Identification of ferrichrome- and ferrioxamine B-mediated iron uptake by Aspergillus fumigatus

Biochemical Journal

Volumn 473, Issue 9, 2016, Pages 1203-1213

  Park, Yong Sung ^a   Kim, Ju Yeon ^a   Yun, Cheol Won ^a  

^a Korea University   (South Korea)

Author keywords

Aspergillus fumigatus; Iron; Saccharomyces cerevisiae; Siderophore; Sit1; Sit2

Indexed keywords

FERRICHROME; FERRIOXAMINE; SIDEROPHORE; VIRULENCE FACTOR; CARRIER PROTEIN; DEFEROXAMINE; FERRIC ION; FUNGAL PROTEIN; IRON;

ARTICLE; ASPERGILLUS FUMIGATUS; BACTERIAL GROWTH; CELL MEMBRANE; DELETION MUTANT; DOWN REGULATION; FLUORESCENCE MICROSCOPY; FUNGUS GROWTH; GENE EXPRESSION; HL 60 CELL LINE; HUMAN; HUMAN CELL; IRON DEPLETION; IRON TRANSPORT; MALE; MOUSE; NONHUMAN; NORTHERN BLOTTING; PLASMID; PRIORITY JOURNAL; PROTOPLAST; SACCHAROMYCES CEREVISIAE; SOUTHERN BLOTTING; SURVIVAL RATE; UPREGULATION; YEAST CELL; ANIMAL; GENETICS; METABOLISM; PATHOGENICITY;

ANIMALS; ASPERGILLUS FUMIGATUS; CELL MEMBRANE; DEFEROXAMINE; FERRIC COMPOUNDS; FERRICHROME; FUNGAL PROTEINS; IRON; MEMBRANE TRANSPORT PROTEINS; MICE; VIRULENCE FACTORS;

EID: 84975247322     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20160066     Document Type: Article

References (42)

1. Halliwell, B. and Gutteridge, J.M. (1984) Oxygen toxicity, oxygen radicals, transition metals and disease. Biochem. J. 219, 1-14 CrossRef PubMed
2. Rawson, F.J., Downard, A.J. and Baronian, K.H. (2014) Electrochemical detection of intracellular and cell membrane redox systems in Saccharomyces cerevisiae. Sci. Rep. 4, 5216 CrossRef PubMed
3. Wofford, J.D. and Lindahl, P.A. (2015) Mitochondrial iron-sulfur cluster activity and cytosolic iron regulate iron traffic in Saccharomyces cerevisiae. J. Biol. Chem. 290, 26968-26977 CrossRef PubMed
4. Philpott, C.C. and Protchenko, O. (2008) Response to iron deprivation in Saccharomyces cerevisiae. Eukaryot. Cell 7, 20-27 CrossRef PubMed
5. Kaplan, J., McVey Ward, D., Crisp, R.J. and Philpott, C.C. (2006) Iron-dependent metabolic remodeling in S. cerevisiae. Biochim. Biophys. Acta 1763, 646-651 CrossRef PubMed
6. Neilands, J.B. (1995) Siderophores. structure and function of microbial iron transport compounds. J. Biol. Chem. 270, 26723-26726 CrossRef PubMed
7. Wang, W., Qiu, Z., Tan, H. and Cao, L. (2014) Siderophore production by actinobacteria. Biometals 27, 623-631 CrossRef PubMed
8. Haas, H., Eisendle, M. and Turgeon, B.G. (2008) Siderophores in fungal physiology and virulence. Annu. Rev. Phytopathol. 46, 149-187 CrossRef PubMed
9. Fiedler, H.-P., Krastel, P., ller, J.M., Gebhardt, K. and Zeeck, A. (2001) Enterobactin: the characteristic catecholate siderophore of Enterobacteriaceae is produced by Streptomyces species. FEMS Microbiol. Lett. 196, 147-151 CrossRef PubMed
10. Winkelmann, G. (2002) Microbial siderophore-mediated transport. Biochem. Soc. Trans. 30, 691-696 CrossRef PubMed
11. Miethke, M. and Marahiel, M.A. (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol. Biol. Rev. 71, 413-451 CrossRef PubMed
12. Georgatsou, E. and Alexandraki, D. (1994) Two distinctly regulated genes are required for ferric reduction, the first step of iron uptake in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 3065-3073 CrossRef PubMed
13. Stearman, R., Daniel, S, Yuan, Yamaguchi-lwai, Y., Klausner, R.D. and Dancis, A. (1996) A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271, 1552-1557 CrossRef PubMed
14. Dancis, A., Klausner, R.D., Hinnebusch, A.G. and Barriocanal, J.G. (1990) Genetic evidence that ferric reductase is required for iron uptake in Saccharomyces cerevisiae. Mol. Cell. Biol. 10, 2294-2301 CrossRef PubMed
15. Yun, C.-W., Ferea, T., Rashford, J., Ardoni, O., Brown, P.O., Botstein, D., Kaplani, J. and Philpott, C.C. (2000) Desferrioxamine-mediated iron uptake in Saccharomyces cerevisiae. J. Biol. Chem. 275, 10709-10715 CrossRef PubMed
16. Askwith, C., Eide, D., Ho, A.V., Bernard, P.S., Li, L., Davis-Kaplan, S., Sipe, D.M. and Kaplan, J. (1994) The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76, 403-410 CrossRef PubMed
17. Yun, C.W., Bauler, M., Moore, R.E., Klebba, P.E. and Philpott, C.C. (2001) 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 CrossRef PubMed
18. Lesuisse, E., Raguzzi, F. and Crichton, R.R. (1987) Iron uptake by the yeast Saccharomyces cerevisiae: involvement of a reduction step. J. Gen. Microbiol. 133, 3229-3236 PubMed
19. Lesuisse, E., Simon-Casteras, M. and Labbe, P. (1998) Siderophore-mediated iron uptake in Saccharomyces cerevisiae:theSIT1 gene encodes a ferrioxamine B permease that belongs to the major facilitator superfamily. Microbiology 144, 3455-3462 CrossRef PubMed
20. Heymann, P., Ernst, J.F. and Winkelmann, G. (1999) Identification of a fungal triacetylfusarinine C siderophore transport gene (TAF1)inSaccharomyces cerevisiae as a member of the major facilitator superfamily. Biometals 4, 301-306 CrossRef
21. Heymann, P., Ernst, J. and Winkelmann, G. (2000) A gene of the major facilitator superfamily encodes a transporter for enterobactin (Enb1p) in Saccharomyces cerevisiae. Biometals 13, 65-72 CrossRef PubMed
22. Yun, C. W. (2000) Siderophore-iron uptake in Saccharomyces cerevisiae. Identification of ferrichrome and fusarinine transporters. J. Biol. Chem. 275, 16354-16359 CrossRef PubMed
23. Heymann, P., Ernst, J.F. and Winkelmann, G. (2000) Identication and substrate specicity of a ferrichrome-type siderophore transporter (Arn1p) in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 186, 221-227 CrossRef PubMed
24. Hortschansky, P., Eisendle, M., Al-Abdallah, Q., Schmidt, A.D., Bergmann, S., Thön, M., Kniemeyer, O., Abt, B., Seeber, B., Werner, E.R. et al. (2007) Interaction of HapX with the CCAAT-binding complex-a novel mechanism of gene regulation by iron. EMBO J. 26, 3157-3168 CrossRef PubMed
25. Oberegger, H., Schoeser, M., Zadra, I., Abt, B. and Haas, H. (2001) SREA is involved in regulation of siderophore biosynthesis, utilization and uptake in Aspergillus nidulans. Mol. Microbiol. 41, 1077-1089 CrossRef PubMed
26. Haas, H., Schoeser, M., Lesuisse, E., Ernst, J.F., Parson, W., Abt, B., Winkelmann, G.N. and Oberegger, H. (2003) Characterization of the Aspergillus nidulans transporters for the siderophores enterobactin and triacetylfusarinine C. Biochem. J. 371, 505-513 CrossRef PubMed
27. Dagenais, T.R.T. and Keller, N.P. (2009) Pathogenesis of Aspergillus fumigatus in invasive aspergillosis. Clin. Microbiol. Rev. 22, 447-465 CrossRef PubMed
28. Lass-Flörl, C., Roilides, E., Löffler, J., Wilflingseder, D. and Romani, L. (2013) Minireview: host defence in invasive aspergillosis. Mycoses 56, 403-413 CrossRef PubMed
29. Latge, J.-P. (1999) Aspergillus fumigatus and aspergillosis. Clin. Microbiol. Rev. 12, 310-350 PubMed
30. Schrettl, M., Beckmann, N., Varga, J., Heinekamp, T., Jacobsen, I.D., Jochl, C., Moussa, T.A., Wang, S., Gsaller, F., Blatzer, M. et al. (2010) HapX-mediated adaption to iron starvation is crucial for virulence of Aspergillus fumigatus. PLoS Pathog. 6, e1001124 PubMed
31. Seifert, M., Nairz, M., Schroll, A., Schrettl, M., Haas, H. and Weiss, G. (2008) Effects of the Aspergillus fumigatus siderophore systems on the regulation of macrophage immune effector pathways and iron homeostasis. Immunobiology 213, 767-778 CrossRef PubMed
32. Raymond-Bouchard, I., Carroll, C.S., Nesbitt, J.R., Henry, K.A., Pinto, L.J., Moinzadeh, M., Scott, J.K. and Moore, M.M. (2012) Structural requirements for the activity of the MirB ferrisiderophore transporter of Aspergillus fumigatus. Eukaryot. Cell 11, 1333-1344 CrossRef PubMed
33. Schrettl, M. (2004) Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J. Exp. Med. 200, 1213-1219 CrossRef PubMed
34. Oberegger, H., Zadra, Schoeser, M., Abt, B., Parson, W. and Haas, H. (2002) Identification of members of the Aspergillus nidulans SREA regulon: genes involved in siderophore biosynthesis and utilization. Biochem. Soc. Trans. 30, 781-783 CrossRef PubMed
35. Hissen, A.H., Wan, A.N., Warwas, M.L., Pinto, L.J. and Moore, M.M. (2005) The Aspergillus fumigatus siderophore biosynthetic gene sidA, encoding L-ornithine-N5-oxygenase, is required for virulence. Infect. Immun. 73, 5493-5503 CrossRef PubMed
36. Schrettl, M., Bignell, E., Kragl, C., Sabiha, Y., Loss, O., Eisendle, M., Wallner, A., Herbert, Jr, N.A., Haynes, K. and Haas, H. (2007) Distinct roles for intra- and extracellular siderophores during Aspergillus fumigatus infection. PLoS Pathog. 3, 1195-1207 CrossRef PubMed
37. Haas, H. (2012) Iron - a key nexus in the virulence of Aspergillus fumigatus. Front. Microbiol. 3, 28 PubMed
38. Schrettl, M., Kim, H.S., Eisendle, M., Kragl, C., Nierman, W.C., Heinekamp, T., Werner, E.R., Jacobsen, I., Illmer, P., Yi, H. et al. (2008) SreA-mediated iron regulation in Aspergillus fumigatus. Mol. Microbiol. 70, 27-43 CrossRef PubMed
39. Moore, M.M. (2013) The crucial role of iron uptake in Aspergillus fumigatus virulence. Curr. Opin. Microbiol. 16, 692-699 CrossRef PubMed
40. Pontecorvo, G., Roper, J., Hemmons, L., Macdonald, K. and Bufton, A. (1953) The genetics of Aspergillus nidulans.Adv.Genet.5, 141-238 CrossRef PubMed
41. Brunelli, J.P. and Pall, M.L. (1993) A series of yeast/Escherichia coli lambda expression vectors designed for directional cloning of cDNAs and cre/lox-mediated plasmid excision. Yeast 9, 1309-1318 CrossRef PubMed
42. Schrettl, M. and Haas, H. (2011) Iron homeostasis - Achilles' heel of Aspergillus fumigatus? Curr. Opin. Microbiol. 14, 400-405 CrossRef PubMed