Trafficking of siderophore transporters in Saccharomyces cerevisiae and intracellular fate of ferrioxamine B conjugates

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Volumn 8, Issue 11, 2007, Pages 1601-1616

  Froissard, Marine ^a   Belgareh touzé, Naïma ^a   Dias, Marylène ^b   Buisson, Nicole ^a   Camadro, Jean Michel ^a   Haguenauer tsapis, Rosine ^a   Lesuisse, Emmanuel ^a  

^a INSTITUT JACQUES MONOD   (France)

^b Chimie Ingénierie Moléculaire et Matériaux d'Angers CIMMA   (France)

Author keywords

Iron; S. cerevisiae; Siderophore; Trafficking

Indexed keywords

CARRIER PROTEIN; ENTEROCHELIN; FERRIOXAMINE; GREEN FLUORESCENT PROTEIN; IRON; PROTOPORPHYRINOGEN OXIDASE; SIDEROPHORE; TRANSPORTER PROTEIN SIT1; UNCLASSIFIED DRUG;

ARTICLE; CELL COMPARTMENTALIZATION; CELL DISRUPTION; CELL FATE; CELL MEMBRANE; CONTROLLED STUDY; ENDOSOME; FLUORESCENCE; INTERNALIZATION; IRON TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN TARGETING; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SPECTROPHOTOMETRY; STEADY STATE; TARGET CELL;

BIOLOGICAL TRANSPORT; CANDIDA ALBICANS; CELL MEMBRANE; DEFEROXAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FERRIC COMPOUNDS; GENOTYPE; GREEN FLUORESCENT PROTEINS; INHIBITORY CONCENTRATION 50; IRON; KINETICS; MITOCHONDRIA; MODELS, CHEMICAL; PROTEIN TRANSPORT; PROTOPORPHYRINOGEN OXIDASE; SACCHAROMYCES CEREVISIAE; SIDEROPHORES; SUBSTRATE SPECIFICITY;

EID: 35348908969     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2007.00627.x     Document Type: Article

References (49)

1. Lesuisse E, Labbe P. Reductive and non-reductive mechanisms of iron assimilation by the yeast Saccharomyces cerevisiae. J Gen Microbiol 1989; 135: 257-263.
2. De Luca NG, Wood PM. Iron uptake by fungi: Contrasted mechanisms with internal or external reduction. Adv Microb Physiol 2000; 43: 39-74.
3. Yun CW, Ferea T, Rashford J, Ardon O, Brown PO, Botstein D, Kaplan J, Philpott CC. Desferrioxamine-mediated iron uptake in Saccharomyces cerevisiae. Evidence for two pathways of iron uptake. J Biol Chem 2000; 275: 10709-10715.
4. Kosman DJ. Molecular mechanisms of iron uptake in fungi. Mol Microbiol 2003; 47: 1185-1197.
5. Lesuisse E, Raguzzi F, Crichton RR. Iron uptake by the yeast Saccharomyces cerevisiae: Involvement of a reduction step. J Gen Microbiol 1987; 133: 3229-3236.
6. Dancis A, Klausner RD, Hinnebusch AG, Barriocanal JG. Genetic evidence that ferric reductase is required for iron uptake in Saccharomyces cerevisiae. Mol Cell Biol 1990; 10: 2294-2301.
7. Dancis A, Roman DG, Anderson GJ, Hinnebusch AG, Klausner RD. Ferric reductase of Saccharomyces cerevisiae: Molecular characterization, role in iron uptake, and transcriptional control by iron. Proc Natl Acad Sci USA 1992; 89: 3869-3873.
8. Georgatsou E, Alexandraki D. Two distinctly regulated genes are required for ferric reduction, the first step of iron uptake in Saccharomyces cerevisiae. Mol Cell Biol 1994; 14: 3065-3073.
9. Askwith C, Eide D, Van Ho A, Bernard PS, Li L, Davis-Kaplan S, Sipe DM, Kaplan J. The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 1994; 76: 403-410.
10. Stearman R, Yuan DS, Yamaguchi-Iwai Y, Klausner RD, Dancis A. A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 1996; 271: 1552-1557.
11. Haas H. Molecular genetics of fungal siderophore biosynthesis and uptake: The role of siderophores in iron uptake and storage. Appl Microbiol Biotechnol 2003; 62: 316-330.
12. 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. Microbiol 1998; 144: 3455-3462.
13. Heymann P, Ernst JF, Winkelmann G. Identification of a fungal triacetylfusarinine C siderophore transport gene (TAF1) in Saccharomyces cerevisiae as a member of the major facilitator superfamily. Biometals 1999; 12: 301-306.
14. Heymann P, Ernst JF, Winkelmann G. Identification and substrate specificity of a ferrichrome-type siderophore transporter (Arn1p) in Saccharomyces cerevisiae. FEMS Microbiol Lett 2000; 186: 221-227.
15. Yun CW, Tiedeman JS, Moore RE, Philpott CC. Siderophore-iron uptake in Saccharomyces cerevisiae. Identification of ferrichrome and fusarinine transporters. J Biol Chem 2000; 275: 16354-16359.
16. Heymann P, Ernst JF, Winkelmann G. A gene of the major facilitator superfamily encodes a transporter for enterobactin (Enb1p) in Saccharomyces cerevisiae. Biometals 2000; 13: 65-72.
17. Moore RE, Kim Y, Philpott CC. The mechanism of ferrichrome transport through Arn1p and its metabolism in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 2003; 100: 5664-5669.
18. Miller MJ, McKee JA, Minnick AA, Dolence EK. The design, synthesis and study of siderophore-antibiotic conjugates. Siderophore mediated drug transport. Biol Met 1991; 4: 62-69.
19. Kim Y, Yun CW, Philpott CC. Ferrichrome induces endosome to plasma membrane cycling of the ferrichrome transporter, Arn1p, in Saccharomyces cerevisiae. Embo J 2002; 21: 3632-3642.
20. Kim Y, Lampert SM, Philpott CC. A receptor domain controls the intracellular sorting of the ferrichrome transporter, ARN1. Embo J 2005; 24: 952-962.
21. Lesuisse E, Knight S, Camadro J, Dancis A. Siderophore uptake by Candida albicans: Effect of serum treatment and comparison with Saccharomyces cerevisiae. Yeast 2002; 19: 329-340.
22. 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 2001; 276: 43049-43055.
23. Hu C, Bai C, Zheng X, Wang Y, Wang Y. Characterization and functional analysis of the siderophore-iron transporter CaArn1p in Candida albicans. J Biol Chem 2002; 277: 30598-30605.
24. Haas H, Schoeser M, Lesuisse E, Ernst JF, Parson W, Abt B, Winkelmann G, Oberegger H. Characterization of the Aspergillus nidulans transporters for the siderophores enterobactin and triacetylfusarinine C. Biochem J 2003; 371: 505-513.
25. Pelletier B, Beaudoin J, Philpott CC, Labbe S. Fep1 represses expression of the fission yeast Schizosaccharomyces pombe siderophore-iron transport system. Nucleic Acids Res 2003; 31: 4332-4344.
26. Schrettl M, Winkelmann G, Haas H. Ferrichrome in Schizosaccharomyces pombe -an iron transport and iron storage compound. Biometals 2004; 17: 647-654.
27. Matringe M, Camadro JM, Labbe P, Scalla R. Protoporphyrinogen oxidase as a molecular target for diphenyl ether herbicides. Biochem J 1989; 260: 231-235.
28. Blondel MO, Morvan J, Dupre S, Urban-Grimal D, Haguenauer-Tsapis R, Volland C. Direct sorting of the yeast uracil permease to the endosomal system is controlled by uracil binding and Rsp5p-dependent ubiquitylation. Mol Biol Cell 2004; 15: 883-895.
29. Umebayashi K, Nakano A. Ergosterol is required for targeting of tryptophan permease to the yeast plasma membrane. J Cell Biol 2003; 161: 1117-1131.
30. Lesuisse E, Blaiseau PL, Dancis A, Camadro JM. Siderophore uptake and use by the yeast Saccharomyces cerevisiae. Microbiol 2001; 147: 289-298.
31. Lesuisse E, Knight SA, Courel M, Santos R, Camadro JM, Dancis A. Genome-wide screen for genes with effects on distinct iron uptake activities in Saccharomyces cerevisiae. Genetics 2005; 169: 107-122.
32. Bugnicourt A, Froissard M, Sereti K, Ulrich HD, Haguenauer-Tsapis R, Galan JM. Antagonistic roles of ESCRT and Vps class C/HOPS complexes in the recycling of yeast membrane proteins. Mol Biol Cell 2004; 15: 4203-4214.
33. Rubio-Texeira M, Kaiser CA. Amino acids regulate retrieval of the yeast general amino acid permease from the vacuolar targeting pathway. Mol Biol Cell 2006; 17: 3031-3050.
34. Nikko E, Marini AM, Andre B. Permease recycling and ubiquitination status reveal a particular role for Bro1 in the multivesicular body pathway. J Biol Chem 2003; 278: 50732-50743.
35. Black MW, Pelham HR. A selective transport route from Golgi to late endosomes that requires the yeast GGA proteins. J Cell Biol 2000; 151: 587-600.
36. Ouchetto H, Dias M, Mornet R, Lesuisse E, Camadro JM. A new route to trihydroxamate-containing artificial siderophores and synthesis of a new fluorescent probe. Bioorg Med Chem 2005; 13: 1799-1803.
37. Koch M, Breithaupt C, Kiefersauer R, Freigang J, Huber R, Messerschmidt A. Crystal structure of protoporphyrinogen IX oxidase: A key enzyme in haem and chlorophyll biosynthesis. Embo J 2004; 23: 1720-1728.
38. Kim Y, Deng Y, Philpott CC. GGA2- and Ubiquitin-dependent Trafficking of Arn1, the Ferrichrome Transporter of Saccharomyces cerevisiae. Mol Biol Cell 2007; 18: 1790-1802.
39. Bernier G, Girijavallabhan V, Murray A, Niyaz N, Ding P, Miller MJ, Malouin F. Desketoneoenactin-siderophore conjugates for Candida: evidence of iron transport-dependent species selectivity. Antimicrob Agents Chemother 2005; 49: 241-248.
40. Lytton SD, Cabantchik ZI, Libman J, Shanzer A. Reversed siderophores as antimalarial agents. II. Selective scavenging of Fe(III) from parasitized erythrocytes by a fluorescent derivative of desferal. Mol Pharmacol 1991; 40: 584-590.
41. Longtine MS, McKenzie A III, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 1998; 14: 953-961.
42. Mumberg D, Muller R, Funk M. Regulatable promoters of Saccharomyces cerevisiae: Comparison of transcriptional activity and their use for heterologous expression. Nucleic Acids Res 1994; 22: 5767-5768.
43. Kolling R, Hollenberg CP. The ABC-transporter Ste6 accumulates in the plasma membrane in a ubiquitinated form in endocytosis mutants. Embo J 1994; 13: 3261-3271.
44. Volland C, Urban-Grimal D, Geraud G, Haguenauer-Tsapis R. Endocytosis and degradation of the yeast uracil permease under adverse conditions. J Biol Chem 1994; 269: 9833-9841.
45. Raguzzi F, Lesuisse E, Crichton RR. Iron storage in Saccharomyces cerevisiae. FEBS Lett 1988; 231: 253-258.
46. Belgareh-Touze N, Avaro S, Rouille Y, Hoflack B, Haguenauer-Tsapis R. Yeast Vps55p, a functional homolog of human obesity receptor gene-related protein, is involved in late endosome to vacuole trafficking. Mol Biol Cell 2002; 13: 1694-1708.
47. Camadro JM, Thome F, Brouillet N, Labbe P. Purification and properties of protoporphyrinogen oxidase from the yeast Saccharomyces cerevisiae. Mitochondrial location and evidence for a precursor form of the protein. J Biol Chem 1994; 269: 32085-32091.
48. Dix D, Bridgham J, Broderius M, Eide D. Characterization of the FET4 protein of yeast. Evidence for a direct role in the transport of iron. J Biol Chem 1997; 272: 11770-11777.
49. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, O'Shea EK. Global analysis of protein localization in budding yeast. Nature 2003; 425: 686-691.