Candida albicans iron acquisition within the host

Almeida, Ricardo S.; Wilson, Duncan; Hube, Bernhard

doi:10.1111/j.1567-1364.2009.00570.x

Cited by 199Antifungal resistance and susceptibilityFungal and yeast genetics researchFungal Infections and Studies

Candida albicans iron acquisition within the host

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Almeida, Ricardo S., Wilson, Duncan, Hube, Bernhard·2009·FEMS Yeast Research

DOI 10.1111/j.1567-1364.2009.00570.x

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Abstract

As a commensal and opportunistic pathogen, Candida albicans possesses a range of determinants that contribute to survival, persistence and virulence. Among this repertoire of fitness and virulence attributes are iron acquisition factors and pathways, which allow fungal cells to gain this essential mineral in the iron-poor environment of the host. The aim of this review is to present the strategies used by C. albicans to exploit host iron reservoirs and their impact on C. albicans pathogenicity. Because iron in the human host is mostly linked to host proteins, pathogens such as C. albicans must possess mechanisms to gain iron from these proteins. Here, we introduce the most important groups of human proteins, including haemoglobin, transferrin, lactoferrin and ferritin, which contain iron and that are potential iron sources for invading microorganisms. We then summarize and discuss the known and proposed strategies by which C. albicans exploits or may exploit iron from host proteins and compare these with strategies from other pathogenic microorganisms.

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The expression of the ferritin receptor, Als3, increases in the hyphae-associated program, and inhibition of the hyphal form leads to its diminished expression and reduced capability of ferritin-binding.
“For example, the expression of the ferritin receptor, Als3, increases in the hyphae-associated program, and inhibition of the hyphal form leads to its diminished expression and reduced capability of ferritin-binding (Almeida et al., 2009).”
From Iron at the Centre of Candida albicans Interactions (2018) · cites this paper as Almeida et al., 2009
The “Ferritin as a potential iron source” section identifies Als3 as hyphal-associated and reports that a mutant unable to form hyphae did not express ALS3 and had reduced ferritin binding. But it also says ferritin binding does not depend on hyphal morphology itself: another mutant lacked true hyphae yet still expressed ALS3 and bound ferritin. The claim overgeneralizes the effect of inhibiting hyphal formation. (LLM, conf=0.87)
Experimental — accuracy not yet measured
Due to the spontaneous generation of toxic free radicals by ferrous iron, a multicopper oxidase enzyme is involved in the reconversion of the produced ferrous iron to a ferric state; a reaction known as ferroxidation.
“Due to the spontaneous generation of toxic free radicals by ferrous iron, a multicopper oxidase enzyme is involved in the reconversion of the produced ferrous iron to a ferric state; a reaction known as ferroxidation (reviewed by Kosman, 2003; Almeida et al., 2009).”
From Iron at the Centre of Candida albicans Interactions (2018) · cites this paper as Almeida et al., 2009
A functional ferric reductase has a ferric reductase domain and a FAD and/or NAD binding domain.
“A functional ferric reductase has a ferric reductase domain and a FAD and/or NAD binding domain.”
From Iron at the Centre of Candida albicans Interactions (2018) · cites this paper as Almeida et al., 2009
These domains were absent in two of the reported reductases while another reductase was lacking a FAD and NAD binding domain.
“These domains were absent in two of the reported reductases while another reductase was lacking a FAD and NAD binding domain (reviewed by Almeida et al., 2009).”
From Iron at the Centre of Candida albicans Interactions (2018) · cites this paper as Almeida et al., 2009
Within the C. albicans genome, there are as much as 17 ferric reductase-related genes but not all these genes are likely to be a ferric reductase.
“Within the C. albicans genome, there are as much as 17 ferric reductase-related genes but not all these genes are likely to be a ferric reductase.”
From Iron at the Centre of Candida albicans Interactions (2018) · cites this paper as Almeida et al., 2009

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Ueta, E., Tanida, T., & Osaki, T. (2001) · Journal of Peptide Research · doi:10.1111/j.1399-3011.2001.00821.x · Cited by 83 · see citing works
A role for complement receptor-like molecules in iron acquisition by Candida albicans
Moors, M. A., Stull, T. L., Blank, K. J., Buckley, H. R., & Mosser, D. M. (1992) · The Journal of experimental medicine · doi:10.1084/jem.175.6.1643 · Cited by 80 · see citing works
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
An, Z., Mei, B., Yuan, W. M., & Leong, S. A. (1997) · The EMBO Journal · doi:10.1093/emboj/16.7.1742 · Cited by 79 · see citing works
Candida albicans CFL1 encodes a functional ferric reductase activity that can rescue a Saccharomyces cerevisiae fre1 mutant The EMBL accession number for the sequence reported in this paper is AJ387722.
Hammacott, J. E., Williams, P. H., & Cashmore, A. M. (2000) · Microbiology · doi:10.1099/00221287-146-4-869 · Cited by 69 · see citing works
Identification of a Candida albicans Ferrichrome Transporter and Its Characterization by Expression inSaccharomyces cerevisiae
Ardon, O., Bussey, H., Philpott, C., Ward, D. M., Davis-Kaplan, S., Verroneau, S., Jiang, B., & Kaplan, J. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m108701200 · Cited by 68 · see citing works
Siderophore production by the pathogenic yeast, Candida albicans
Ismail, A., Bedell, G. W., & Lupan, D. M. (1985) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(85)90499-1 · Cited by 63 · see citing works
Iron(III) complexation of Desferrioxamine B encapsulated in apoferritin
Dominguez-Vera, J. M. (2004) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2003.12.015 · Cited by 61 · see citing works
Human recombinant lactoferrin acts synergistically with antimicrobials commonly used in neonatal practice against coagulase-negative staphylococci and Candida albicans causing neonatal sepsis
Pammi, M., & Rong, L. (2008) · Journal of Medical Microbiology · doi:10.1099/jmm.0.2008/001263-0 · Cited by 59 · see citing works
Oxygen accessibility and iron levels are critical factors for the antifungal action of ciclopirox against Candida albicans
Sigle, H.-C., Thewes, S., Niewerth, M., Körting, H. C., Schäfer‐Korting, M., & Hube, B. (2005) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dki089 · Cited by 58 · see citing works
Self-citation
Genome-wide expression profiling of the response to ciclopirox olamine in Candida albicans
Lee, R. B., Liu, T. T., Barker, K. S., Lee, R. E., & Rogers, P. D. (2005) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dki105 · Cited by 57 · see citing works
Iron uptake by fungi: Contrasted mechanisms with internal or external reduction
Luca, N. G. D., & Wood, P. M. (2000) · Advances in microbial physiology/Advances in Microbial Physiology · doi:10.1016/s0065-2911(00)43002-x · Cited by 56 · see citing works
Siderophore uptake by Candida albicans: effect of serum treatment and comparison with Saccharomyces cerevisiae
Lesuisse, E., Knight, S. A. B., Camadro, J., & Dancis, A. (2002) · Yeast · doi:10.1002/yea.840 · Cited by 56 · see citing works
Sensing the host environment: recognition of hemoglobin by the pathogenic yeast Candida albicans
Pendrak, M. L., Yan, S. S., & Roberts, D. D. (2004) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2004.02.006 · Cited by 55 · see citing works
Characterization of iron-binding motifs in Candida albicans high-affinity iron permease CaFtr1p by site-directed mutagenesis
Fang, H., & Wang, Y. (2002) · Biochemical Journal · doi:10.1042/bj20021005 · Cited by 54 · see citing works
Iron and ferritin in inflammation and cancer.
Torti, S. V., & Torti, F. M. (1994) · PubMed · Cited by 53 · see citing works
Receptor-induced switch in site-site cooperativity during iron release by transferrin
Bali, P. K., & Aisen, P. (1992) · Biochemistry · doi:10.1021/bi00131a011 · Cited by 53 · cited 1× · see citing works
“The proposed mechanism by which transferrin releases iron to other host cells is via binding to the transferrin receptor coupled with acidification to pH 5.6 (Bali & Aisen, 1992).”
BackgroundInfluential
Burkholderia cenocepacia utilizes ferritin as an iron source
Whitby, P. W., VanWagoner, T. M., Springer, J. M., Morton, D. J., Seale, T. W., & Stull, T. L. (2006) · Journal of Medical Microbiology · doi:10.1099/jmm.0.46199-0 · Cited by 53 · see citing works
Antibacterial Effects of Lactoferricin B
Vorland, L. H. (1999) · Scandinavian Journal of Infectious Diseases · doi:10.1080/003655499750006245 · Cited by 53 · see citing works
Lactoferrin Peptide Increases the Survival of Candida albicans - Inoculated Mice by Upregulating Neutrophil and Macrophage Functions, Especially in Combination with Amphotericin B and Granulocyte-Macrophage Colony-Stimulating Factor
Tanida, T., Rao, F., Hamada, T., Ueta, E., & Osaki, T. (2001) · Infection and Immunity · doi:10.1128/iai.69.6.3883-3890.2001 · Cited by 50 · see citing works
Outer membrane peptides ofYersinia pestis mediating siderophore-independent assimilation of iron
Sikkema, D. J., & Brubaker, R. R. (1989) · BioMetals · doi:10.1007/bf01142557 · Cited by 49 · see citing works
Isolation of the mRNA-capping enzyme and ferric-reductase-related genes from Candida albicans
Yamada-Okabe, T., Shimmi, O., Doi, R., Mizumoto, K., Arisawa, M., & Yamada-Okabe, H. (1996) · Microbiology · doi:10.1099/00221287-142-9-2515 · Cited by 46 · see citing works
Iron overload exacerbates experimental meningoencephalitis by Cryptococcus neoformans
Barluzzi, R., Saleppico, S., Nocentini, A., Boelaert, J. R., Neglia, R. G., Bistoni, F., & Blasi, E. (2002) · Journal of Neuroimmunology · doi:10.1016/s0165-5728(02)00324-7 · Cited by 43 · see citing works
Desketoneoenactin-Siderophore Conjugates for Candida : Evidence of Iron Transport-Dependent Species Selectivity
Bernier, G., Girijavallabhan, V. M., Murray, A. P., Niyaz, N. M., Ding, P., Miller, M. J., & Malouin, F. (2004) · Antimicrobial Agents and Chemotherapy · doi:10.1128/aac.49.1.241-248.2005 · Cited by 42 · see citing works
Hemoglobin Is Utilized byCandida albicansin the Hyphal Form but Not Yeast Form
Tanaka, W. T. H., Nakao, N., Mikami, T., & Matsumoto, T. (1997) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1997.6247 · Cited by 40 · see citing works
Endothelial Cell Injury Caused by Candida albicans Is Dependent on Iron
Fratti, R. A., Belanger, P. H., Ghannoum, M. A., Edwards, J. E., & Filler, S. G. (1998) · Infection and Immunity · doi:10.1128/iai.66.1.191-196.1998 · Cited by 39 · see citing works
Hemoglobin Induces Binding of Several Extracellular Matrix Proteins to Candida albicans
Yan, S. S., Rodrigues, R. G., Cahn-Hidalgo, D., Walsh, T. J., & Roberts, D. D. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.10.5638 · Cited by 39 · see citing works
Trafficking of Siderophore Transporters in Saccharomyces cerevisiae and Intracellular Fate of Ferrioxamine B Conjugates
Froissard, M., Belgareh‐Touzé, N., Dias, M., Buisson, N., Camadro, J., Haguenauer‐Tsapis, R., & Lesuisse, E. (2007) · Traffic · doi:10.1111/j.1600-0854.2007.00627.x · Cited by 38 · see citing works
Reduction of 2,3-bis(2-methoxy-4-nitro-5-sulfophenyl)-2H-tetrazolium-5-carboxanilide inner salt (XTT) is dependent on CaFRE10 ferric reductase for Candida albicans grown in unbuffered media
Knight, S. A. B., & Dancis, A. (2006) · Microbiology · doi:10.1099/mic.0.28843-0 · Cited by 37 · see citing works
Use of Green Fluorescent Protein and Reverse Transcription-PCR To Monitor Candida albicans Agglutinin-Like Sequence Gene Expression in a Murine Model of Disseminated Candidiasis
Green, C. B., Zhao, X., & Hoyer, L. L. (2005) · Infection and Immunity · doi:10.1128/iai.73.3.1852-1855.2005 · Cited by 36 · see citing works
Modification of ferritin during iron loading
Welch, K. D., Eden, M. E. V., & Aust, S. D. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(01)00676-1 · Cited by 30 · see citing works
Infection-Associated Genes of Candida Albicans
Hube, B. (2006) · Future Microbiology · doi:10.2217/17460913.1.2.209 · Cited by 29 · see citing works
Self-citation
Experimental candidiasis in iron overload
Abe, F., Tateyma, M., Shibuya, H., Azumi, N., & Ommura, Y. (1985) · Mycopathologia · doi:10.1007/bf00437134 · Cited by 27 · see citing works
Fungistatic activity of iron-free bovin lactoferrin against several fungal plant pathogens and antagonists
Lahoz, E., Pisacane, A., Iannaccone, M., Palumbo, D., & Capparelli, R. (2008) · Natural Product Research · doi:10.1080/14786410701650253 · Cited by 24 · see citing works
The N‐terminal sequence of human lactotransferrin: Its close homology with the amino‐terminal regions of other transferrins
Jollès, J., Mazurier, J., Metz‐Boutigue, M., Spik, G., Montreuil, J., & Jollès, P. (1976) · FEBS Letters · doi:10.1016/0014-5793(76)80646-1 · Cited by 23 · see citing works
Candida albicansferric reductaseFRP1is regulated by direct interaction with Rim101p transcription factor
Liang, Y., Gui, L., Wei, D., Zheng, W. L., Xing, L.-J., & Li, M. (2008) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2008.00468.x · Cited by 21 · see citing works
The location of exon boundaries in the multimeric iron-storage protein ferritin
Harrison, P. M., Ford, G. C., Smith, J. M., & White, J. L. (1991) · BioMetals · doi:10.1007/bf01135385 · Cited by 16 · see citing works
Utilization of ferroproteins byCandida albicans during candidastasis by apotransferrin
Han, Y. (2005) · Archives of Pharmacal Research · doi:10.1007/bf02973884 · Cited by 14 · see citing works
Candida albicans can utilize siderophore during candidastasis caused by apotransferrin
Lee, J.-H., & Han, Y. (2006) · Archives of Pharmacal Research · doi:10.1007/bf02969401 · Cited by 11 · see citing works
Hemochromatosis. Common genes, uncommon illness?
Harrison, H., & Adams, P. C. (2002) · PubMed · Cited by 5 · see citing works
Plasma Transferrin Receptor Helps to Predict Iron Deficiency in the Anemia of Chronic Disease
Fleming, D. J., & Wood, R. J. (2009) · Nutrition Reviews · doi:10.1111/j.1753-4887.1995.tb01544.x · Cited by 2 · see citing works

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Candida albicans pathogenicity mechanisms
Mayer, F. L., Wilson, D., & Hube, B. (2013) · Virulence · doi:10.4161/viru.22913 · Cited by 1,848 · see citing works
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Candida albicans Als3, a multifunctional adhesin and invasin
Liu, Y., & Filler, S. G. (2011) · Eukaryotic Cell · doi:10.1128/ec.00279-10 · Cited by 354 · see citing works
Shared and distinct mechanisms of iron acquisition by bacterial and fungal pathogens of humans
Caza, M., & Kronstad, J. W. (2013) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2013.00080 · Cited by 306 · see citing works
Stress adaptation in a pathogenic fungus
Brown, A. J. P., Budge, S., Kaloriti, D., Tillmann, A., Jacobsen, M. D., Yin, Z., Ene, I. V., Bohovych, I., Sandai, D., Kastora, S., et al. (2014) · Journal of Experimental Biology · doi:10.1242/jeb.088930 · Cited by 299 · see citing works
Fungi that Infect Humans
Köhler, J. R., Hube, B., Puccia, R., Casadevall, A., & Perfect, J. R. (2017) · Microbiology Spectrum · doi:10.1128/microbiolspec.funk-0014-2016 · Cited by 301 · see citing works
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Fungal Biofilms, Drug Resistance, and Recurrent Infection
Desai, J. V., Mitchell, A. P., & Andes, D. R. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019729 · Cited by 252 · see citing works
Genomic Plasticity of the Human Fungal Pathogen Candida albicans
Selmecki, A., Forche, A., & Berman, J. (2010) · Eukaryotic Cell · doi:10.1128/ec.00060-10 · Cited by 247 · see citing works
Candida albicans Scavenges Host Zinc via Pra1 during Endothelial Invasion
Citiulo, F., Jacobsen, I. D., Miramón, P., Schild, L., Brunke, S., Zipfel, P., Brock, M., Hube, B., & Wilson, D. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1002777 · Cited by 242 · see citing works
Self-citation
Two unlike cousins: <scp>C</scp> andida albicans and <scp>C</scp> . glabrata infection strategies
Brunke, S., & Hube, B. (2013) · Cellular Microbiology · doi:10.1111/cmi.12091 · Cited by 239 · see citing works
Self-citation
Iron - a key nexus in the virulence of Aspergillus fumigatus
Haas, H. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00028 · Cited by 217 · see citing works
Candida Survival Strategies
Polke, M., Hube, B., & Jacobsen, I. D. (2015) · Advances in applied microbiology · doi:10.1016/bs.aambs.2014.12.002 · Cited by 188 · see citing works
Self-citation
SREBP Coordinates Iron and Ergosterol Homeostasis to Mediate Triazole Drug and Hypoxia Responses in the Human Fungal Pathogen Aspergillus fumigatus
Blatzer, M., Barker, B. M., Willger, S. D., Beckmann, N., Blosser, S. J., Cornish, E. J., Mazurie, A., Grahl, N., Haas, H., & Cramer, R. A. (2011) · PLoS Genetics · doi:10.1371/journal.pgen.1002374 · Cited by 175 · see citing works
Metabolism in fungal pathogenesis
Ene, I. V., Brunke, S., Brown, A. J. P., & Hube, B. (2014) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a019695 · Cited by 169 · see citing works
Self-citation
Candida albicans Inhibits Pseudomonas aeruginosa Virulence through Suppression of Pyochelin and Pyoverdine Biosynthesis
Lopez-Medina, E., Fan, D., Coughlin, L. A., Ho, E. X., Lamont, I. L., Reimmann, C., Hooper, L. V., & Koh, A. Y. (2015) · PLOS Pathogens · doi:10.1371/journal.ppat.1005129 · Cited by 143 · see citing works
Iron homeostasis—Achilles’ heel of Aspergillus fumigatus?
Schrettl, M., & Haas, H. (2011) · Current Opinion in Microbiology · doi:10.1016/j.mib.2011.06.002 · Cited by 139 · see citing works
Essential metals at the host-pathogen interface: nutritional immunity and micronutrient assimilation by human fungal pathogens
Crawford, A., & Wilson, D. (2015) · FEMS Yeast Research · doi:10.1093/femsyr/fov071 · Cited by 120 · see citing works
Self-citation
Non-canonical signalling mediates changes in fungal cell wall PAMPs that drive immune evasion
Pradhan, A., Avelar, G. M., Bain, J. M., Childers, D., Pelletier, C., Larcombe, D. E., Shekhova, E., Netea, M. G., Brown, G. D., Erwig, L., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-13298-9 · Cited by 119 · see citing works
Iron at the Centre of Candida albicans Interactions
Fourie, R., Kuloyo, O. O., Mochochoko, B. M., Albertyn, J., & Pohl, C. H. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00185 · Cited by 118 · see citing works
A Relay Network of Extracellular Heme-Binding Proteins Drives C. albicans Iron Acquisition from Hemoglobin
Kuznets, G., Vigonsky, E., Weissman, Z., Lalli, D., Gildor, T., Kauffman, S. J., Turano, P., Becker, J., Lewinson, O., & Kornitzer, D. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1004407 · Cited by 118 · see citing works
Adaptation of Cryptococcus neoformans to Mammalian Hosts: Integrated Regulation of Metabolism and Virulence
Kronstad, J., Saikia, S., Nielson, E. D., Kretschmer, M., Jung, W. H., Hu, G., Geddes, J. M. H., Griffiths, E., Choi, J., Cadieux, B., et al. (2011) · Eukaryotic Cell · doi:10.1128/ec.05273-11 · Cited by 116 · see citing works
Cap2-HAP complex is a critical transcriptional regulator that has dual but contrasting roles in regulation of iron homeostasis in Candida albicans
Singh, R. P., Prasad, H. K., Sinha, I., Agarwal, N., & Natarajan, K. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.233569 · Cited by 113 · see citing works
Candida albicans specializations for iron homeostasis: from commensalism to virulence
Noble, S. M. (2013) · Current Opinion in Microbiology · doi:10.1016/j.mib.2013.09.006 · Cited by 104 · see citing works
FungiFun: A web-based application for functional categorization of fungal genes and proteins
Priebe, S., Linde, J., Albrecht, D., Guthke, R., & Brakhage, A. A. (2010) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2010.11.001 · Cited by 98 · see citing works
Conserved and Divergent Roles of Bcr1 and CFEM Proteins in Candida parapsilosis and Candida albicans
Ding, C., Vidanes, G. M., Maguire, S. L., Guida, A., Synnott, J. M., Andes, D. R., & Butler, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028151 · Cited by 93 · see citing works
Elevated catalase expression in a fungal pathogen is a double-edged sword of iron
Pradhan, A., Herrero-de-Dios, C. M., Belmonte, R. C., Budge, S., López, A., Kolmogorova, A., Lee, K. K., Martin, B. D., Ribeiro, A., Bebes, A., et al. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006405 · Cited by 91 · see citing works
Opportunistic yeast pathogens: reservoirs, virulence mechanisms, and therapeutic strategies
Polvi, E. J., Li, X., O’Meara, T. R., Leach, M. D., & Cowen, L. E. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1860-z · Cited by 90 · see citing works
Pseudomonas aeruginosa secreted factors impair biofilm development in Candida albicans
Holcombe, L. J., McAlester, G., Munro, C. A., Enjalbert, B., Brown, A. J. P., Gow, N. A. R., Ding, C., Butler, G., O'Gara, F., & Morrissey, J. P. (2010) · Microbiology · doi:10.1099/mic.0.037549-0 · Cited by 82 · see citing works
RNA Enrichment Method for Quantitative Transcriptional Analysis of Pathogens In Vivo Applied to the Fungus Candida albicans
Amorim-Vaz, S., Tran, V. D. T., Pradervand, S., Pagni, M., Coste, A. T., & Sanglard, D. (2015) · mBio · doi:10.1128/mbio.00942-15 · Cited by 78 · see citing works
An encapsulation of iron homeostasis and virulence in Cryptococcus neoformans
Kronstad, J. W., Hu, G., & Jung, W. H. (2013) · Trends in Microbiology · doi:10.1016/j.tim.2013.05.007 · Cited by 78 · see citing works
Structural basis of haem-iron acquisition by fungal pathogens
Nasser, L., Weissman, Z., Pinsky, M., Amartely, H., Dvir, H., & Kornitzer, D. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.156 · Cited by 76 · see citing works
Systems Biology of Fungal Infection
Horn, F., Heinekamp, T., Kniemeyer, O., Pollmächer, J., Valiante, V., & Brakhage, A. A. (2012) · Frontiers in Microbiology · doi:10.3389/fmicb.2012.00108 · Cited by 72 · see citing works
Overview of selected virulence attributes in Aspergillus fumigatus, Candida albicans, Cryptococcus neoformans, Trichophyton rubrum, and Exophiala dermatitidis
Boral, H., Metin, B., Döğen, A., Seyedmousavi, S., & İlkit, M. (2017) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2017.10.008 · Cited by 71 · see citing works
Regulation of mammalian siderophore 2,5-DHBA in the innate immune response to infection
Liu, Z., Reba, S., Chen, W.-D., Porwal, S. K., Boom, W. H., Petersen, R. B., Rojas, R., Viswanathan, R., & Devireddy, L. (2014) · Journal of Experimental Medicine · doi:10.1084/jem.20132629 · Cited by 70 · see citing works
Calcineurin Signaling and Membrane Lipid Homeostasis Regulates Iron Mediated MultiDrug Resistance Mechanisms in Candida albicans
Hameed, S., Dhamgaye, S., Singh, A., Goswami, S. K., & Prasad, R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018684 · Cited by 69 · see citing works
Fungal iron availability during deep seated candidiasis is defined by a complex interplay involving systemic and local events
Potrykus, J., Stead, D., MacCallum, D. M., Urgast, D. S., Raab, A., van Rooijen, N., Feldmann, J., & Brown, A. J. P. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003676 · Cited by 66 · see citing works
A novel role of the vacuolar calcium channel Yvc1 in stress response, morphogenesis and pathogenicity of Candida albicans
Yu, Q., Wang, F., Zhao, Q., Chen, J., Zhang, B., Ding, X., Wang, H., Yang, B., Lu, G., Zhang, B., et al. (2013) · International Journal of Medical Microbiology · doi:10.1016/j.ijmm.2013.11.022 · Cited by 66 · see citing works
Candida albicans FRE8 encodes a member of the NADPH oxidase family that produces a burst of ROS during fungal morphogenesis
Rossi, D. C. P., Gleason, J. E., Sánchez, H., Schatzman, S. S., Culbertson, E. M., Johnson, C. J., McNees, C. A., Coelho, C., Nett, J. E., Andes, D. R., et al. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006763 · Cited by 67 · see citing works
Dynamic Transcript Profiling of Candida albicans Infection in Zebrafish: A Pathogen-Host Interaction Study
Chen, Y. Y., Chao, C., Liu, F., Hsu, P., Chen, H.-F., Peng, S.-C., Chuang, Y., Lan, C., Hsieh, W., & Wong, D. S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0072483 · Cited by 64 · see citing works
Nutrient-Limited Operational Strategies for the Microbial Production of Biochemicals
Rajpurohit, H., & Eiteman, M. A. (2022) · Microorganisms · doi:10.3390/microorganisms10112226 · Cited by 62 · see citing works
Zinc Exploitation by Pathogenic Fungi
Wilson, D., Citiulo, F., & Hube, B. (2012) · PLoS Pathogens · doi:10.1371/journal.ppat.1003034 · Cited by 62 · see citing works
Self-citation
Comparison of the hemolytic activity between C. albicans and non-albicans Candida species
Rossoni, R. D., Barbosa, J. O., Vilela, S. F. G., Jorge, A. O. C., & Junqueira, J. C. (2013) · Brazilian Oral Research · doi:10.1590/s1806-83242013000600007 · Cited by 62 · see citing works
Regulatory Networks Controlling Nitrogen Sensing and Uptake in Candida albicans
Ramachandra, S., Linde, J., Brock, M., Guthke, R., Hube, B., & Brunke, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092734 · Cited by 61 · see citing works
Self-citation
Bacterial-fungal metabolic interactions within the microbiota and their potential relevance in human health and disease: a short review
Lapière, A., & Richard, M. L. (2022) · Gut Microbes · doi:10.1080/19490976.2022.2105610 · Cited by 61 · see citing works
Hemoglobin Uptake by Paracoccidioides spp. Is Receptor-Mediated
Bailão, E. F. L. C., Parente, J. A., Pigosso, L. L., de Castro, K. P., Fonseca, F. L., Bailão, M. G. S., Báo, S. N., Bailão, A. M., Rodrigues, M. L., Hernández, O., et al. (2014) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0002856 · Cited by 60 · see citing works
Iron acquisition in the cystic fibrosis lung and potential for novel therapeutic strategies
Tyrrell, J., & Callaghan, M. (2016) · Microbiology · doi:10.1099/mic.0.000220 · Cited by 56 · see citing works
In Vivo Systematic Analysis of Candida albicans Zn2-Cys6 Transcription Factors Mutants for Mice Organ Colonization
Vandeputte, P., Ischer, F., Sanglard, D., & Coste, A. T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026962 · Cited by 56 · see citing works
Cell wall proteome of pathogenic fungi
Karkowska‐Kuleta, J., & Kozik, A. (2015) · Acta Biochimica Polonica · doi:10.18388/abp.2015_1032 · Cited by 53 · see citing works
Functional characterization of the ferroxidase, permease high‐affinity iron transport complex from Candida albicans
Ziegler, L., Terzulli, A., Gaur, R., McCarthy, R., & Kosman, D. J. (2011) · Molecular Microbiology · doi:10.1111/j.1365-2958.2011.07704.x · Cited by 53 · see citing works
Conflicting interests in the pathogen–host tug of war: fungal micronutrient scavenging versus mammalian nutritional immunity
Potrykus, J., Ballou, E. R., Childers, D. S., & Brown, A. J. P. (2014) · PLoS Pathogens · doi:10.1371/journal.ppat.1003910 · Cited by 52 · see citing works
Metal Chelation as a Powerful Strategy to Probe Cellular Circuitry Governing Fungal Drug Resistance and Morphogenesis
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Authors: Almeida, R. S., Wilson, D., & Hube, B.
Affiliations: Universidade de São Paulo (BR)
Leibniz-Institut für Naturstoff-Forschung und Infektionsbiologie e. V. - Hans-Knöll-Institut (HKI) (DE)
Corresponding author: Hube, Bernhard
ORCID: Almeida, Ricardo S.
Wilson, Duncan
Hube, Bernhard
Venue: FEMS Yeast Research
Publisher: Oxford University Press (OUP)
Published: 2009-11
Volume: 9
Issue: 7
Pages: 1000-1012
ISSN: 1567-1356 (ISSN-L)
1567-1364
DOI: 10.1111/j.1567-1364.2009.00570.x
OpenAlex: W2160042020
Semantic Scholar: 4b748f190f18862bde0e478cf1e0d43e77d953bd
Cited by: 199
References: 120
Citations by year: 2026: 2 · 2025: 13 · 2024: 10 · 2023: 11 · 2022: 11 · 2021: 14 · 2020: 10 · 2019: 10 · 2018: 5 · 2017: 17 · 2016: 9 · 2015: 14 · 2014: 18 · 2013: 21 · 2012: 11
FWCI: 1.26
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: FEMS Yeast Research (publishedVersion)
PubMed (publishedVersion)
Funders: Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
Keywords: Candida albicans, iron acquisition, fungal virulence, hemoglobin, transferrin, lactoferrin, ferritin, host-pathogen interaction, fungal pathogenicity
MeSH terms: Candida albicans, Humans, Iron, Models, Biological, Virulence

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Candida albicans iron acquisition within the host

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