Histoplasma requires SID1, a member of an iron-regulated siderophore gene cluster, for host colonization

PLoS Pathogens

Volumn 4, Issue 4, 2008, Pages

  Hwang, Lena H ^a   Mayfield, Jacob A ^b   Rine, Jasper ^b   Sil, Anita ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL ENZYME; IRON; ORNITHINE MONOOXYGENASE; SIDEROPHORE; FERRIC CITRATE IRON REDUCTASE; FERRIC ION; FLAVINE MONONUCLEOTIDE REDUCTASE; FUNGAL PROTEIN; PROTEIN KINASE; SID1 KINASE;

ARTICLE; FUNGAL COLONIZATION; FUNGAL GENE; FUNGAL STRAIN; FUNGAL VIRULENCE; GENE CLUSTER; GENE CONTROL; GENE DISRUPTION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE SEQUENCE; GENETIC TRANSCRIPTION; HISTOPLASMA CAPSULATUM; HOST; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PROMOTER REGION; PROTEIN SECRETION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; SID1 GENE; ANIMAL; C57BL MOUSE; CELL CULTURE; DISEASE MODEL; DNA MICROARRAY; DRUG EFFECT; ENZYMOLOGY; FEMALE; GENETIC TRANSFORMATION; GENETICS; GENOME; HISTOPLASMA; HOST PATHOGEN INTERACTION; MACROPHAGE; METABOLISM; MICROBIOLOGY; MOUSE; PATHOGENICITY;

AJELLOMYCES; AJELLOMYCES CAPSULATUS; FUNGI; MAMMALIA; MURINAE;

ANIMALS; CELLS, CULTURED; DISEASE MODELS, ANIMAL; FEMALE; FERRIC COMPOUNDS; FMN REDUCTASE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENES, FUNGAL; GENOME; HISTOPLASMA; HOST-PATHOGEN INTERACTIONS; IRON; MACROPHAGES; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN KINASES; SIDEROPHORES; TRANSFORMATION, GENETIC;

EID: 43049121756     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000044     Document Type: Article

References (40)

1. Schaible UE, Kaufmann SH (2004) Iron and microbial infection. Nat Rev Microbiol 2: 946-953.
2. Woods JP (2003) Knocking on the right door and making a comfortable home: Histoplasma capsulatum intracellular pathogenesis. Curr Opin Microbiol 6: 327-331.
3. Lane TE, Wu-Hsieh BA, Howard DH (1991) Iron limitation and the gamma interferon-mediated antihistoplasma state of murine macrophages. Infect Immun 59: 2274-2278.
4. Newman SL, Gootee L, Brunner G, Deepe GS Jr (1994) Chloroquine induces human macrophage killing of Histoplasma capsulatum by limiting the availability of intracellular iron and is therapeutic in a murine model of histoplasmosis. J Clin Invest 93: 1422-1429.
5. Cain JA, Deepe GS Jr (1998) Evolution of the primary immune response to Histoplasma capsulatum in murine lung. Infect Immun 66: 1473-1481.
6. Howard DH, Rafie R, Tiwari A, Faull KF (2000) Hydroxamate siderophores of Histoplasma capsulatum. Infect Immun 68: 2338-2343.
7. Burt WR, Underwood AL, Appleton GL (1981) Hydroxamic acid from Histoplasma capsulatum that displays growth factor activity. Appl Environ Microbiol 42: 560-563.
8. Timmerman MM, Woods JP (1999) Ferric reduction is a potential iron acquisition mechanism for Histoplasma capsulatum. Infect Immun 67: 6403-6408.
9. Nittler MP, Hocking-Murray D, Foo CK, Sil A (2005) Identification of Histoplasma capsulatum transcripts induced in response to reactive nitrogen species. Mol Biol Cell 16: 4792-4813.
10. Hwang L, Hocking-Murray D, Bahrami AK, Andersson M, Rine J, et al. (2003) Identifying phase-specific genes in the fungal pathogen Histoplasma capsulatum using a genomic shotgun microarray. Mol Biol Cell 14: 2314-2326.
11. Haas H (2003) Molecular genetics of fungal siderophore biosynthesis and uptake: the role of siderophores in iron uptake and storage. Appl Microbiol Biotechnol 62: 316-330.
12. Neilands JB (1995) Siderophores: structure and function of microbial iron transport compounds. J Biol Chem 270: 26723-26726.
13. Schrettl M, Bignell E, Kragl C, Sabiha Y, Loss O, et al. (2007) Distinct Roles for Intra- and Extracellular Siderophores during Aspergillus fumigatus Infection. PLoS Pathog 3: e128.
14. Oide S, Moeder W, Krasnoff S, Gibson D, Haas H, et al. (2006) NPS6, encoding a nonribosomal peptide synthetase involved in siderophore-mediated iron metabolism, is a conserved virulence determinant of plant pathogenic ascomycetes. Plant Cell 18: 2836-2853.
15. Haas H, Schoeser M, Lesuisse E, Ernst JF, Parson W, et al. (2003) Characterization of the Aspergillus nidulans transporters for the siderophores enterobactin and triacetylfusarinine C. Biochem J 371: 505-513.
16. Mitsuhashi N, Miki T, Senbongi H, Yokoi N, Yano H, et al. (2000) MTABC3, a novel mitochondrial ATP-binding cassette protein involved in iron homeostasis. J Biol Chem 275: 17536-17540.
17. Scazzocchio C (2000) The fungal GATA factors. Curr Opin Microbiol 3: 126-131.
18. Voisard C, Wang J, McEvoy JL, Xu P, Leong SA (1993) 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.
19. Haas H, Zadra I, Stoffler G, 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.
20. Zhou LW, Haas H, Marzluf GA (1998) Isolation and characterization of a new gene, sre, which encodes a GATA-type regulatory protein that controls iron transport in Neurospora crassa. Mol Gen Genet 259: 532-540.
21. Freter R, O'Brien PC, Macsai MS (1981) Role of chemotaxis in the association of motile bacteria with intestinal mucosa: in vivo studies. Infect Immun 34: 234-240.
22. Taylor RK, Miller VL, Furlong DB, Mekalanos JJ (1986) Identification of a pilus colonization factor that is coordinately regulated with cholera toxin. Ann Sclavo Collana Monogr 3: 51-61.
23. Howard DH (2004) Iron gathering by zoopathogenic fungi. FEMS Immunol Med Microbiol 40: 95-100.
24. Lin JS, Wu-Hsieh BA (2004) Functional T cells in primary immune response to histoplasmosis. Int Immunol 16: 1663-1673.
25. Schrettl M, Bignell E, Kragl C, Joechl C, Rogers T, et al. (2004) Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J Exp Med 200: 1213-1219.
26. Mei B, Budde AD, Leong SA (1993) sid1, a gene initiating siderophore biosynthesis in Ustilago maydis: molecular characterization, regulation by iron, and role in phytopathogenicity. Proc Natl Acad Sci U S A 90: 903-907.
27. Eichhorn H, Lessing F, Winterberg B, Schirawski J, Kamper J, et al. (2006) A ferroxidation/permeation iron uptake system is required for virulence in Ustilago maydis. Plant Cell 18: 3332-3345.
28. Ramanan N, Wang Y (2000) A high-affinity iron permease essential for Candida albicans virulence. Science 288: 1062-1064.
29. An Z, Mei B, Yuan WM, Leong SA (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.
30. Yuan WM, Gentil GD, Budde AD, Leong SA (2001) Characterization of the Ustilago maydis sid2 gene, encoding a multidomain peptide synthetase in the ferrichrome biosynthetic gene cluster. J Bacteriol 183: 4040-4051.
31. Kragl C, Schrettl M, Abt B, Sarg B, Lindner HH, et al. (2007) EstB-mediated hydrolysis of the siderophore triacetylfusarinine C optimizes iron uptake of Aspergillus fumigatus. Eukaryot Cell 6: 1278-1285.
32. Bok JW, Keller NP (2004) LaeA, a regulator of secondary metabolism in Aspergillus spp. Eukaryot Cell 3: 527-535.
33. Bok JW, Noordermeer D, Kale SP, Keller NP (2006) Secondary metabolic gene cluster silencing in Aspergillus nidulans. Mol Microbiol 61: 1636-1645.
34. Worsham PL, Goldman WE (1988) Quantitative plating of Histoplasma capsulatum without addition of conditioned medium or siderophores. J Med Vet Mycol 26: 137-143.
35. Woods JP, Heinecke EL, Goldman WE (1998) Electrotransformation and expression of bacterial genes encoding hygromycin phosphotransferase and beta-galactosidase in the pathogenic fungus Histoplasma capsulatum. Infect Immun 66: 1697-1707.
36. Sullivan TD, Rooney PJ, Klein BS (2002) Agrobacterium tumefaciens integrates transfer DNA into single chromosomal sites of dimorphic fungi and yields homokaryotic progeny from multinucleate yeast. Eukaryot Cell 1: 895-905.
37. Gebhart D, Bahrami AK, Sil A (2006) Identification of a copper-inducible promoter for use in ectopic expression in the fungal pathogen Histoplasma capsulatum. Eukaryot Cell 5: 935-944.
38. Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95: 14863-14868.
39. Sebghati TS, Engle JT, Goldman WE (2000) Intracellular parasitism by Histoplasma capsulatum: fungal virulence and calcium dependence. Science 290: 1368-1372.
40. Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160: 47-56.