environ. Pollut. 107:153-158.
25. Matthews, T. M., and C. Webb. 1991. Culture systems, p. 249-289. In M. F. Tuite and S. G. Oliver (ed.), Saccharomyces, vol. 4. Plenum Press, New York, NY.
26. Mitton, K. P., P. K. Swain, S. Chen, S. Xu, D. J. Zack, and A. Swaroop. 2000. The leucine zipper of NRL interacts with the CRX homeodomain. A possible mechanism of transcriptional synergy in rhodopsin regulation. J. Biol. Chem. 275:29794-29799.
27. Moreno, M. A., J. Amich, R. Vicentefranqueira, F. Leal, and J. A. Calera. 2007. Culture conditions for zincand pH-regulated gene expression studies in Aspergillus fumigatus. Int. Microbiol. 10:187-192.
28. Moreno, M. A., O. Ibrahim-Granet, R. Vicentefranqueira, J. Amich, P. Ave, F. Leal, J. P. Latge, and J. A. Calera. 2007. The regulation of zinc homeostasis by the ZafA transcriptional activator is essential for Aspergillus fumigatus virulence. Mol. Microbiol. 64:1182-1197.
29. Nierman, W. C., A. Pain, M. J. Anderson, J. R. Wortman, H. S. Kim, J. Arroyo, M. Berriman, K. Abe, D. B. Archer, C. Bermejo, J. Bennett, P. Bowyer, D. Chen, M. Collins, R. Coulsen, R. Davies, P. S. Dyer, M. Farman, N. Fedorova, N. Fedorova, T. V. Feldblyum, R. Fischer, N. Fosker, A. Fraser, J. L. García, M. J. García, A. Goble, G. H. Goldman, K. Gomi, S. Griffith-Jones, R. Gwilliam, B. Haas, H. Haas, D. Harris, H. Horiuchi, J. Huang, S. Humphray, J. Jiménez, N. Keller, H. Khouri, K. Kitamoto, T. Kobayashi, S. Konzack, R. Kulkarni, T. Kumagai, A. Lafon, J. P. Latge, W. Li, A. Lord, C. Lu, W. H. Majoros, G. S. May, B. L. Miller, Y. Mohamoud, M. Molina, M. Monod, I. Mouyna, S. Mulligan, L. Murphy, S. O'Neil, I. Paulsen, M. A. Peñalva, M. Pertea, C. Price, B. L. Pritchard, M. A. Quail, E. Rabbinowitsch, N. Rawlins, M. A. Rajandream, U. Reichard, H. Renauld, G. D. Robson, S. Rodríguez de Córdoba, J. M. Rodríguez-Peña, C. M. Ronning, S. Rutter, S. L. Salzberg, M. Sánchez, J. C. Sánchez-Ferrero, D. Saunders, K. Seeger, R. Squares, S. Squares, M. Takeuchi, F. Tekaia, G. Turner, C. R. Vazquez de Aldana, J. Weidman, O. White, J. Woodward, J. H. Yu, C. Fraser, J. E. Galagan, K. Asai, M. Machida, N. Hall, B. Barrell, and D. W. Denning. 2005. Genomic sequence of the pathogenic and allergenic filamentous fungus Aspergillus fumigatus. Nature 438:1151-1156.
30. Pauly, P. C., and D. A. Harris. 1998. Copper stimulates endocytosis of the prion protein. J. Biol. Chem. 273:33107-33110.
31. Peñalva, M. A., and H. N. Arst, Jr. 2004. Recent advances in the characterization of ambient pH regulation of gene expression in filamentous fungi and yeasts. Annu. Rev. Microbiol. 58:425-451.
32. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
33. Sandrin, T. R., and R. M. Maier. 2003. Impact of metals on the biodegradation of organic pollutants. Environ. Health Perspect. 111:1093-1101.
34. Segal, B. H. 2009. Aspergillosis. N. Engl. J. Med. 360:1870-1884.
35. Serrano, R., D. Bernal, E. Simón, and J. Ariño. 2004. Copper and iron are the limiting factors for growth of the yeast Saccharomyces cerevisiae in an alkaline environment. J. Biol. Chem. 279:19698-19704.
36. Serrano, R., A. Ruíz, D. Bernal, J. R. Chambers, and J. Ariño. 2002. The transcriptional response to alkaline pH in Saccharomyces cerevisiae: evidence for calcium-mediated signalling. Mol. Microbiol. 46:1319-1333.
37. Soller, B. R., T. Khan, J. Favreau, C. Hsi, J. C. Puyana, and S. O. Heard. 2003. Investigation of muscle pH as an indicator of liver pH and injury from hemorrhagic shock. J. Surg. Res. 114:195-201.
38. Tapiero, H., and K. D. Tew. 2003. Trace elements in human physiology and pathology: zinc and metallothioneins. Biomed. Pharmacother. 57:399-411.
39. Tatsumi, H., K. Ikegaya, S. Murakami, H. Kawabe, E. Nakano, and H. Motai. 1994. Elucidation of the thermal stability of the neutral proteinase II from Aspergillus oryzae. Biochim. Biophys. Acta 1208:179-185.
40. Taylor, K. M., and R. I. Nicholson. 2003. The LZT proteins; the LIV-1 subfamily of zinc transporters. Biochim. Biophys. Acta 1611:16-30.
41. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
42. Tilburn, J., S. Sarkar, D. A. Widdick, E. A. Espeso, M. Orejas, J. Mungroo, M. A. Peñalva, and H. N. Arst, Jr. 1995. The Aspergillus PacC zinc finger transcription factor mediates regulation of both acidand alkaline-expressed genes by ambient pH. EMBO J. 14:779-790.
43. Uetz, P., L. Giot, G. Cagney, T. A. Mansfield, R. S. Judson, J. R. Knight, D. Lockshon, V. Narayan, M. Srinivasan, P. Pochart, A. Qureshi-Emili, Y. Li, B. Godwin, D. Conover, T. Kalbfleisch, G. Vijayadamodar, M. Yang, M. Johnston, S. Fields, and J. M. Rothberg. 2000. A comprehensive analysis of protein-protein interactions in Saccharomyces cerevisiae. Nature 403:623-627.
44. van der Rest, M. E., A. H. Kamminga, A. Nakano, Y. Anraku, B. Poolman, and W. N. Konings. 1995. The plasma membrane of Saccharomyces cerevisiae: structure, function, and biogenesis. Microbiol. Rev. 59:304-322.
45. Vicentefranqueira, R., M. A. Moreno, F. Leal, and J. A. Calera. 2005. The zrfA and zrfB genes of Aspergillus fumigatus encode the zinc transporter proteins of a zinc uptake system induced in an acid, zinc-depleted environment. Eukaryot. Cell 4:837-848.
46. von Heijne, G. 1992. Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. J. Mol. Biol. 225:487-494.
47. Wang, Z., L. S. Feng, V. Matskevich, K. Venkataraman, P. Parasuram, and J. H. Laity. 2006. Solution structure of a Zap1 zinc-responsive domain provides insights into metalloregulatory transcriptional repression in Saccharomyces cerevisiae. J. Mol. Biol. 357:1167-1183.
48. Waters, B. M., and D. J. Eide. 2002. Combinatorial control of yeast FET4 gene expression by iron, zinc, and oxygen. J. Biol. Chem. 277:33749-33757.
49. Watt, N. T., and N. M. Hooper. 2003. The prion protein and neuronal zinc homeostasis. Trends Biochem. Sci. 28:406-410.
50. Weidner, G., C. d'Enfert, A. Koch, P. C. Mol, and A. A. Brakhage. 1998. Development of a homologous transformation system for the human pathogenic fungus Aspergillus fumigatus based on the pyrG gene encoding orotidine 5 -monophosphate decarboxylase. Curr. Genet. 33:378-385.
51. Wheeler, K. A., B. F. Hurdman, and J. I. Pitt. 1991. Influence of pH on the growth of some toxigenic species of Aspergillus, Penicillium and Fusarium. Int. J. Food Microbiol. 12:141-149.
52. Xu, W., and A. P. Mitchell. 2001. Yeast PalA/AIP1/Alix homolog Rim20p associates with a PEST-like region and is required for its proteolytic cleavage. J. Bacteriol. 183:6917-6923.
53. Zahn, R. 2003. The octapeptide repeats in mammalian prion protein constitute a pH-dependent folding and aggregation site. J. Mol. Biol. 334:477-488.
54. Zhang, X., and T. F. Smith. 1998. Yeast "operons." Microb. Comp. Genomics 3:133-140.
55. Zhao, H., E. Butler, J. Rodgers, T. Spizzo, S. Duesterhoeft, and D. Eide. 1998. Regulation of zinc homeostasis in yeast by binding of the ZAP1 transcriptional activator to zinc-responsive promoter elements. J. Biol. Chem. 273:28713-28720.
56. Zhao, H., and D. Eide. 1996. The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. Proc. Natl. Acad. Sci. USA 93:2454-2458.
57. Zhao, H., and D. Eide. 1996. The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J. Biol. Chem. 271:23203-23210.
58. Zhou, Q., R. W. Gedrich, and D. A. Engel. 1995. Transcriptional repression of the c-fos gene by YY1 is mediated by a direct interaction with ATF/ CREB. J. Virol. 69:4323-4330.