1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Microbiology
  4. Volume 78, 2024
  5. Article

Annual Review of Microbiology

Volume 78, 2024

Metals at the Host–Fungal Pathogen Battleground

Abstract

Fungal infections continue to represent a major threat to public health, particularly with the emergence of multidrug-resistant fungal pathogens. As part of the innate immune response, the host modulates the availability of metals as armament against pathogenic microbes, including fungi. The transition metals Fe, Cu, Zn, and Mn are essential micronutrients for all life forms, but when present in excess, these same metals are potent toxins. The host exploits the double-edged sword of these metals, and will either withhold metal micronutrients from pathogenic fungi or attack them with toxic doses. In response to these attacks, fungal pathogens cleverly adapt by modulating metal transport, metal storage, and usage of metals as cofactors for enzymes. Here we review the current state of understanding on Fe, Cu, Zn, and Mn at the host–fungal pathogen battleground and provide perspectives for future research, including a hope for new antifungals based on metals.

Keyword(s): copper, fungal pathogen, immunity, iron, manganese, zinc
Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-041222-023745
2024-11-20
2024-12-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/78/1/annurev-micro-041222-023745.html?itemId=/content/journals/10.1146/annurev-micro-041222-023745&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Agranoff D, Collins L, Kehres D, Harrison T, Maguire M, Krishna S. 2005.. The Nramp orthologue of Cryptococcus neoformans is a pH-dependent transporter of manganese, iron, cobalt and nickel. . Biochem. J. 385::225–32
     [Crossref] [Google Scholar]
  2. 2.
    Alkafeef SS, Lane S, Yu C, Zhou T, Solis NV, et al. 2020.. Proteomic profiling of the monothiol glutaredoxin Grx3 reveals its global role in the regulation of iron dependent processes. . PLOS Genet. 16::e1008881
     [Crossref] [Google Scholar]
  3. 3.
    Almeida F, Rodrigues ML, Coelho C. 2019.. The still underestimated problem of fungal diseases worldwide. . Front. Microbiol. 10::214
     [Crossref] [Google Scholar]
  4. 4.
    Andrawes N, Weissman Z, Pinsky M, Moshe S, Berman J, Kornitzer D. 2022.. Regulation of heme utilization and homeostasis in Candida albicans. . PLOS Genet. 18::e1010390
     [Crossref] [Google Scholar]
  5. 5.
    Andreini C, Bertini I, Rosato A. 2009.. Metalloproteomes: a bioinformatic approach. . Acc. Chem. Res. 42::1471–79
     [Crossref] [Google Scholar]
  6. 6.
    Armitage AE, Eddowes LA, Gileadi U, Cole S, Spottiswoode N, et al. 2011.. Hepcidin regulation by innate immune and infectious stimuli. . Blood 118::4129–39
     [Crossref] [Google Scholar]
  7. 7.
    Attarian R, Hu G, Sánchez-León E, Caza M, Croll D, et al. 2018.. The monothiol glutaredoxin Grx4 regulates iron homeostasis and virulence in Cryptococcus neoformans. . mBio 9::e02377-18
     [Crossref] [Google Scholar]
  8. 8.
    Avila DS, Puntel RL, Aschner M. 2013.. Manganese in health and disease. . Metal Ions Life Sci. 13::199–227
     [Crossref] [Google Scholar]
  9. 9.
    Bairwa G, Hee Jung W, Kronstad JW. 2017.. Iron acquisition in fungal pathogens of humans. . Metallomics 9::215–27
     [Crossref] [Google Scholar]
  10. 10.
    Ballou ER, Wilson D. 2016.. The roles of zinc and copper sensing in fungal pathogenesis. . Curr. Opin. Microbiol. 32::128–34
     [Crossref] [Google Scholar]
  11. 11.
    Bates S, MacCallum DM, Bertram G, Munro CA, Hughes HB, et al. 2005.. Candida albicans Pmr1p, a secretory pathway P-type Ca2+/Mn2+-ATPase, is required for glycosylation and virulence. . J. Biol. Chem. 280::23408–15
     [Crossref] [Google Scholar]
  12. 12.
    Bellotti D, Miller A, Rowińska-Żyrek M, Remelli M. 2022.. Zn2+ and Cu2+ binding to the extramembrane loop of Zrt2, a zinc transporter of Candida albicans. . Biomolecules 12::121
     [Crossref] [Google Scholar]
  13. 13.
    Besold AN, Gilston BA, Radin JN, Ramsoomair C, Culbertson EM, et al. 2018.. Role of calprotectin in withholding zinc and copper from Candida albicans. . Infect. Immun. 86::e00779-17
     [Crossref] [Google Scholar]
  14. 14.
    Brancaccio D, Gallo A, Piccioli M, Novellino E, Ciofi-Baffoni S, Banci L. 2017.. [4Fe-4S] cluster assembly in mitochondria and its impairment by copper. . J. Am. Chem. Soc. 139::719–30
     [Crossref] [Google Scholar]
  15. 15.
    Brophy MB, Nakashige TG, Gaillard A, Nolan EM. 2013.. Contributions of the S100A9 C-terminal tail to high-affinity Mn(II) chelation by the host-defense protein human calprotectin. . J. Am. Chem. Soc. 135::17804–17
     [Crossref] [Google Scholar]
  16. 16.
    Chen C, Noble SM. 2012.. Post-transcriptional regulation of the Sef1 transcription factor controls the virulence of Candida albicans in its mammalian host. . PLOS Pathog. 8::e1002956
     [Crossref] [Google Scholar]
  17. 17.
    Chen C, Pande K, French SD, Tuch BB, Noble SM. 2011.. An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis. . Cell Host Microbe 10::118–35
     [Crossref] [Google Scholar]
  18. 18.
    Citiulo F, Jacobsen ID, Miramón P, Schild L, Brunke S, et al. 2012.. Candida albicans scavenges host zinc via Pra1 during endothelial invasion. . PLOS Pathog. 8::e1002777
     [Crossref] [Google Scholar]
  19. 19.
    Clark HL, Jhingran A, Sun Y, Vareechon C, de Jesus Carrion S, et al. 2016.. Zinc and manganese chelation by neutrophil S100A8/A9 (calprotectin) limits extracellular Aspergillus fumigatus hyphal growth and corneal infection. . J. Immunol. 196::336–44
     [Crossref] [Google Scholar]
  20. 20.
    Crawford AC, Lehtovirta-Morley LE, Alamir O, Niemiec MJ, Alawfi B, et al. 2018.. Biphasic zinc compartmentalisation in a human fungal pathogen. . PLOS Pathog. 14::e1007013
     [Crossref] [Google Scholar]
  21. 21.
    Crowley JD, Traynor DA, Weatherburn DC. 2000.. Enzymes and proteins containing manganese: an overview. . Metal Ions Biol. Syst. 37::209–78
     [Google Scholar]
  22. 22.
    Culbertson EM, Bruno VM, Cormack BP, Culotta VC. 2020.. Expanded role of the Cu-sensing transcription factor Mac1p in Candida albicans. . Mol. Microbiol. 114::1006–18
     [Crossref] [Google Scholar]
  23. 23.
    Culbertson EM, Khan AA, Muchenditsi A, Lutsenko S, Sullivan DJ, et al. 2020.. Changes in mammalian copper homeostasis during microbial infection. . Metallomics 12::416–26
     [Crossref] [Google Scholar]
  24. 24.
    Culotta VC, Yang M, Hall MD. 2005.. Manganese transport and trafficking: lessons learned from Saccharomyces cerevisiae. . Eukaryot. Cell 4::1159–65
     [Crossref] [Google Scholar]
  25. 25.
    Damo SM, Kehl-Fie TE, Sugitani N, Holt ME, Rathi S, et al. 2013.. Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens. . PNAS 110::3841–46
     [Crossref] [Google Scholar]
  26. 26.
    Denning DW, Bromley MJ. 2015.. Infectious disease. How to bolster the antifungal pipeline. . Science 347::1414–16
     [Crossref] [Google Scholar]
  27. 27.
    Ding C, Festa RA, Chen YL, Espart A, Palacios Ò, et al. 2013.. Cryptococcus neoformans copper detoxification machinery is critical for fungal virulence. . Cell Host Microbe 13::265–76
     [Crossref] [Google Scholar]
  28. 28.
    Diss L, Blaudez D, Gelhaye E, Chalot M. 2011.. Genome-wide analysis of fungal manganese transporters, with an emphasis on Phanerochaete chrysosporium. . Environ. Microbiol. Rep. 3::367–82
     [Crossref] [Google Scholar]
  29. 29.
    Fan J, Zhang H, Li Y, Chen Z, Chen T, et al. 2021.. Identification and characterization of Nramp transporter AoNramp1 in Aspergillus oryzae. . 3 Biotech 11::452
     [Crossref] [Google Scholar]
  30. 30.
    Fisher MC, Henk DA, Briggs CJ, Brownstein JS, Madoff LC, et al. 2012.. Emerging fungal threats to animal, plant and ecosystem health. . Nature 484::186–94
     [Crossref] [Google Scholar]
  31. 31.
    Foote JW, Delves HT. 1984.. Albumin bound and alpha 2-macroglobulin bound zinc concentrations in the sera of healthy adults. . J. Clin. Pathol. 37::1050–54
     [Crossref] [Google Scholar]
  32. 32.
    Frey AG, Bird AJ, Evans-Galea MV, Blankman E, Winge DR, Eide DJ. 2011.. Zinc-regulated DNA binding of the yeast Zap1 zinc-responsive activator. . PLOS ONE 6::e22535
     [Crossref] [Google Scholar]
  33. 33.
    Ganz T. 2009.. Iron in innate immunity: starve the invaders. . Curr. Opin. Immunol. 21::63–67
     [Crossref] [Google Scholar]
  34. 34.
    Garcia-Santamarina S, Festa RA, Smith AD, Yu CH, Probst C, et al. 2018.. Genome-wide analysis of the regulation of Cu metabolism in Cryptococcus neoformans. . Mol. Microbiol. 108::473–94
     [Crossref] [Google Scholar]
  35. 35.
    Gross C, Kelleher M, Iyer VR, Brown PO, Winge DR. 2000.. Identification of the copper regulon in Saccharomyces cerevisiae by DNA microarrays. . J. Biol. Chem. 275::32310–16
     [Crossref] [Google Scholar]
  36. 36.
    Gupta M, Outten CE. 2020.. Iron-sulfur cluster signaling: the common thread in fungal iron regulation. . Curr. Opin. Chem. Biol. 55::189–201
     [Crossref] [Google Scholar]
  37. 37.
    Heymann P, Gerads M, Schaller M, Dromer F, Winkelmann G, Ernst JF. 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::5246–55
     [Crossref] [Google Scholar]
  38. 38.
    Hong-Hermesdorf A, Miethke M, Gallaher SA, Kropat J, Dodani SC, et al. 2014.. Sub-cellular metal imaging identifies dynamic sites of Cu accumulation in Chlamydomonas. . Nat. Chem. Biol. 10::1034–42
     [Crossref] [Google Scholar]
  39. 39.
    Hood MI, Skaar EP. 2012.. Nutritional immunity: transition metals at the pathogen-host interface. . Nat. Rev. Microbiol. 10::525–37
     [Crossref] [Google Scholar]
  40. 40.
    Hwang LH, Mayfield JA, Rine J, Sil A. 2008.. Histoplasma requires SID1, a member of an iron-regulated siderophore gene cluster, for host colonization. . PLOS Pathog. 4::e1000044
     [Crossref] [Google Scholar]
  41. 41.
    Irving H, Williams RJP. 1953.. The stability of transition-metal complexes. . J. Chem. Soc. 637::3192–210
     [Crossref] [Google Scholar]
  42. 42.
    Jeong J, Eide DJ. 2013.. The SLC39 family of zinc transporters. . Mol. Aspects Med. 34::612–19
     [Crossref] [Google Scholar]
  43. 43.
    Jungmann J, Reins H, Lee J, Romeo A, Hassett R, et al. 1993.. MAC1, a nuclear regulatory protein related to Cu-dependent transcription factors is involved in Cu/Fe utilization and stress resistance in yeast. . EMBO J. 13::5051–56
     [Crossref] [Google Scholar]
  44. 44.
    Kosman DJ. 2018.. The teleos of metallo-reduction and metallo-oxidation in eukaryotic iron and copper trafficking. . Metallomics 10::370–77
     [Crossref] [Google Scholar]
  45. 45.
    Kumar R, Breindel C, Saraswat D, Cullen PJ, Edgerton M. 2017.. Candida albicans Sap6 amyloid regions function in cellular aggregation and zinc binding, and contribute to zinc acquisition. . Sci. Rep. 7::2908
     [Crossref] [Google Scholar]
  46. 46.
    Kuznets G, Vigonsky E, Weissman Z, Lalli D, Gildor T, et al. 2014.. A relay network of extracellular heme-binding proteins drives C. albicans iron acquisition from hemoglobin. . PLOS Pathog. 10::e1004407
     [Crossref] [Google Scholar]
  47. 47.
    Li CX, Gleason JE, Zhang SX, Bruno VM, Cormack BP, Culotta VC. 2015.. Candida albicans adapts to host copper during infection by swapping metal cofactors for superoxide dismutase. . PNAS 112::E5336–42
     [Google Scholar]
  48. 48.
    Lionakis MS, Drummond RA, Hohl TM. 2023.. Immune responses to human fungal pathogens and therapeutic prospects. . Nat. Rev. Immunol. 23::433–52
     [Crossref] [Google Scholar]
  49. 49.
    Liuzzi JP, Lichten LA, Rivera S, Blanchard RK, Aydemir TB, et al. 2005.. Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. . PNAS 102::6843–48
     [Crossref] [Google Scholar]
  50. 50.
    Mackie J, Szabo EK, Urgast DS, Ballou ER, Childers DS, et al. 2016.. Host-imposed copper poisoning impacts fungal micronutrient acquisition during systemic Candida albicans infections. . PLOS ONE 11::e0158683
     [Crossref] [Google Scholar]
  51. 51.
    Macomber L, Imlay JA. 2009.. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. . PNAS 106::8344–49
     [Crossref] [Google Scholar]
  52. 52.
    Mesquita LA, Bailão AM, de Curcio JS, da Silva KLP, da Rocha Fernandes G, et al. 2023.. Global molecular response of Paracoccidioides brasiliensis to zinc deprivation: analyses at transcript, protein and microRNA levels. . J. Fungi 9::281
     [Crossref] [Google Scholar]
  53. 53.
    Misslinger M, Scheven MT, Hortschansky P, López-Berges MS, Heiss K, et al. 2019.. The monothiol glutaredoxin GrxD is essential for sensing iron starvation in Aspergillus fumigatus. . PLOS Genet. 15::e1008379
     [Crossref] [Google Scholar]
  54. 54.
    Moraes D, Rodrigues JGC, Silva MG, Soares LW, de Almeida Soares CM, et al. 2023.. Copper acquisition and detoxification machineries are conserved in dimorphic fungi. . Fungal Biol. Rev. 44::100296
     [Crossref] [Google Scholar]
  55. 55.
    Nairz M, Weiss G. 2020.. Iron in infection and immunity. . Mol. Aspects Med. 75::100864
     [Crossref] [Google Scholar]
  56. 56.
    Nakashige TG, Zhang B, Krebs C, Nolan EM. 2015.. Human calprotectin is an iron-sequestering host-defense protein. . Nat. Chem. Biol. 11::765–71
     [Crossref] [Google Scholar]
  57. 57.
    Nasser L, Weissman Z, Pinsky M, Amartely H, Dvir H, Kornitzer D. 2016.. Structural basis of haem-iron acquisition by fungal pathogens. . Nat. Microbiol. 1::16156
     [Crossref] [Google Scholar]
  58. 58.
    Nguyen QB, Kadotani N, Kasahara S, Tosa Y, Mayama S, Nakayashiki H. 2008.. Systematic functional analysis of calcium-signalling proteins in the genome of the rice-blast fungus, Magnaporthe oryzae, using a high-throughput RNA-silencing system. . Mol. Microbiol. 68::1348–65
     [Crossref] [Google Scholar]
  59. 59.
    Nicastro R, Gaillard H, Zarzuela L, Péli-Gulli MP, Fernández-García E, et al. 2022.. Manganese is a physiologically relevant TORC1 activator in yeast and mammals. . eLife 11::e80497
     [Crossref] [Google Scholar]
  60. 60.
    Nobile CJ, Nett JE, Hernday AD, Homann OR, Deneault JS, et al. 2009.. Biofilm matrix regulation by Candida albicans Zap1. . PLOS Biol. 7::e1000133
     [Crossref] [Google Scholar]
  61. 61.
    O'Halloran TV, Culotta VC. 2000.. Metallochaperones, an intracellular shuttle service for metal ions. . J. Biol. Chem. 275::25057–60
     [Crossref] [Google Scholar]
  62. 62.
    Park YS, Kang S, Seo H, Yun CW. 2018.. A copper transcription factor, AfMac1, regulates both iron and copper homeostasis in the opportunistic fungal pathogen Aspergillus fumigatus. . Biochem. J. 475::2831–45
     [Crossref] [Google Scholar]
  63. 63.
    Potrykus J, Stead D, MacCallum DM, Urgast DS, Raab A, et al. 2013.. Fungal iron availability during deep seated candidiasis is defined by a complex interplay involving systemic and local events. . PLOS Pathog. 9::e1003676
     [Crossref] [Google Scholar]
  64. 64.
    Probst C, Garcia-Santamarina S, Brooks JT, Van Der Kloet I, Baars O, et al. 2022.. Interactions between copper homeostasis and the fungal cell wall affect copper stress resistance. . PLOS Pathog. 18::e1010195
     [Crossref] [Google Scholar]
  65. 65.
    Raffa N, Osherov N, Keller NP. 2019.. Copper utilization, regulation, and acquisition by Aspergillus fumigatus. . Int. J. Mol. Sci. 20::1980
     [Crossref] [Google Scholar]
  66. 66.
    Raffa N, Won TH, Sukowaty A, Candor K, Cui C, et al. 2021.. Dual-purpose isocyanides produced by Aspergillus fumigatus contribute to cellular copper sufficiency and exhibit antimicrobial activity. . PNAS 118::e2015224118
     [Crossref] [Google Scholar]
  67. 67.
    Raja MR, Waterman SR, Qiu J, Bleher R, Williamson PR, O'Halloran TV. 2013.. A copper hyperaccumulation phenotype correlates with pathogenesis in Cryptococcus neoformans. . Metallomics 5::363–71
     [Crossref] [Google Scholar]
  68. 68.
    Ray SC, Rappleye CA. 2022.. Mac1-dependent copper sensing promotes Histoplasma adaptation to the phagosome during adaptive immunity. . mBio 13::e0377321
     [Crossref] [Google Scholar]
  69. 69.
    Riedelberger M, Penninger P, Tscherner M, Hadriga B, Brunnhofer C, et al. 2020.. Type I interferons ameliorate zinc intoxication of Candida glabrata by macrophages and promote fungal immune evasion. . iScience 23::101121
     [Crossref] [Google Scholar]
  70. 70.
    Robinson JR, Isikhuemhen OS, Anike FN. 2021.. Fungal-metal interactions: a review of toxicity and homeostasis. . J. Fungi 7::225
     [Crossref] [Google Scholar]
  71. 71.
    Ror S, Panwar SL. 2019.. Sef1-regulated iron regulon responds to mitochondria-dependent iron-sulfur cluster biosynthesis in Candida albicans. . Front. Microbiol. 10::1528
     [Crossref] [Google Scholar]
  72. 72.
    Rossi DCP, Figueroa JAL, Buesing WR, Candor K, Blancett LT, et al. 2021.. A metabolic inhibitor arms macrophages to kill intracellular fungal pathogens by manipulating zinc homeostasis. . J. Clin. Investig. 131::e147268
     [Crossref] [Google Scholar]
  73. 73.
    Rossi DCP, Gleason JE, Sanchez H, Schatzman SS, Culbertson EM, et al. 2017.. Candida albicans FRE8 encodes a member of the NADPH oxidase family that produces a burst of ROS during fungal morphogenesis. . PLOS Pathog. 13::e1006763
     [Crossref] [Google Scholar]
  74. 74.
    Roy U, Yaish S, Weissman Z, Pinsky M, Dey S, et al. 2022.. Ferric reductase-related proteins mediate fungal heme acquisition. . eLife 11::e80604
     [Crossref] [Google Scholar]
  75. 75.
    Savary S, Ficke A, Aubertot J-N, Hollier C. 2012.. Crop losses due to diseases and their implications for global food production losses and food security. . Food Secur. 4::519–37
     [Crossref] [Google Scholar]
  76. 76.
    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::1213–19
     [Crossref] [Google Scholar]
  77. 77.
    Shen Q, Beucler MJ, Ray SC, Rappleye CA. 2018.. Macrophage activation by IFN-γ triggers restriction of phagosomal copper from intracellular pathogens. . PLOS Pathog. 14::e1007444
     [Crossref] [Google Scholar]
  78. 78.
    Smith AD, Garcia-Santamarina S, Ralle M, Loiselle DR, Haystead TA, Thiele DJ. 2021.. Transcription factor-driven alternative localization of Cryptococcus neoformans superoxide dismutase. . J. Biol. Chem. 296::100391
     [Crossref] [Google Scholar]
  79. 79.
    Smith AD, Logeman BL, Thiele DJ. 2017.. Copper acquisition and utilization in fungi. . Annu. Rev. Microbiol. 71::597–623
     [Crossref] [Google Scholar]
  80. 80.
    Solis NV, Wakade RS, Filler SG, Krysan DJ. 2023.. Candida albicans oropharyngeal infection is an exception to iron-based nutritional immunity. . mBio 14::e0009523
     [Crossref] [Google Scholar]
  81. 81.
    Subramanian Vignesh K, Landero Figueroa JA, Porollo A, Caruso JA, Deepe GS Jr. 2013.. Granulocyte macrophage-colony stimulating factor induced Zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival. . Immunity 39::697–710
     [Crossref] [Google Scholar]
  82. 82.
    Sun TS, Ju X, Gao HL, Wang T, Thiele DJ, et al. 2014.. Reciprocal functions of Cryptococcus neoformans copper homeostasis machinery during pulmonary infection and meningoencephalitis. . Nat. Commun. 5::5550
     [Crossref] [Google Scholar]
  83. 83.
    Sunuwar L, Tomar V, Wildeman A, Culotta V, Melia J. 2023.. Hepatobiliary manganese homeostasis is dynamic in the setting of inflammation or infection in mice. . FASEB J. 37::e23123
     [Crossref] [Google Scholar]
  84. 84.
    Takács T, Németh MT, Bohner F, Vágvölgyi C, Jankovics F, et al. 2022.. Characterization and functional analysis of zinc trafficking in the human fungal pathogen Candida parapsilosis. . Open Biol. 12::220077
     [Crossref] [Google Scholar]
  85. 85.
    Tangen KL, Jung WH, Sham AP, Lian T, Kronstad JW. 2007.. The iron- and cAMP-regulated gene SIT1 influences ferrioxamine B utilization, melanization and cell wall structure in Cryptococcus neoformans. . Microbiology 153::29–41
     [Crossref] [Google Scholar]
  86. 86.
    Thiele D. 1988.. ACE1 regulates expression of the Saccharomyces cerevisiae metallothionein gene. . Mol. Cell. Biol. 8::2745–52
     [Google Scholar]
  87. 87.
    Toh EA, Ohkusu M, Ishiwada N, Watanabe A, Kamei K. 2022.. Genetic system underlying responses of Cryptococcus neoformans to cadmium. . Curr. Genet. 68::125–41
     [Crossref] [Google Scholar]
  88. 88.
    Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, et al. 2009.. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. . PLOS Pathog. 5::e1000639
     [Crossref] [Google Scholar]
  89. 89.
    Vallee BL, Auld DS. 1990.. Zinc coordination, function, and structure of zinc enzymes and other proteins. . Biochemistry 29::5647–59
     [Crossref] [Google Scholar]
  90. 90.
    van Wijlick L, Znaidi S, Hernández-Cervantes A, Basso V, Bachellier-Bassi S, d'Enfert C. 2022.. Functional portrait of Irf1 (Orf19.217), a regulator of morphogenesis and iron homeostasis in Candida albicans. . Front. Cell. Infect. Microbiol. 12::960884
     [Crossref] [Google Scholar]
  91. 91.
    Weissman Z, Berdicevsky I, Cavari BZ, Kornitzer D. 2000.. The high copper tolerance of Candida albicans is mediated by a P-type ATPase. . PNAS 97::3520–25
     [Crossref] [Google Scholar]
  92. 92.
    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::33949–56
     [Crossref] [Google Scholar]
  93. 93.
    Wiemann P, Perevitsky A, Lim FY, Shadkchan Y, Knox BP, et al. 2017.. Aspergillus fumigatus copper export machinery and reactive oxygen intermediate defense counter host copper-mediated oxidative antimicrobial offense. . Cell Rep. 19::1008–21
     [Crossref] [Google Scholar]
  94. 94.
    Wildeman AS, Patel NK, Cormack BP, Culotta VC. 2023.. The role of manganese in morphogenesis and pathogenesis of the opportunistic fungal pathogen Candida albicans. . PLOS Pathog. 19::e1011478
     [Crossref] [Google Scholar]
  95. 95.
    Wilson D. 2021.. The role of zinc in the pathogenicity of human fungal pathogens. . Adv. Appl. Microbiol. 117::35–61
     [Crossref] [Google Scholar]
  96. 96.
    Wu C, Guo Z, Zhang M, Chen H, Peng M, et al. 2022.. Golgi-localized calcium/manganese transporters FgGdt1 and FgPmr1 regulate fungal development and virulence by maintaining Ca2+ and Mn2+ homeostasis in Fusarium graminearum. . Environ. Microbiol. 24::4623–40
     [Crossref] [Google Scholar]
  97. 97.
    Xue P, Hu G, Jung WH, Kronstad JW. 2023.. Metals and the cell surface of Cryptococcus neoformans. . Curr. Opin. Microbiol. 74::102331
     [Crossref] [Google Scholar]
  98. 98.
    Zacchi LF, Gomez-Raja J, Davis DA. 2010.. Mds3 regulates morphogenesis in Candida albicans through the TOR pathway. . Mol. Cell. Biol. 30::3695–710
     [Crossref] [Google Scholar]
  99. 99.
    Zhai P, Chai Y, Lu L. 2022.. Fungal zinc homeostasis and its potential as an antifungal target: a focus on the human pathogen Aspergillus fumigatus. . Microorganisms 10::2469
     [Crossref] [Google Scholar]
  100. 100.
    Zhang X, Krause KH, Xenarios I, Soldati T, Boeckmann B. 2013.. Evolution of the ferric reductase domain (FRD) superfamily: modularity, functional diversification, and signature motifs. . PLOS ONE 8::e58126
     [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-micro-041222-023745
Loading
Metals at the Host–Fungal Pathogen Battleground
Annual Review of Microbiology 78, 23 (2024); https://doi.org/10.1146/annurev-micro-041222-023745
/content/journals/10.1146/annurev-micro-041222-023745
/content/journals/10.1146/annurev-micro-041222-023745
Loading

Data & Media loading...

Supplemental Materials

  • Supplemental Figures

file format pdf download PDF
  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error