Haemin uptake and use as an iron source by Candida albicans: Role of CaHMX1-encoded haem oxygenase

Microbiology

Volumn 149, Issue 3, 2003, Pages 579-588

  Santos, Renata ^a   Buisson, Nicole ^a   Knight, Simon ^b   Dancis, Andrew ^b   Camadro, Jean Michel ^a   Lesuisse, Emmanuel ^a  

^a INSTITUT JACQUES MONOD   (France)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGAR; HEME OXYGENASE; HEMIN; IRON; SIDEROPHORE;

BINDING AFFINITY; CANDIDA ALBICANS; CELL CULTURE; CELL STRUCTURE; CELL TRANSPORT; COMPLEX FORMATION; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME ACTIVITY; FUNGAL CELL; FUNGUS GROWTH; GENE CONSTRUCT; GENE EXPRESSION; GENE MUTATION; GENETIC CODE; IRON DEFICIENCY; IRON TRANSPORT; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; REDUCTION; REGULATORY MECHANISM; REVIEW; SACCHAROMYCES CEREVISIAE; TEMPERATURE; TRANSPORT KINETICS;

CANDIDA ALBICANS; CULTURE MEDIA; GENE EXPRESSION REGULATION, FUNGAL; HEME OXYGENASE (DECYCLIZING); HEMIN; HUMANS; IRON; KINETICS; MUTATION; TRANSCRIPTION, GENETIC;

CANDIDA ALBICANS; FUNGI; SACCHAROMYCES CEREVISIAE;

EID: 0037352408     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.26108-0     Document Type: Review

References (49)

1. Ardon, O., Bussey, H., Philpott, C., Ward, D., Davis-Kaplan, S., Verroneau, S., Jiang, B. & Kaplan, J. (2001). Identification of a Candida albicans ferrichrome transporter and its characterization by expression in Saccharomyces cerevisiae. J Biol Chem 276, 43049-43055.
2. Braun, B. R. & Johnson, A. D. (1997). Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277, 105-109.
3. Brown, A. J. & Gow, N. A. (1999). Regulatory networks controlling Candida albicans morphogenesis. Trends Microbiol 7, 333-338.
4. Buchler, J. W. (1975). Static coordination chemistry of metalloporphyrins. In Porphyrins and Metalloporphyrins, pp. 157-224. Edited by K. M. Smith. Amsterdam: Elsevier.
5. Casanova, M., Cervera, A., Gozalbo, D. & Martinez, J. (1997). Hemin induces germ tube formation in Candida albicans. Infect Immun 65, 4360-4364.
6. Chu, G., Katakura, K., Zhang, X., Yoshida, T. & Ikeda-Saito, M. (1999). Heme degradation as catalyzed by a recombinant bacterial heme oxygenase (HmuO) from Corynebacterium diphtheriae. J Biol Chem 274, 21319-21325.
7. Dancis, A., Roman, D. G., Anderson, G. J., Hinnebusch, A. G. & 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. Eck, R., Hundt, S., Hartl, A., Roemer, E. & Kunkel, W. (1999). A multicopper oxidase gene from Candida albicans: cloning, characterization and disruption. Microbiology 145, 2415-2422.
9. Eide, D. J. (2000). Metal ion transport in eukaryotic microorganisms: insights from Saccharomyces cerevisiae. Adv Microb Physiol 43, 1-38.
10. Emery, T. (1987). Reductive mechanisms of iron assimilation. In Iron Transport in Microbes, Plants and Animals, pp. 235-250. Edited by G. Winkelmann, D. van der Helm & J. B. Neilands. Weinheim: VCH.
11. Foster, L. A. (2002). Utilization and cell-surface binding of hemin by Histoplasma capsulatum. Can J Microbiol 48, 437-442.
12. Galbraith, R., Sassa, S. & Kappas, A. (1985). Heme binding to murine erythroleukemia cells. Evidence for a heme receptor. J Biol Chem 260, 12198-12202.
13. Genco, C. & Dixon, D. (2001). Emerging strategies in microbial haem capture. Mol Microbiol 39, 1-11.
14. Hammacott, J. E., Williams, P. H. & Cashmore, A. M. (2000). Candida albicans CFL1 encodes a functional ferric reductase activity that can rescue a Saccharomyces cerevisiae fre1 mutant. Microbiology 146, 869-876.
15. Heymann, P., Ernst, J. F. & 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.
16. Heymann, P., Ernst, J. F. & Winkelmann, G. (2000). A gene of the major facilitator superfamily encodes a transporter for enterobactin (Enb1p) in Saccharomyces cerevisiae. Biometals 13, 65-72.
17. Heymann, P., Gerads, M., Schaller, M., Dromer, F., Winkelmann, G. & Ernst, J. (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.
18. Holzberg, M. & Artis, W. M. (1983). Hydroxamate siderophore production by opportunistic and systemic fungal pathogens. Infect Immun 40, 1134-1139.
19. Howard, D. H. (1999). Acquisition, transport, and storage of iron by pathogenic fungi. Clin Microbiol Rev 12, 394-404.
20. Hu, C., Bai, C., Zheng, X., Wang, Y. & Wang, Y. (2002). Characterization and functional analysis of the siderophore-iron transporter CaArn1p in Candida albicans. J Biol Chem 277, 30598-30605.
21. Ismail, A., Bedell, G. W. & Lupan, D. M. (1985). Siderophore production by the pathogenic yeast, Candida albicans. Biochem Biophys Res Commun 130, 885-891.
22. Knight, S. A., Lesuisse, E., Stearman, R., Klausner, R. D. & Dancis, A. (2002). Reductive iron uptake by Candida albicans: role of copper, iron and the TUP1 regulator. Microbiology 148, 29-40.
23. Kohrer, K. & Domdey, H. (1991). Preparation of high molecular weight RNA. Methods Enzymol 194, 398-405.
24. Laine, L. & Bonacini, M. (1994). Esophageal disease in human immunodeficiency virus infection. Arch Intern Med 154, 1577-1582.
25. Leng, P., Lee, P. R., Wu, H. & Brown, A. J. (2001). Efg1, a morphogenetic regulator in Candida albicans, is a sequence-specific DNA binding protein. J Bacteriol 183, 4090-4093.
26. Lesuisse, E., Raguzzi, F. & Crichton, R. R. (1987). Iron uptake by the yeast Saccharomyces cerevisiae: involvement of a reduction step. J Gen Microbiol 133, 3229-3236.
27. Lesuisse, E., Simon-Casteras, M. & 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.
28. Lesuisse, E., Knight, S. A., Camadro, J. M. & Dancis, A. (2002). Siderophore uptake by Candida albicans: effect of serum treatment and comparison with Saccharomyces cerevisiae. Yeast 19, 329-340.
29. Liu, H. (2001). Transcriptional control of dimorphism in Candida albicans. Curr Opin Microbiol 4, 728-735.
30. Manns, J. M., Mosser, D. M. & Buckley, H. R. (1994). Production of a hemolytic factor by Candida albicans. Infect Immun 62, 5154-5156.
31. Moors, M. A., Stull, T. L., Blank, K. J., Buckley, H. R. & Mosser, D. M. (1992). A role for complement receptor-like molecules in iron acquisition by Candida albicans. J Exp Med 175, 1643-1651.
32. Morrissey, J. A., Williams, P. H. & Cashmore, A. M. (1996). Candida albicans has a cell-associated ferric-reductase activity which is regulated in response to levels of iron and copper. Microbiology 142, 485-492.
33. Morse, D. & Choi, A. M. (2002). Heme oxygenase-1: 'the emerging molecule' has arrived. Am J Respir Cell Mol Biol 27, 8-16.
34. Payne, S. M. (1993). Iron acquisition in microbial pathogenesis. Trends Microbiol 1, 66-69.
35. Poss, K. & Tonegawa, S. (1997). Heme oxygenase 1 is required for mammalian iron reutilization. Proc Natl Acad Sci U S A 94, 10919-10924.
36. Ramanan, N. & Wang, Y. (2000). A high-affinity iron permease essential for Candida albicans virulence. Science 288, 1062-1064.
37. Ratledge, C. & Dover, L. G. (2000). Iron metabolism in pathogenic bacteria. Annu Rev Microbiol 54, 881-941.
38. Rex, J. H., Rinaldi, M. G. & Pfaller, M. A. (1995). Resistance of Candida species to fluconazole. Antimicrob Agents Chemother 39, 1-8.
39. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
40. Schuller, D. J., Wilks, A., Ortiz de Montellano, P. R. & Poulos, T. L. (1999). Crystal structure of human heme oxygenase-1. Nat Struct Biol 6, 860-867.
41. Schuller, D. J., Zhu, W., Stojiljkovic, I., Wilks, A. & Poulos, T. L. (2001). Crystal structure of heme oxygenase from the gram-negative pathogen Neisseria meningitidis and a comparison with mammalian heme oxygenase-1. Biochemistry 40, 11552-11558.
42. Stearman, R., Yuan, D. S., Yamaguchi-Iwai, Y., Klausner, R. D. & Dancis, A. (1996). A permease-oxidase complex involved in high-affinity iron uptake in yeast. Science 271, 1552-1557.
43. Stoldt, V. R., Sonneborn, A., Leuker, C. E. & Ernst, J. F. (1997). Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J 16, 1982-1991.
44. Sweet, S. P. & Douglas, L. J. (1991). Effect of iron concentration on siderophore synthesis and pigment production by Candida albicans. FEMS Microbiol Lett 64, 87-91.
45. Van Ho, A., Ward, D. M. & Kaplan, J. (2002). Transition metal transport in yeast. Annu Rev Microbiol 56, 237-261.
46. Weissman, Z., Shemer, R. & Kornitzer, D. (2002). Deletion of the copper transporter CaCCC2 reveals two distinct pathways for iron acquisition in Candida albicans. Mol Microbiol 44, 1551-1560.
47. Whiteway, M. (2000). Transcriptional control of cell type and morphogenesis in Candida albicans. Curr Opin Microbiol 3, 582-588.
48. Wilson, R., Davis, D. & Mitchell, A. (1999). Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J Bacteriol 181, 1868-1874.
49. Yun, C. W., Tiedeman, J. S., Moore, R. E. & Philpott, C. C. (2000). Siderophore-iron uptake in Saccharomyces cerevisiae. Identification of ferrichrome and fusarinine transporters. J Biol Chem 275, 16354-16359.