Host iron withholding demands siderophore utilization for Candida glabrata to survive macrophage killing

PLoS Pathogens

Volumn 7, Issue 3, 2011, Pages

  Nevitt, Tracy ^a   Thiele, Dennis J ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; FERRICHROME; HEME; IRON; PROTEIN SIT1; SIDEROPHORE; UNCLASSIFIED DRUG; FUNGAL PROTEIN; VIRULENCE FACTOR;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANDIDA ALBICANS; CANDIDA GLABRATA; CARBOXY TERMINAL SEQUENCE; CELL ACTIVATION; CELL MEMBRANE; CELL SURVIVAL; COPPER DEFICIENCY; ENZYME SPECIFICITY; FUNGAL VIRULENCE; HUMAN; HUMAN CELL; IRON DEFICIENCY; IRON OVERLOAD; IRON TRANSPORT; MACROPHAGE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOSOME; PROTEIN EXPRESSION; PROTEIN FUNCTION; SACCHAROMYCES CEREVISIAE; AMINO ACID SEQUENCE; CANDIDIASIS; GENETICS; METABOLISM; MOLECULAR GENETICS; PATHOGENICITY;

BACTERIA (MICROORGANISMS); CANDIDA GLABRATA;

AMINO ACID SEQUENCE; CANDIDA GLABRATA; CANDIDIASIS; CARRIER PROTEINS; FUNGAL PROTEINS; HUMANS; IRON; MOLECULAR SEQUENCE DATA; SIDEROPHORES; VIRULENCE FACTORS;

EID: 79953283725     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001322     Document Type: Article

References (53)

1. Moran C, Grussemeyer CA, Spalding JR, Benjamin DK Jr, Reed SD, (2010) Comparison of costs, length of stay, and mortality associated with Candida glabrata and Candida albicans bloodstream infections. Am J Infect Control 38: 78-80.
2. Tumbarello M, Sanguinetti M, Trecarichi EM, La Sorda M, Rossi M, et al. (2008) Fungaemia caused by Candida glabrata with reduced susceptibility to fluconazole due to altered gene expression: risk factors, antifungal treatment and outcome. J Antimicrob Chemother 62: 1379-1385.
3. Klevay MJ, Horn DL, Neofytos D, Pfaller MA, Diekema DJ, (2009) Initial treatment and outcome of Candida glabrata versus Candida albicans bloodstream infection. Diagn Microbiol Infect Dis 64: 152-157.
4. Fidel PL Jr, Vazquez JA, Sobel JD, (1999) Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin Microbiol Rev 12: 80-96.
5. Halliwell B, Gutteridge JM, (1985) The importance of free radicals and catalytic metal ions in human diseases. Mol Aspects Med 8: 89-193.
6. Hentze MW, Muckenthaler MU, Galy B, Camaschella C, (2010) Two to tango: regulation of Mammalian iron metabolism. Cell 142: 24-38.
7. Philpott CC, Protchenko O, (2008) Response to iron deprivation in Saccharomyces cerevisiae. Eukaryot Cell 7: 20-27.
8. Boukhalfa H, Crumbliss AL, (2002) Chemical aspects of siderophore mediated iron transport. Biometals 15: 325-339.
9. Raymond KN, Dertz EA, Kim SS, (2003) Enterobactin: an archetype for microbial iron transport. Proc Natl Acad Sci U S A 100: 3584-3588.
10. Haas H, Eisendle M, Turgeon BG, (2008) Siderophores in fungal physiology and virulence. Annu Rev Phytopathol 46: 149-187.
11. Heymann P, Gerads M, Schaller M, Dromer F, Winkelmann G, et al. (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.
12. Weissman Z, Shemer R, Conibear E, Kornitzer D, (2008) An endocytic mechanism for haemoglobin-iron acquisition in Candida albicans. Mol Microbiol 69: 201-217.
13. Andrews NC, (2008) Forging a field: the golden age of iron biology. Blood 112: 219-230.
14. Cellier MF, Courville P, Campion C, (2007) Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect 9: 1662-1670.
15. Khan FA, Fisher MA, Khakoo RA, (2007) Association of hemochromatosis with infectious diseases: expanding spectrum. Int J Infect Dis 11: 482-487.
16. Wrighting DM, Andrews NC, (2008) Iron homeostasis and erythropoiesis. Curr Top Dev Biol 82: 141-167.
17. De Domenico I, McVey Ward D, Kaplan J, (2008) Regulation of iron acquisition and storage: consequences for iron-linked disorders. Nat Rev Mol Cell Biol 9: 72-81.
18. Barton JC, Acton RT, (2009) Hemochromatosis and Vibrio vulnificus wound infections. J Clin Gastroenterol 43: 890-893.
19. Cunningham-Rundles S, Giardina PJ, Grady RW, Califano C, McKenzie P, et al. (2000) Effect of transfusional iron overload on immune response. J Infect Dis 182 (Suppl 1): S115-121.
20. Singh N, Sun HY, (2008) Iron overload and unique susceptibility of liver transplant recipients to disseminated disease due to opportunistic pathogens. Liver Transpl 14: 1249-1255.
21. Kontoyiannis DP, Chamilos G, Lewis RE, Giralt S, Cortes J, et al. (2007) Increased bone marrow iron stores is an independent risk factor for invasive aspergillosis in patients with high-risk hematologic malignancies and recipients of allogeneic hematopoietic stem cell transplantation. Cancer 110: 1303-1306.
22. Manns JM, Mosser DM, Buckley HR, (1994) Production of a hemolytic factor by Candida albicans. Infect Immun 62: 5154-5156.
23. Santos R, Buisson N, Knight S, Dancis A, Camadro JM, et al. (2003) Haemin uptake and use as an iron source by Candida albicans: role of CaHMX1-encoded haem oxygenase. Microbiology 149: 579-588.
24. Sherman DJ, Martin T, Nikolski M, Cayla C, Souciet JL, et al. (2009) Genolevures: protein families and synteny among complete hemiascomycetous yeast proteomes and genomes. Nucleic Acids Res 37: D550-554.
25. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
26. 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.
27. Yun CW, Tiedeman JS, Moore RE, Philpott CC, (2000) Siderophore-iron uptake in Saccharomyces cerevisiae. Identification of ferrichrome and fusarinine transporters. J Biol Chem 275: 16354-16359.
28. Kim Y, Yun CW, Philpott CC, (2002) Ferrichrome induces endosome to plasma membrane cycling of the ferrichrome transporter, Arn1p, in Saccharomyces cerevisiae. EMBO J 21: 3632-3642.
29. Kim Y, Lampert SM, Philpott CC, (2005) A receptor domain controls the intracellular sorting of the ferrichrome transporter, ARN1. EMBO J 24: 952-962.
30. Blackburn NJ, Ralle M, Hassett R, Kosman DJ, (2000) Spectroscopic analysis of the trinuclear cluster in the Fet3 protein from yeast, a multinuclear copper oxidase. Biochemistry 39: 2316-2324.
31. Mestas J, Hughes CC, (2004) Of mice and not men: differences between mouse and human immunology. J Immunol 172: 2731-2738.
32. Huang ZL, Failla ML, (2000) Copper deficiency suppresses effector activities of differentiated U937 cells. J Nutr 130: 1536-1542.
33. Huang ZL, Failla ML, Reeves PG, (2001) Differentiation of human U937 promonocytic cells is impaired by moderate copper deficiency. Exp Biol Med (Maywood) 226: 222-228.
34. Fernandes A, Preza GC, Phung Y, De Domenico I, Kaplan J, et al. (2009) The molecular basis of hepcidin-resistant hereditary hemochromatosis. Blood 114: 437-443.
35. Girelli D, De Domenico I, Bozzini C, Campostrini N, Busti F, et al. (2008) Clinical, pathological, and molecular correlates in ferroportin disease: a study of two novel mutations. J Hepatol 49: 664-671.
36. Zohn IE, De Domenico I, Pollock A, Ward DM, Goodman JF, et al. (2007) The flatiron mutation in mouse ferroportin acts as a dominant negative to cause ferroportin disease. Blood 109: 4174-4180.
37. De Domenico I, Ward DM, Musci G, Kaplan J, (2007) Evidence for the multimeric structure of ferroportin. Blood 109: 2205-2209.
38. Iglesias-Osma C, Gonzalez-Villaron L, San Miguel JF, Caballero MD, Vazquez L, et al. (1995) Iron metabolism and fungal infections in patients with haematological malignancies. J Clin Pathol 48: 223-225.
39. Karp JE, Merz WG, (1986) Association of reduced total iron binding capacity and fungal infections in leukemic granulocytopenic patients. J Clin Oncol 4: 216-220.
40. Drakesmith H, Prentice A, (2008) Viral infection and iron metabolism. Nat Rev Microbiol 6: 541-552.
41. Porto G, De Sousa M, (2007) Iron overload and immunity. World J Gastroenterol 13: 4707-4715.
42. White C, Lee J, Kambe T, Fritsche K, Petris MJ, (2009) A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J Biol Chem 284: 33949-33956.
43. Lesuisse E, Knight SA, Camadro JM, Dancis A, (2002) Siderophore uptake by Candida albicans: effect of serum treatment and comparison with Saccharomyces cerevisiae. Yeast 19: 329-340.
44. Paradkar PN, De Domenico I, Durchfort N, Zohn I, Kaplan J, et al. (2008) Iron depletion limits intracellular bacterial growth in macrophages. Blood 112: 866-874.
45. Bullen JJ, Spalding PB, Ward CG, Gutteridge JM, (1991) Hemochromatosis, iron and septicemia caused by Vibrio vulnificus. Arch Intern Med 151: 1606-1609.
46. Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 6: e1000713.
47. 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: 1195-1207.
48. 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.
49. Waterman SR, Hacham M, Hu G, Zhu X, Park YD, et al. (2007) Role of a CUF1/CTR4 copper regulatory axis in the virulence of Cryptococcus neoformans. J Clin Invest 117: 794-802.
50. Deng Y, Guo Y, Watson H, Au WC, Shakoury-Elizeh M, et al. (2009) Gga2 mediates sequential ubiquitin-independent and ubiquitin-dependent steps in the trafficking of ARN1 from the trans-Golgi network to the vacuole. J Biol Chem 284: 23830-23841.
51. Hu CJ, Bai C, Zheng XD, Wang YM, Wang Y, (2002) Characterization and functional analysis of the siderophore-iron transporter CaArn1p in Candida albicans. J Biol Chem 277: 30598-30605.
52. Edlind TD, Henry KW, Vermitsky JP, Edlind MP, Raj S, et al. (2005) Promoter-dependent disruption of genes: simple, rapid, and specific PCR-based method with application to three different yeast. Curr Genet 48: 117-125.
53. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K, eds. (1995) Current protocols in molecular biology. New York Greene Publishing Associates and Wiley-Interscience.