Iron gathering of opportunistic pathogenic fungi: A mini review

Acta Microbiologica et Immunologica Hungarica

Volumn 52, Issue 2, 2005, Pages 185-197

  Nyilasi, Ildikó ^a   Papp, T ^a   Tako M ^a   Nagy, Erzsébet ^a   Vagvolgyi Cs ^a  

^a UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Iron transport; Opportunistic mycosis; Siderophore; Virulence factor

Indexed keywords

ANTIFUNGAL AGENT; DEFEROXAMINE; FERRIC ION; HEME OXYGENASE; HEMIN; HYDROXIDE; HYDROXYACID; IRON; IRON CHELATING AGENT; OXIDE; OXYGENASE; SIDEROPHORE;

ACID SECRETION; BINDING AFFINITY; BIOSYNTHESIS; CATALYSIS; CONCENTRATION (PARAMETERS); CONFERENCE PAPER; FUNGUS; GENETICS; HUMAN; IRON BLOOD LEVEL; IRON OVERLOAD; IRON TRANSPORT; MEMBRANE; MICROBIAL GROWTH; MICROORGANISM; MOLECULAR WEIGHT; MUCORMYCOSIS; NONHUMAN; OXIDATION REDUCTION REACTION; TRANSPORT KINETICS; VIRULENCE;

FUNGI; MAMMALIA; ZYGOMYCETES;

EID: 20444441115     PISSN: 12178950     EISSN: None     Source Type: Journal    
DOI: 10.1556/AMicr.52.2005.2.4     Document Type: Conference Paper

References (75)

1. Singh, N.: Trends in the epidemiology of opportunistic fungal infections: predisposing factors and the impact of antimicrobial use practices. Clin Infect Dis 33, 1692-1696 (2001).
2. Walsh, T. J., Groll, A. H.: Emerging fungal pathogens: evolving challenges to immunocompromised patients for the twenty-first century. Transpl Infect Dis 1, 217-261 (1999).
3. Viviani, M. A., De Mareie, S., Graybill, J. R., Yamaguchi, H., Anaissie, E., Caillot, D.: New approaches in antifungal chemotherapy. Med Mycol 36, 194-206 (1999).
4. Weinberg, E. D.: The role of iron in protozoan and fungal infectious diseases. J Eukaryot Microbiol 46, 231-238 (1999).
5. Boelaert, J. R., Van Roost, G. F., Vergauwe, P. L., Verbanck, J. J., De Vroey, C., Segaert, M. F.: The role of deferoxamine in dialysis associated mucormycosis: report of three cases and review of the literature. Clin Nephrol 29, 261-266 (1988).
6. Prokopowicz, G. P., Barkley, S. F., Kauffman, C. A.: Indolent zygomycosis associated with deferoxamine chelation therapy. Mycoses 37, 427-431 (1994).
7. Boelaert, J. R., De Locht, M., Van Cutsem, J., Kerrels, V., Cantinieaux, B., Verdonck, A., Van Landuyt, H. W., Schneider, Y. J.: Mucormycosis during deferoxamine therapy is a siderophore-mediated infection: in vitro and in vivo animal studies. J Clin Investig 91, 1979-1986 (1993).
8. Reissbrodt, R., Kingsley, R., Rabsch, W., Beer, W., Roberts, M., Williams, P. H.: Iron-regulated excretion of α-keto acids by Salmonella typhimurium. J Bacteriol 179, 4538-4544 (1997).
9. Byers, B. R., Arceneaux, J. E. L.: Microbial iron transport: iron acquisition by pathogenic microorganisms. Metal Ions Biol Syst 35, 37-66 (1998).
10. Guerinot, M. L.: Microbial iron transport. Annu Rev Microbiol 48, 743-772 (1994).
11. Howard, D. H.: Acquisition, transport, and storage of iron by pathogenic fungi. Clin Microbiol Rev 12, 394-404 (1999).
12. Howard, D. H.: Iron gathering by zoopathogenic fungi. FEMS Immun and Med Microbiol 1641, 1-6 (2003).
13. Fekete, F. A., Chandhoke, V., Jellison, J.: Iron-binding compounds produced by wood-decaying basidiomycetes. Appl Environ Microbiol 55, 2720-2722 (1989).
14. Ismail, A., Bedell, G. W., Lupan, D. M.: Siderophore production by the pathogenic yeast, Candida albicans. Biochem Biophys Res Commun 130, 885-891 (1985).
15. Thieken, A., Winkelmann, G.: Rhizoferrin: A complexone type siderophore of the Mucorales and Entomophtorales (Zygomycetes). FEMS Microbiol Lett 94, 37-42 (1992).
16. Holzberg, M., Artis, W. M.: Hydroxamate siderophore production by opportunistic and systemic fungal pathogens. Infect Immun 40, 1134-1139 (1983).
17. Winkelmann, G.: Structures and functions of fungal siderophores containing hydroxamate and complexone type iron binding ligands. Mycol Res 96, 529-534 (1992).
18. van der Helm, D., Winkelmann, G.: Hydroxamates and polycarboxylates as iron transport agents (siderophores) in fungi. In: Winkelmann, G., Winge, D. R. (eds): Metal ions in fungi. Marcel Dekker, New York, 1994, pp. 39-98.
19. Renshaw, J. C., Robson, G. D., Trinci, A. P. J., Wiebe, M. G., Livens, F. R., Collison, D., Taylor, R. J.: Fungal siderophores: structures, functions and application. Mycol Res 106, 1123-1142 (2002).
20. Matzanke, B. F., Bill, E., Trautwein, A. X., Winkelmann, G.: Ferricrocin functions as the main intracellular iron-storage compound in mycelia of Neurospora crassa. Biol Metals 1, 18-25 (1988).
21. Ardon, O., Weizman, H., Libman, J., Shanzer, A., Chen, Y., Hadar, Y.: Iron uptake in Ustilago maydis: studies with fluorescent ferrichrome analogues. Microbiology 143, 3625-3631 (1997).
22. Müller, G., Barclay, S. J., Raymond, K. N.: The mechanism and specificity of iron transport in Rhodotorula pilmanae probed by synthetic analogs of rhodotorulic acid. J Biol Chem 260, 13916-13920 (1985).
23. Winkelmann, G.: Kinetics, energetics, and mechanisms of siderophore iron transport in fungi. In: Barton, L. L. (ed.): Iron chelation in plants and soil microorganisms. Academic Press, Inc., New York, 1993, pp. 219-239.
24. Kim, Y., Yun, C. W., Philpott, C. C.: Ferrichrome induces endosome to plasma membrane cycling of the ferrichrome transporter, Arn1p, in Saccharomyces cerevisiae. EMBO J 21, 3632-3642 (2002).
25. Yun, C. W., Ferea, T., Rashford, J., Ardon, O., Brown, P. O., Botstein, D., Kaplan, J., Philpott, C. C.: Desferrioxamine-mediated iron uptake in Saccharomyces cerevisiae. J Biol Chem 275, 10709-10715 (2000).
26. Lesuisse, E., Blaiseau, P. L., Dancis, A., Camadro, J. M.: Siderophore uptake and use by the yeast Saccharomyces cerevisiae. Microbiology 147, 289-298 (2001).
27. Matzanke, B. F.: Iron storage in fungi. In: Winkelmann, G., Winge, D. R. (eds): Metal ions in fungi. Marcel Dekker, New York, 1994, pp. 179-214.
28. Santos, R., Buisson, N., Knight, S., Dancis, A., Camadro, J. M., Lesuisse, E.: Haemin uptake and use as an iron source by Candida albicans: role of CaHMX1-encoded haem oxygenase. Microbiology 149, 579-588 (2003).
29. Timmerman, M. M., Woods, J. P.: Potential role for extracellular glutathione-dependent ferric reductase in utilization of environmental and host ferric compounds by Histoplasma capsulatum. Infect Immun 69, 7671-7678 (2001).
30. Foster, L-A. A.: Utilization and cell-surface binding of hemin by Histoplasma capsulatum. Can J Microbiol 48, 437-442 (2002).
31. Nyhus, K. J., Wilborn, A. T., Jacobson, E. S.: Ferric iron reduction by Cryptococcus neoformans. Infect Immun 65, 434-438 (1997).
32. Winkelmann, G.: Surface iron polymers and hydroxy acids. A model of iron supply in sideramine-free fungi. Arch Microbiol 121, 43-51 (1979).
33. Lesuisse, E., Labbe, P.: Reductive iron assimilation in Saccharomyces cerevisiae. In: Winkelmann, G., Winge, D. R. (eds): Metal ions in fungi. Marcel Dekker, New York, 1994, pp. 149-178.
34. Neilands, J. B., Konopka, K., Schwyn, B., Coy, M., Francis, R. T., Paw, B. H., Bagg, A.: Comparative biochemistry of microbial iron assimilation. In: Winkelmann, G., Winge, D. R. (eds): Iron transport in microbes, plants and animals. VCH Weinheim, New York, 1987, pp. 3-34.
35. Lesuisse, E., Labbe, P.: Reductive and non-reductive mechanisms of iron assimilation by the yeast Saccharomyces cerevisiae. J Gen Microbiol 135, 257-263 (1989).
36. Yun, C. W., Bauler, M., Moore, R. E., Klebba, P. E., Philpott, C. C.: The role of the FRE family of plasma membrane reductases in the uptake of siderophore-iron in Saccharomyces cerevisiae. J Biol Chem 276, 10218-10223 (2001).
37. Stearman, R., Yuan, D. S., Yamaguchi-Iwai, Y., Klausner, R. D., Dancis, A.: A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271, 1552-1557 (1996).
38. Askwith, C., Eide, D., Van Ho, A., Bernard, P. S., Li, L., Davis-Kaplan, S., Sipe, D. M., Kaplan, J.: The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76, 403-410 (1994).
39. Dix, D. R., Bridgham, J. T., Broderius, M. A., Byersdorfer, C. A., Eide, D. J.: The FET4 gene encodes the low affinity Fe(II) transport protein of Saccharomyces cerevisiae. J Biol Chem 269, 26092-26099 (1994).
40. Lesuisse, E., Simon-Casteras, M., Labbe, P.: Siderophore-mediated iron uptake in Saccharomyces cerevisiae: the SIT1 gene encodes a ferrioxamine B permease that belongs to the major facilitator superfamily. Microbiology 144, 3455-3462 (1998).
41. Heymann, P., Ernst, J. F., Winkelmann, G.: Identification of a fungal triacetylfusarinine C siderophore transport gene (TAF1) in Saccharomyces cerevisiae as a member of the major facilitator superfamily. Biometals 12, 301-306 (1999).
42. Heymann, P., Ernst, J. F., Winkelmann, G.: A gene of the major facilitator superfamily encodes a transporter for enterobactin (Enb1) in Saccharomyces cerevisiae. BioMetals 13, 65-72 (2000).
43. Heymann, P., Ernst, J. F., Winkelmann, G.: Identification and substrate specificity of a ferrichrome-type siderophore transporter (Arn1p) in Saccharomyces cerevisiae. FEMS Microbiol Lett 186, 221-227 (2000).
44. Yun, C. W., Tiederman, J. S., Moore, R. E., Philpott, C. C.: Siderophore-iron uptake in Saccharomyces cerevisiae. Identification of ferrichrome and fusarinine transporters. J Biol Chem 275, 16354-16359 (2000).
45. Yamaguchi-Iwai, Y., Dancis, A., Klausner, R. D.: AFT1: a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO J 14, 1231-1239 (1995).
46. Blaiseau, P. L., Lesuisse, E., Camadro, J. M.: Aft2p, a novel iron-regulated transcription activator that modulates, with Aft1p, intracellular iron use and resistance to oxidative stress in yeast. J Biol Chem 276, 34221-34226 (2001).
47. + is required for ferric iron uptake and encodes a protein that is homologous to the gp91-phox subunit of the human NADPH phagocyte oxidoreductase. Mol Cell Biol 13, 4342-4350 (1993).
48. Askwith, C., Kaplan, J.: An oxidase-permease-based iron transport system in Schizosaccharomyces pombe and its expression in Saccharomyces cerevisiae. J Biol Chem 272, 401-405 (1997).
49. Pelletier, B., Beaudoin, J., Mukai, Y., Labbé, S.: Fep1, an iron sensor regulating iron transporter gene expression in Schizosaccharomyces pombe. J Biol Chem 277, 22950-22958 (2002).
50. Pelletier, B., Beaudoin, J., Philpott, C. C., Labbé, S.: Fep1, represses expression of the fission yeast Schizosaccharomyces pombe siderophore-iron transport system. Nucl Acids Res 31, 4332-4344 (2003).
51. Ramanan, N., Wang, Y.: A high-affinity iron permease essential for Candida albicans. Science 288, 1062-1064 (2000).
52. Hammacott, J. E., Williams, P. H., Cashmore, A. M.: Candida albicans CFL1 encodes a functional ferric reductase activity that can rescue a Saccharomyces cerevisiae fre1 mutant. Microbiology 146, 869-876 (2000).
53. Eck, R., Hundt, S., Härtl, A., Ruemer, E., Künkel, W.: A multicopper oxidase gene from Candida albicans: cloning, characterization and disruption. Microbiology 145, 2415-2422 (1999).
54. Ardon, O., Bussey, H., Philpott, C., Ward, D., Davis-Kaplan, S., Verroneau, S., Jiang, B., Kaplan, J.: Identification of a Candida albicans ferrichrome transporter and its characterization by expression in Saccharomyces cerevisiae. J Biol Chem 276, 43049-43055 (2001).
55. Hu, C.-H., Bai, C., Zheng, X.-D., Wang, Y.-M., Wang, Y.: Characterization and functional analysis of the siderophore-iron transporter CaAm1p in Candida albicans. J Biol Chem 277, 30598-30605 (2002).
56. Heymann, P., Gerads, M., Schaller, M., Dromer, F., Winkelmann, G., Ernst, J. F.: The siderophore iron transporter of Candida albicans (Sit1p/Arn1p) mediates uptake of ferrichrome-type siderophores and is required for epithelial invasion. Infect Immun 70, 5246-5255 (2002).
57. th Congress of the International Society for Human and Animal Mycology, San Antonio, TX, 2003, No. 196, p. 421.
58. Lian, T., Simmer, M. I., D'Souza, C. A., Steen, B. R., Zuyderduyn, S. D., Jones, S. J. M., Marra, M. A., Kronstad, J. W.: Iron-regulated transcription and capsule formation in the fungal pathogen Cryptococcus neoformans. Mol Microbiol (in press).
59. Fu, Y., Lee, H., Collins, M., Tsai, H-F., Spellberg, B., Edwards, J. E., Kwon-Chung, K. J., Ibrahim, A. S.: Cloning and functional characterization of the Rhizopus oryzae high affinity permease (rFTR) gene. FEMS Microbiol Lett 235, 169-176 (2004).
60. de Locht, M. D., Boelaert, J. R., Schneider, Y.-J.: Iron uptake from ferrioxamine and from ferrirhizoferrin by germinating spores of Rhizopus microsporus. Biochem Pharmacol 47, 1843-1850 (1994).
61. Yuan, W. M., Gentil, G. D., Budde, A. D., Leong, S. A.: Characterization of the Ustilago maydis sid2 gene, encoding a multidomain peptide synthetase in the ferrichrome biosynthetic gene cluster. J Bacteriol 183, 4040-4051 (2001).
62. Wilhite, S. E., Lumsden, R. D., Straney, D. C.: Peptide synthetase gene in Trichoderma virens. Appl Environ Microbiol 67, 5055-5062 (2001).
63. Mei, B., Budde, A. D., Leong, S. A.: sid1, a gene initiating siderophore biosynthesis in Ustilago maydis: molecular characterization, regulation by iron and role in phytopathogenicity. Proc Nat Acad Sc USA 90, 903-907 (1993).
64. Voisard, C., Wang, J., McEvoy, J. L., Xu, P., Leong, S. A.: Urbs1, a gene regulating siderophore biosynthesis in Ustilago maydis, encodes a protein similar to the erythroid transcription factor GATA-1. Mol Cell Biol 13, 7091-7100 (1993).
65. Oberegger, H., Zadra, I., Schoeser, M., Abt, B., Parson, W., Haas, H.: Identification of members of the Aspergillus nidulans SREA regulon: genes involved in siderophore biosynthesis and utilization. Biochem Soc Trans 30, 781-783 (2002).
66. An, Z., Mei, B., Yuan, W. M., Leong, S. A.: The distal GATA sequences of the sid1 promoter of Ustilago maydis mediate iron repression of siderophore production and interact directly with Urbs1, a GATA family transcription factor. EMBO J 16, 1742-1750 (1997).
67. Zhou, L., Marzluf, G. A.: Functional analysis of the two zinc fingers of SRE, a GATA-type factor negatively regulates siderophore synthesis in Neurospora crassa. Biochem 38, 4335-4341 (1999).
68. Oberegger, H., Schoeser, M., Zadra, I., Abt, B., Haas, H.: SREA is involved in regulation of siderophore biosynthesis, utilization and uptake in Aspergillus nidulans. Mol Microbiol 41, 1077-1089 (2001).
69. Haas, H., Angermayr, K., Stöffler, G.: Molecular analysis of a Penicillium chrysogenum GATA factor encoding gene (sreP) exhibiting significant homology to the Ustilago maydis Urbs1 gene. Gene 184, 33-37 (1997).
70. Haas, H.: Molecular genetics of fungal siderophore biosynthesis and uptake: the role of siderophores in iron uptake and storage. Appl Microbiol Biotechnol 62, 316-330 (2003).
71. 5-monooxygenase (sidA) and a nonribosomal peptide synthetase (sidC). Mol Microbiol 49, 359-375 (2003).
72. Vergne, A. F., Walz, A. J., Miller, M. J.: Iron chelators from mycobacteria (1954-1999) and potencial therapeutic applications. Natural Product Reports 17, 99-116 (2000).
73. Ghosh, M., Miller, M. J.: Design, synthesis, and biological evaluation of isocyanaurate-based antifungal macrolide antibiotic conjugates: iron transport-mediated drug delivery. Biorg Med Chem 3, 1519-1525 (1995).
74. Lu, Y., Miller, M. J.: Syntheses and studies of multiwarhead siderophore-5-fluorouridine conjugates. Biorg Med Chem 7, 3025-3038 (1999).
75. Bernier, G., Girijavallabhan, V., Murray, A., Niyaz, N., Ding, P., Miller, M. J., Malouin, F.: Desketoneoenactin-siderophore conjugates for Candida: Evidence of iron transport-dependent species selectivity. Antimicrob Agents Chemother 49, 241-248 (2005).