Characterization of the Aspergillus nidulans transporters for the siderophores enterobactin and triacetylfusarinine C

Biochemical Journal

Volumn 371, Issue 2, 2003, Pages 505-513

  Haas, Hubertus ^a   Schoeser, Michelle ^a,f   Lesuisse, Emmanuel ^b   Ernst, Joachim F ^c   Parson, Walther ^d   Abt, Beate ^a   Winkelmann, Günther ^e   Oberegger, Harald ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

^b INSTITUT JACQUES MONOD   (France)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^e UNIVERSITY OF TÜBINGEN   (Germany)

^f NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Fungi; Iron uptake; Major facilitator; Phylogenetic analysis

Indexed keywords

BIOSYNTHESIS; CHROMOSOMES; COMPOSITION; IRON;

SIDEROPHORES;

BIOCHEMISTRY;

COMPLEMENTARY DNA; ENTEROCHELIN; IRON; SIDEROPHORE; TRIACETYLFUSARININE C; UNCLASSIFIED DRUG;

ARTICLE; ASCOMYCETES; ASPERGILLUS NIDULANS; BIOSYNTHESIS; CHROMOSOMAL LOCALIZATION; EXPRESSED SEQUENCE TAG; FUNGUS; GENE EXPRESSION; GENOME; IRON TRANSPORT; NONHUMAN; NORTHERN BLOTTING; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; ASPERGILLUS NIDULANS; BACTERIAL OUTER MEMBRANE PROTEINS; CARRIER PROTEINS; CLONING, MOLECULAR; CONSENSUS SEQUENCE; DNA PRIMERS; ENTEROBACTIN; EXONS; INTRONS; IRON; MEMBRANE TRANSPORT PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMIDS; POLYMERASE CHAIN REACTION; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; SIDEROPHORES;

ASCOMYCOTA; ASPERGILLUS; EMERICELLA NIDULANS; FUNGI; SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0038523854     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20021685     Document Type: Article

References (58)

1. Bagg, A. and Neilands, J. B. (1987) Molecular mechanism of regulation of siderophore-mediated iron assimilation. Microbiol. Rev. 51, 509-518
2. Leong, S. A. and Winkelmann, G. (1998) Molecular biology of iron transport in fungi. Met. Ions Biol. Syst. 35, 147-186
3. De Luca, N. G. and Wood, P. M. (2000) Iron uptake by fungi: contrasted mechanisms with internal or external reduction. Adv. Microb. Physiol. 43, 39-74
4. Weinberg, E. D. (1999) The role of iron in protozoan and fungal infectious diseases. J. Eukaryotic Microbiol. 46, 231-238
5. Roosenberg, J. M., Lin, Y. M., Lu, Y. and Miller, M. J. (2000) Studies and syntheses of siderophores, microbial iron chelators, and analogs as potential drug delivery agents. Curr. Med. Chem. 7, 159-197
6. Lesuisse, E. and Labbe, P. (1989) Reductive and non-reductive mechanisms of iron assimilation by the yeast Saccharomyces cerevisiae. J. Gen. Microbiol. 135, 257-263
7. Dancis, A., Roman, D. G., Anderson, G. J., Hinnebusch, A. G. and Klausner, R. D. (1992) Ferric reductase of Saccharomyces cerevisiae: molecular characterization, role in iron uptake, and transcriptional control by iron. Proc. Natl. Acad. Sci. U.S.A. 89, 3869-3873
8. 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
9. 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
10. Askwith, C., Eide, D., Van Ho, A., 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 (Cambridge, Mass.) 76, 403-410
11. Stearman, R., Yuan, D. S., Yamaguchi-Iwai, Y., Klausner, R. D. and Dancis, A. (1996) A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science (Washington, D.C.) 271, 1552-1557
12. Yun, C. W., Ferea, T., Rashford, J., Ardon, O., Brown, P. O., Botstein, D., Kaplan, J. and Philpott, C. C. (2000) Desferrioxamine-mediated iron uptake in Saccharomyces cerevisiae. Evidence for two pathways of iron uptake. J. Biol. Chem. 275, 10709-10715
13. Lesuisse, E., Simon-Casteras, M. and Labbe, P. (1998) 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
14. Heymann, P., Ernst, J. F. and Winkelmann, G. (1999) 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
15. Heymann, P., Ernst, J. F. and Winkelmann, G. (2000) A gene of the major facilitator superfamily encodes a transporter for enterobactin (Enb1p) in Saccharomyces cerevisiae. Biometals 13, 65-72
16. Heymann, P., Ernst, J. F. and Winkelmann, G. (2000) Identification and substrate specificity of a ferrichrome-type siderophore transporter (Arn1p) in Saccharomyces cerevisiae. FEMS Microbiol. Lett. 186, 221-227
17. Yun, C. W., Tiedeman, J. S., Moore, R. E. and Philpott, C. C. (2000) Siderophore-iron uptake in Saccharomyces cerevisiae. Identification of ferrichrome and fusarinine transporters. J. Biol. Chem. 275, 16354-16359
18. Yamaguchi-Iwai, Y., Dancis, A. and Klausner, R. D. (1995) AFT1: a mediator of iron regulated transcriptional control in Saccharomyces cerevisiae. EMBO J. 14, 1231-1239
19. Blaiseau, P. L., Lesuisse, E. and Camadro, J. M. (2001) 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
20. Robertson, L. S., Causton, H. C., Young, R. A. and Fink, G. R. (2000) The yeast A kinases differentially regulate iron uptake and respiratory function. Proc. Natl. Acad. Sci. U.S.A. 97, 5984-5988
21. Lesuisse, E., Blaiseau, P. L., Dancis, A. and Camadro, J. M. (2001) Siderophore uptake and use by the yeast Saccharomyces cerevisiae. Microbiology 147, 289-298
22. Weissman, Z., Shemer, R. and Kornitzer, D. (2002) Deletion of the copper transporter CaCCC2 reveals two distinct pathways for iron acquisition in Candida albicans. Mol. Microbiol. 44, 1551-1560
23. Heymann, P., Gerads, M., Schaller, M., Dromer, F., Winkelmann, G. and Ernst, J. F. (2002) 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
24. Eck, R., Hundt, S., Hartl, A., Roemer, E. and Kunkel, W. (1999) A multicopper oxidase gene from Candida albicans: cloning, characterization and disruption. Microbiology 145, 2415-2422
25. Ramanan, N. and Wang, Y. (2000) A high-affinity iron permease essential for Candida albicans virulence. Science (Washington, D.C.) 288, 1062-1064
26. Knight, S. A., Lesuisse, E., Stearman, R., Klausner, R. D. and Dancis, A. (2002) Reductive iron uptake by Candida albicans: role of copper, iron and the TUP1 regulator. Microbiology 148, 29-40
27. Ismail, A., Bedell, G. W. and Lupan, D. M. (1985) Siderophore production by the pathogenic yeast, Candida albicans. Biochem. Biophys. Res. Commun. 130, 885-891
28. Sweet, S. P. and Douglas, L. J. (1991) Effect of iron concentration on siderophore synthesis and pigment production by Candida albicans. FEMS Microbiol. Lett. 64, 87-91
29. Ardon, O., Bussey, H., Philpott, C., Ward, D. M., Davis-Kaplan, S., Verroneau, S., Jiang, B. and Kaplan, J. (2001) Identification of a Candida albicans ferrichrome transporter and its characterization by expression in Saccharomyces cerevisiae. J. Biol. Chem. 276, 43049-43055
30. Lesuisse, E., Knight, S. A., Camadro, J. M. and Dancis, A. (2002) Siderophore uptake by Candida albicans: effect of serum treatment and comparison with Saccharomyces cerevisiae. Yeast 19, 329-340
31. Hu, C. J., Bai, C., Zheng, X. D., Wang, Y. M. and Wang, Y. (2002) Characterization and functional analysis of the siderophore-Fe transporter CaArn1p in Candida albicans. J. Biol. Chem. 277, 30598-30605
32. Latge, J. P. (1999) Aspergillus fumigatus and aspergillosis. Clin. Microbiol. Rev. 12, 310-350
33. Brookman, J. L. and Denning, D. W. (2000) Molecular genetics in Aspergillus fumigatus. Curr. Opin. Microbiol. 3, 468-474
34. 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
35. Haas, H., Zadra, I., Stoffler, G. and Angermayr, K. (1999) The Aspergillus nidulans GATA factor SREA is involved in regulation of siderophore biosynthesis and control of iron uptake. J. Biol. Chem. 274, 4613-4619
36. Oberegger, H., Zadra, I., 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
37. Pontecorvo, G., Roper, J. A., Hemmons, L. M., MacDonald, K. D. and Bufton, A. W. J. (1953) The genetics of Aspergillus nidulans. Adv. Genet. 5, 141-238
38. Payne, S. M. (1994) Detection, isolation, and characterization of siderophores. Methods Enzymol. 235, 329-344
39. Sambrook, J., Fritsch, E. F. and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
40. Zadra, I., Abt, B., Parson, W. and Haas, H. (2000) xylP promoter-based expression system and its use for antisense downregulation of the Penicillium chrysogenum nitrogen regulator NRE. Appl. Environ. Microbiol. 66, 4810-4816
41. Upshall, A., Gilbert, T., Saari, G., O'Hara, P. J., Weglenski, P., Berse, B., Miller, K. and Timberlake, W. E. (1986) Molecular analysis of the argB gene of Aspergillus nidulans. Mol. Gen. Genet. 204, 349-354
42. Tilburn, J., Sarkar, S., Widdick, D. A., Espeso, E. A., Orejas, M., Mungroo, J., Penalva, M. A. and Arst, Jr, H. N. (1995) The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid- and alkaline-expressed genes by ambient pH. EMBO J. 14, 779-790
43. Punt, P. J., Greaves, P. A., Kuyvenhoven, A., van Deutekom, J. C., Kinghorn, J. R., Pouwels, P. H. and van den Hondel, C. A. (1991) A twin-reporter vector for simultaneous analysis of expression signals of divergently transcribed, contiguous genes in filamentous fungi. Gene 104, 119-122
44. Konetschny-Rapp, S., Huschka, H. G., Winkelmann, G. and Jung, G. (1988) High-performance liquid chromatography of siderophores from fungi. Biol. Met. 1, 9-17
45. Wiebe, C. and Winkelmann, G. (1975) Kinetic studies on the specificity of chelate-iron uptake in Aspergillus. J. Bacteriol. 123, 837-842
46. Fidel, S., Doonan, J. H. and Morris, N. R. (1988) Aspergillus nidulans contains a single actin gene which has unique intron locations and encodes a γ-actin. Gene 70, 283-293
47. Higgins, D. G., Thompson, J. D. and Gibson, T. J. (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 266, 383-402
48. Brody, H., Griffith, J., Cuticchia, A. J., Arnold, J. and Timberlake, W. E. (1991) Chromosome-specific recombinant DNA libraries from the fungus Aspergillus nidulans. Nucleic Acids Res. 19, 3105-3109
49. Frohman, M. A., Dush, M. K. and Martin, G. R. (1988) Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc. Natl. Acad. Sci. U.S.A. 85, 8998-9002
50. Ballance, D. J. (1986) Sequences important for gene expression in filamentous fungi. Yeast 2, 229-236
51. Pao, S. S., Paulsen, I. T. and Saier, Jr, M. H. (1998) Major facilitator superfamily. Microbiol. Mol. Biol. Rev. 62, 1-34
52. Scazzocchio, C. (2000) The fungal GATA factors. Curr. Opin. Microbiol. 3, 126-131
53. An, Z., Mei, B., Yuan, W. M. and Leong, S. A. (1997) 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
54. Oberegger, H., Schoeser, M., Zadra, I., Schrettl, M., Parson, W. and Haas, H. (2002) Regulation of freA, acoA, lysF and cycA expression by iron availability in A. nidulans. Appl. Env. Microbiol. 68, 5769-5772
55. Remm, M., Storm, C. E. and Sonnhammer, E. L. (2001) Automatic clustering of orthologs and in-paralogs from pairwise species comparisons. J. Mol. Biol. 314, 1041-1052
56. Brakhage, A. A. and Turner, G. (1992) L-lysine repression of penicillin biosynthesis and the expression of penicillin biosynthesis genes acvA and ipnA in Aspergillus nidulans. FEMS Microbiol. Lett. 77, 123-127
57. Gietz, R. D. and Schiestl, R. H. (1991) Applications of high efficiency lithium acetate transformation of intact yeast cells using single-stranded nucleic acids as carrier. Yeast 7, 253-263
58. Winkelmann, G. (2001) Siderophore transport in Fungi. In Microbial Transport Systems (Winkelmann, G., ed.), pp. 463-479, Wiley-VCH, Weinheim