Essential metals at the host-pathogen interface: Nutritional immunity and micronutrient assimilation by human fungal pathogens

FEMS Yeast Research

Volumn 15, Issue 7, 2015, Pages

  Crawford, Aaron ^a   Wilson, Duncan ^a  

^a Institute of Medical Science   (United Kingdom)

Author keywords

Fungal pathogenicity; Host pathogen interactions; Iron; Zinc

Indexed keywords

CALGRANULIN; FERRITIN; HEME; IRON; SIDEROPHORE; TRACE ELEMENT; ZINC; METAL;

FUNGAL VIRULENCE; FUNGUS IMMUNITY; HOST PATHOGEN INTERACTION; HUMAN; MACROPHAGE; MYCOSIS; NONHUMAN; NUTRIENT UPTAKE; SHORT SURVEY; FUNGUS; IMMUNOLOGY; METABOLISM; MYCOSES;

FUNGI; HOST-PATHOGEN INTERACTIONS; HUMANS; METALS; MICRONUTRIENTS; MYCOSES;

EID: 84994292491     PISSN: 15671356     EISSN: 15671364     Source Type: Journal    
DOI: 10.1093/femsyr/fov071     Document Type: Short Survey

References (95)

1. Almeida RS, Brunke S, Albrecht A, et al. The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog 2008;4:e1000217.
2. Almeida RS, Wilson D, Hube B. Candida albicans iron acquisition within the host. FEMS Yeast Res 2009;9:1000-12.
3. Amich J, Vicentefranqueira R, Leal F, et al. Aspergillus fumigatus survival in alkaline and extreme zinc-limiting environments relies on the induction of a zinc homeostasis system encoded by the zrfC and aspf2 genes. Eukaryot Cell 2010;9:424-37.
4. Amich J, Vicentefranqueira R, Mellado E, et al. The ZrfC alkaline zinc transporter is required for Aspergillus fumigatus virulence and its growth in the presence of the Zn/Mn-chelating protein calprotectin. Cell Microbiol 2014;16:548-64.
5. Bailãao EF, Parente JA, Pigosso LL, et al. Hemoglobin uptake by Paracoccidioides spp. is receptor-mediated. PLoS Neglect Trop D 2014;8:e2856.
6. Bensen ES, Martin SJ, Li M, et al. Transcriptional profiling in Candida albicans reveals new adaptive responses to extracellular pH and functions for Rim101p. Mol Microbiol 2004;54:1335-51.
7. Bowman BH, Taylor JW, White TJ. Molecular evolution of the fungi: human pathogens. Mol Biol Evol 1992;9:893-904.
8. Branzk N, Lubojemska A, Hardison SE, et al. Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol 2014;15:1017-25.
9. Braun BR, Head WS,Wang MX, et al. Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 2000;156:31-44.
10. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science 2004;303:1532-5.
11. Brown GD, Denning DW, Gow NA, et al. Hidden killers: human fungal infections. Sci Transl Med 2012;4:165rv113.
12. Brunke S, Hube B. Adaptive prediction as a strategy in microbial infections. PLoS Pathog 2014;10:e1004356.
13. Cadieux B, Lian T, Hu G, et al. The mannoprotein Cig1 supports iron acquisition from heme and virulence in the pathogenic fungus Cryptococcus neoformans. J Infect Dis 2013;207:1339-47.
14. Citiulo F, Jacobsen ID, Miramon P, et al. Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathog 2012;8:e1002777.
15. Conklin DS, McMaster JA, Culbertson MR, et al. COT1, a gene involved in cobalt accumulation in Saccharomyces cerevisiae. Mol Cell Biol 1992;12:3678-88.
16. Corbin BD, Seeley EH, Raab A, et al. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 2008;319:962-5.
17. Dalle F, Wachtler B, L'Ollivier C, et al. Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell Microbiol 2010;12:248-71.
18. Dantas Ada S, Day A, Ikeh M, et al. Oxidative stress responses in the human fungal pathogen, Candida albicans. Biomolecules 2015;5:142-65.
19. Ding C, Festa RA, Chen YL, et al. Cryptococcus neoformans copper detoxification machinery is critical for fungal virulence. Cell Host Microbe 2013;13:265-76.
20. Edgeworth J, Gorman M, Bennett R, et al. Identification of p8,14 as a highly abundant heterodimeric calcium binding protein complex of myeloid cells. J Biol Chem 1991;266:7706-13.
21. Eigentler A, Schulz TF, Larcher C, et al. C3bi-binding protein on Candida albicans: temperature-dependent expression and relationship to human complement receptor type 3. Infect Immun 1989;57:616-22.
22. Fradin C, De Groot P, MacCallum D, et al. Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood. Mol Microbiol 2005;56: 397-415.
23. Fritz P, Beck-Jendroschek V, Brasch J. Inhibition of dermatophytes by the antimicrobial peptides human betadefensin- 2, ribonuclease 7 and psoriasin. Med Mycol 2012;50: 579-84.
24. Frohner IE, Bourgeois C, Yatsyk K, et al. Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol Microbiol 2009;71:240-52.
25. Gao HL, Feng WY, Li XL, et al. Golgi apparatus localization of ZNT7 in the mouse cerebellum. Histol Histopathol 2009;24:567-72.
26. Garć ia-Santamarina S, Thiele DJ. Copper at the fungal pathogenhost axis. J Biol Chem 2015;290:18945-53.
27. Glaser R, Harder J, Lange H, et al. Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 2005;6:57-64.
28. Gleason JE, Galaleldeen A, Peterson RL, et al. Candida albicans SOD5 represents the prototype of an unprecedented class of Cu-only superoxide dismutases required for pathogen defense. PNAS 2014;111:5866-71.
29. Haas H. Fungal siderophore metabolism with a focus on Aspergillus fumigatus. Nat Prod Rep 2014;31:1266-76.
30. Hansberg W, Salas-Lizana R, Dominguez L. Fungal catalases: function, phylogenetic origin and structure. Arch Biochem Biophys 2012;525:170-80.
31. Heymann P, Gerads M, Schaller M, et al. The siderophore iron transporter of Candida albicans (Sit1p/Arn1p) mediates uptake of ferrichrome-type siderophores and is required for epithelial invasion. Infect Immun 2002;70:5246-55.
32. Hood MI, Skaar EP. Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 2012;10: 525-37.
33. Hwang CS, Rhie GE, Oh JH, et al. Copper- and zinc-containing superoxide dismutase (Cu/ZnSOD) is required for the protection of Candida albicans against oxidative stresses and the expression of its full virulence. Microbiology 2002;148:3705-13.
34. Kaloriti D, Jacobsen M, Yin Z, et al. Mechanisms underlying the exquisite sensitivity of Candida albicans to combinatorial cationic and oxidative stress that enhances the potent fungicidal activity of phagocytes. mBio 2014;5:e01334-14.
35. Kaloriti D, Tillmann A, Cook E, et al. Combinatorial stresses kill pathogenic Candida species. Med Mycol 2012;50:699-709.
36. Kamizono A, Nishizawa M, Teranishi Y, et al. Identification of a gene conferring resistance to zinc and cadmium ions in the yeast Saccharomyces cerevisiae. Mol Gen Genet 1989;219:161-7.
37. Kehl-Fie TE, Skaar EP. Nutritional immunity beyond iron: a role for manganese and zinc. Curr Opin Chem Biol 2010;14:218-24.
38. Kim MJ, Kil M, Jung JH, et al. Roles of Zinc-responsive transcription factor Csr1 in filamentous growth of the pathogenic Yeast Candida albicans. J Microbiol Biotechn 2008;18:242-7.
39. Kornitzer D. Fungal mechanisms for host iron acquisition. Curr Opin Microbiol 2009;12:377-83.
40. Kumamoto CA. Niche-specific gene expression during C. albicans infection. Curr Opin Microbiol 2008;11:325-30.
41. Kuznets G, Vigonsky E,Weissman Z, et al. A relay network of extracellular heme-binding proteins drives C. albicans iron acquisition from hemoglobin. PLoS Pathog 2014;10:e1004407.
42. Leitch JM, Yick PJ, Culotta VC. The right to choose:multiple pathways for activating copper,zinc superoxide dismutase. J Biol Chem 2009;284:24679-83.
43. Lorenz MC, Bender JA, Fink GR. Transcriptional response of Candida albicans upon internalization by macrophages. Eukaryot Cell 2004;3:1076-87.
44. McCormick A, Heesemann L, Wagener J, et al. NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microbes Infect/ Institut Pasteur 2010;12:928-36.
45. McCormick NH, Kelleher SL. ZnT4 provides zinc to zincdependent proteins in the trans-Golgi network critical for cell function and Zn export in mammary epithelial cells. Am J Physiol- Cell Ph 2012;303:C291-7.
46. MacDiarmid CW, Gaither LA, Eide D. Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 2000;19:2845-55.
47. McDonagh A, Fedorova ND, Crabtree J, et al. Sub-telomere directed gene expression during initiation of invasive aspergillosis. PLoS Pathog 2008;4:e1000154.
48. Manns JM, Mosser DM, Buckley HR. Production of a hemolytic factor by Candida albicans. Infect Immun 1994;62: 5154-6.
49. Martchenko M, Alarco AM, Harcus D, et al. Superoxide dismutases in Candida albicans: transcriptional regulation and functional characterization of the hyphal-induced SOD5 gene. Mol Biol Cell 2004;15:456-67.
50. Mech F, Wilson D, Lehnert T, et al. Epithelial invasion outcompetes hypha development during Candida albicans infection as revealed by an image-based systems biology approach. Cytometry A 2014;85:126-39.
51. Miramon P, Dunker C, Windecker H, et al. Cellular responses of Candida albicans to phagocytosis and the extracellular activities of neutrophils are critical to counteract carbohydrate starvation, oxidative and nitrosative stress. PloS One 2012;7:e52850.
52. Miramon P, Kasper L, Hube B. Thriving within the host: Candida spp. interactions with phagocytic cells. Med Microbiol Immunol 2013;202:183-95.
53. Mitchell A, Romano GH, Groisman B, et al. Adaptive prediction of environmental changes by microorganisms. Nature 2009;460:220-4.
54. Mochon AB, Jin Y, Kayala MA, et al. Serological profiling of a Candida albicans protein microarray reveals permanent hostpathogen interplay and stage-specific responses during candidemia. PLoS Pathog 2010;6:e1000827.
55. Moors MA, Stull TL, Blank KJ, et al. A role for complement receptor-like molecules in iron acquisition by Candida albicans. J Exp Med 1992;175:1643-51.
56. Moreno MA, Ibrahim-Granet O, Vicentefranqueira R, et al. The regulation of zinc homeostasis by the ZafA transcriptional activator is essential for Aspergillus fumigatus virulence. Mol Microbiol 2007;64:1182-97.
57. Moyes DL, Murciano C, Runglall M, et al. Candida albicans yeast and hyphae are discriminated by MAPK signaling in vaginal epithelial cells. PloS One 2011;6:e26580.
58. Moyes DL, Naglik JR. Mucosal immunity and Candida albicans infection. Clin Dev Immunol 2011;2011:346307.
59. Nairz M, Haschka D, Demetz E, et al. Iron at the interface of immunity and infection. Front Pharmacol 2014;5:152.
60. Nevitt T, Thiele DJ. Host iron withholding demands siderophore utilization for Candida glabrata to survive macrophage killing. PLoS Pathog 2011;7:e1001322.
61. Neyrolles O, Mintz E, Catty P. Zinc and copper toxicity in host defense against pathogens: Mycobacterium tuberculosis as a model example of an emerging paradigm. Front Cell Infect Microbiol 2013;3:89.
62. Nobile CJ, Mitchell AP. Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol 2005;15:1150-5.
63. Nobile CJ, Nett JE, Hernday AD, et al. Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol 2009;7:e1000133.
64. Pendrak ML, Chao MP, Yan SS, et al. Heme oxygenase in Candida albicans is regulated by hemoglobin and is necessary for metabolism of exogenous heme and hemoglobin to alphabiliverdin. J Biol Chem 2004;279:3426-33.
65. Potrykus J, Ballou ER, Childers DS, et al. Conflicting interests in the pathogen-host tug of war: fungal micronutrient scavenging versus mammalian nutritional immunity. PLoS Pathog 2014;10:e1003910.
66. Potrykus J, Stead D, Maccallum DM, et al. Fungal iron availability during deep seated candidiasis is defined by a complex interplay involving systemic and local events. PLoS Pathog 2013;9:e1003676.
67. Ramanan N,Wang Y. A high-affinity iron permease essential for Candida albicans virulence. Science 2000;288:1062-4.
68. Schneider Rde O, Diehl C, Dos Santos FM, et al. Effects of zinc transporters on Cryptococcus gattii virulence. Sci Rep 2015;5:10104.
69. Schneider Rde O, Fogaca Nde S, Kmetzsch L, et al. Zap1 regulates zinc homeostasis and modulates virulence in Cryptococcus gattii. PloS One 2012;7:e43773.
70. Schrettl M, Bignell E, Kragl C, et al. Siderophore biosynthesis but not reductive iron assimilation is essential for Aspergillus fumigatus virulence. J Exp Med 2004;200:1213-9.
71. Seider K, Heyken A, Luttich A, et al. Interaction of pathogenic yeasts with phagocytes: survival, persistence and escape. Curr Opin Microbiol 2010;13:392-400.
72. Simm C, Lahner B, Salt D, et al. Saccharomyces cerevisiae vacuole in zinc storage and intracellular zinc distribution. Eukaryot Cell 2007;6:1166-77.
73. Soloviev DA, FonziWA, Sentandreu R, et al. Identification of pHregulated antigen 1 released from Candida albicans as the major ligand for leukocyte integrin alphaMbeta2. J Immunol 2007;178:2038-46.
74. Stringaro A, Crateri P, Adriani D, et al. Expression of the complement-binding protein (MP60) of Candida albicans in experimental vaginitis. Mycopathologia 1998;144:147-52.
75. Subramanian Vignesh K, Landero Figueroa JA, Porollo A, et al. Granulocyte macrophage-colony stimulating factor induced Zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival. Immunity 2013a;39: 697-710.
76. Subramanian Vignesh K, Landero Figueroa JA, Porollo A, et al. Zinc sequestration: arming phagocyte defense against fungal attack. PLoS Pathog 2013b;9:e1003815.
77. Thewes S, Kretschmar M, Park H, et al. In vivo and ex vivo comparative transcriptional profiling of invasive and non-invasive Candida albicans isolates identifies genes associated with tissue invasion. Mol Microbiol 2007;63:1606-28.
78. Urban CF, Ermert D, Schmid M, et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 2009;5:e1000639.
79. Urban CF, Reichard U, Brinkmann V, et al. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol 2006;8:668-76.
80. Vicentefranqueira R, Moreno MA, Leal F, et al. The zrfA and zrfB genes of Aspergillus fumigatus encode the zinc transporter proteins of a zinc uptake system induced in an acid, zinc-depleted environment. Eukaryot Cell 2005;4: 837-48.
81. Wachtler B, Wilson D, Haedicke K, et al. From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PloS One 2011;6:e17046.
82. Waldron KJ, Rutherford JC, Ford D, et al. Metalloproteins and metal sensing. Nature 2009;460:823-30.
83. Weissman Z, Berdicevsky I, Cavari BZ, et al. The high copper tolerance of Candida albicans is mediated by a P-type ATPase. PNAS 2000;97:3520-5.
84. Weissman Z, Kornitzer D. A family of Candida cell surface haembinding proteins involved in haemin and haemoglobin-iron utilization. Mol Microbiol 2004;53:1209-20.
85. Weissman Z, Shemer R, Conibear E, et al. An endocytic mechanism for haemoglobin-iron acquisition in Candida albicans. Mol Microbiol 2008;69:201-17.
86. Wilson D. An evolutionary perspective on zinc uptake by human fungal pathogens. Metallomics 2015;7:979-85.
87. Wilson D, Citiulo F, Hube B. Zinc exploitation by pathogenic fungi. PLoS Pathog 2012;8:e1003034.
88. Wilson D, Mayer FL, Miramon P, et al. Distinct roles of Candida albicans-specific genes in host-pathogen interactions. Eukaryot Cell 2014;13:977-89.
89. Wilson D, Thewes S, Zakikhany K, et al. Identifying infectionassociated genes of Candida albicans in the postgenomic era. FEMS Yeast Res 2009;9:688-700.
90. Winters MS, Chan Q, Caruso JA, et al. Metallomic analysis of macrophages infected with Histoplasma capsulatum reveals a fundamental role for zinc in host defenses. J Infect Dis 2010;202:1136-45.
91. Xu W, Solis NV, Ehrlich RL, et al. Activation and alliance of regulatory pathways in C. albicans during mammalian infection. PLoS Biol 2015;13:e1002076.
92. Zhao H, Eide D. The yeast ZRT1 gene encodes the zinc transporter protein of a high-affinity uptake system induced by zinc limitation. PNAS 1996a;93:2454-8.
93. Zhao H, Eide D. The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J Biol Chem 1996b;271:23203-10.
94. Zhao H, Eide DJ. Zap1p, a metalloregulatory protein involved in zinc-responsive transcriptional regulation in Saccharomyces cerevisiae. Mol Cell Biol 1997;17:5044-52.
95. Zipfel PF, Skerka C, Kupka D, et al. Immune escape of the human facultative pathogenic yeast Candida albicans: the many faces of the Candida Pra1 protein. Int J Med Microbiol 2011;301: 423-30.