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Annual Review of Microbiology

Volume 71, 2017

Copper Acquisition and Utilization in Fungi

Abstract

Fungal cells colonize and proliferate in distinct niches, from soil and plants to diverse tissues in human hosts. Consequently, fungi are challenged with the goal of obtaining nutrients while simultaneously elaborating robust regulatory mechanisms to cope with a range of availability of nutrients, from scarcity to excess. Copper is essential for life but also potentially toxic. In this review we describe the sophisticated homeostatic mechanisms by which fungi acquire, utilize, and control this biochemically versatile trace element. Fungal pathogens, which can occupy distinct host tissues that have their own intrinsic requirements for copper homeostasis, have evolved mechanisms to acquire copper to successfully colonize the host, disseminate to other tissues, and combat host copper bombardment mechanisms that would otherwise mitigate virulence.

Keyword(s): compartmentalization, metals, pathogenesis, transcription, transporter, virulence
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2017-09-08
2025-04-30
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Literature Cited

  1. Achard ME, Stafford SL, Bokil NJ, Chartres J, Bernhardt PV. 1.  et al. 2012. Copper redistribution in murine macrophages in response to Salmonella infection. Biochem. J. 444:51–57 [Google Scholar]
  2. Akoumianaki T, Kyrmizi I, Valsecchi I, Gresnigt MS, Samonis G. 2.  et al. 2016. Aspergillus cell wall melanin blocks LC3-associated phagocytosis to promote pathogenicity. Cell Host Microbe 19:79–90 [Google Scholar]
  3. Aller SG, Eng ET, De Feo CJ, Unger VM. 3.  2004. Eukaryotic CTR copper uptake transporters require two faces of the third transmembrane domain for helix packing, oligomerization, and function. J. Biol. Chem. 279:53435–41 [Google Scholar]
  4. Andersson M, Mattle D, Sitsel O, Klymchuk T, Nielsen AM. 4.  et al. 2014. Copper-transporting P-type ATPases use a unique ion-release pathway. Nat. Struct. Mol. Biol. 21:43–48 [Google Scholar]
  5. Arnesano F, Banci L, Bertini I, Cantini F, Ciofi-Baffoni S. 5.  et al. 2001. Characterization of the binding interface between the copper chaperone Atx1 and the first cytosolic domain of Ccc2 ATPase. J. Biol. Chem. 276:41365–76 [Google Scholar]
  6. Arnesano F, Banci L, Bertini I, Huffman DL, O'Halloran TV. 6.  2001. Solution structure of the Cu(I) and apo forms of the yeast metallochaperone, Atx1. Biochemistry 40:1528–39 [Google Scholar]
  7. Askwith C, Eide D, Van Ho A, Bernard PS, Li L. 7.  et al. 1994. The FET3 gene of S. cerevisiae encodes a multicopper oxidase required for ferrous iron uptake. Cell 76:403–10 [Google Scholar]
  8. Banci L, Bertini I, Cantini F, Felli IC, Gonnelli L. 8.  et al. 2006. The Atx1-Ccc2 complex is a metal-mediated protein-protein interaction. Nat. Chem. Biol. 2:367–68 [Google Scholar]
  9. Banci L, Bertini I, Chasapis CT, Rosato A, Tenori L. 9.  2007. Interaction of the two soluble metal-binding domains of yeast Ccc2 with copper(I)-Atx1. Biochem. Biophys. Res. Commun. 364:645–49 [Google Scholar]
  10. Banci L, Bertini I, Ciofi-Baffoni S, Huffman DL, O'Halloran TV. 10.  2001. Solution structure of the yeast copper transporter domain Ccc2a in the apo and Cu(I)-loaded states. J. Biol. Chem. 276:8415–26 [Google Scholar]
  11. Banci L, Bertini I, Ciofi-Baffoni S, Kozyreva T, Zovo K, Palumaa P. 11.  2010. Affinity gradients drive copper to cellular destinations. Nature 465:645–48 [Google Scholar]
  12. Barelle CJ, Priest CL, Maccallum DM, Gow NA, Odds FC, Brown AJ. 12.  2006. Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell Microbiol 8:961–71 [Google Scholar]
  13. Beaudoin J, Ioannoni R, Mailloux S, Plante S, Labbé S. 13.  2013. Transcriptional regulation of the copper transporter Mfc1 in meiotic cells. Eukaryot. Cell 12:575–90 [Google Scholar]
  14. Beaudoin J, Labbé S. 14.  2001. The fission yeast copper-sensing transcription factor Cuf1 regulates the copper transporter gene expression through an Ace1/Amt1-like recognition sequence. J. Biol. Chem. 276:15472–80 [Google Scholar]
  15. Beaudoin J, Labbé S. 15.  2006. Copper induces cytoplasmic retention of fission yeast transcription factor Cuf1. Eukaryot. Cell 5:277–92 [Google Scholar]
  16. Beaudoin J, Labbé S. 16.  2007. Crm1-mediated nuclear export of the Schizosaccharomyces pombe transcription factor Cuf1 during a shift from low to high copper concentrations. Eukaryot. Cell 6:764–75 [Google Scholar]
  17. Beaudoin J, Mercier A, Langlois R, Labbé S. 17.  2003. The Schizosaccharomyces pombe Cuf1 is composed of functional modules from two distinct classes of copper metalloregulatory transcription factors. J. Biol. Chem. 278:14565–77 [Google Scholar]
  18. Beaudoin J, Thiele DJ, Labbé S, Puig S. 18.  2011. Dissection of the relative contribution of the Schizosaccharomyces pombe Ctr4 and Ctr5 proteins to the copper transport and cell surface delivery functions. Microbiology 157:1021–31 [Google Scholar]
  19. Bedard K, Krause KH. 19.  2007. The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol. Rev. 87:245–313 [Google Scholar]
  20. Beers J, Glerum DM, Tzagoloff A. 20.  1997. Purification, characterization, and localization of yeast Cox17p, a mitochondrial copper shuttle. J. Biol. Chem. 272:33191–96 [Google Scholar]
  21. Bellemare DR, Shaner L, Morano KA, Beaudoin J, Langlois R, Labbé S. 21.  2002. Ctr6, a vacuolar membrane copper transporter in Schizosaccharomyces pombe. J. Biol. Chem. 277:46676–86 [Google Scholar]
  22. Bertini I, Felli IC, Gonnelli L, Pierattelli R, Spyranti Z, Spyroulias GA. 22.  2006. Mapping protein-protein interaction by 13C′-detected heteronuclear NMR spectroscopy. J. Biomol. NMR 36:111–22 [Google Scholar]
  23. Bertini I, Hartmann HJ, Klein T, Liu G, Luchinat C, Weser U. 23.  2000. High resolution solution structure of the protein part of Cu7 metallothionein. Eur. J. Biochem. 267:1008–18 [Google Scholar]
  24. Brenes-Pomales A, Lindegren G, Lindegren CC. 24.  1955. Gene control of copper-sensitivity in Saccharomyces. Nature 176:841–42 [Google Scholar]
  25. Brouwer M, Brouwer-Hoexum T. 25.  1992. Glutathione-mediated transfer of copper(I) into American lobster apohemocyanin. Biochemistry 31:4096–102 [Google Scholar]
  26. Broxton CN, Culotta VC. 26.  2016. SOD enzymes and microbial pathogens: surviving the oxidative storm of infection. PLOS Pathog 12:e1005295 [Google Scholar]
  27. Carr HS, George GN, Winge DR. 27.  2002. Yeast Cox11, a protein essential for cytochrome c oxidase assembly, is a Cu(I)-binding protein. J. Biol. Chem. 277:31237–42 [Google Scholar]
  28. Chiarla C, Giovannini I, Siegel JH. 28.  2008. Patterns of correlation of plasma ceruloplasmin in sepsis. J. Surg. Res. 144:107–10 [Google Scholar]
  29. Cobine PA, McKay RT, Zangger K, Dameron CT, Armitage IM. 29.  2004. Solution structure of Cu6 metallothionein from the fungus Neurospora crassa. Eur. J. Biochem. 271:4213–21 [Google Scholar]
  30. Cobine PA, Ojeda LD, Rigby KM, Winge DR. 30.  2004. Yeast contain a non-proteinaceous pool of copper in the mitochondrial matrix. J. Biol. Chem. 279:14447–55 [Google Scholar]
  31. Cobine PA, Pierrel F, Bestwick ML, Winge DR. 31.  2006. Mitochondrial matrix copper complex used in metallation of cytochrome oxidase and superoxide dismutase. J. Biol. Chem. 281:36552–59 [Google Scholar]
  32. Corazza A, Harvey I, Sadler PJ. 32.  1996. 1H, 13C-NMR and X-ray absorption studies of copper(I) glutathione complexes. Eur. J. Biochem. 236:697–705 [Google Scholar]
  33. Culotta VC, Howard WR, Liu XF. 33.  1994. CRS5 encodes a metallothionein-like protein in Saccharomyces cerevisiae. J. Biol. Chem. 269:25295–302 [Google Scholar]
  34. Culotta VC, Hsu T, Hu S, Fürst P, Hamer D. 34.  1989. Copper and the ACE1 regulatory protein reversibly induce yeast metallothionein gene transcription in a mouse extract. PNAS 86:8377–81 [Google Scholar]
  35. Culotta VC, Joh HD, Lin SJ, Slekar KH, Strain J. 35.  1995. A physiological role for Saccharomyces cerevisiae copper/zinc superoxide dismutase in copper buffering. J. Biol. Chem. 270:29991–97 [Google Scholar]
  36. Culotta VC, Klomp LW, Strain J, Casareno RL, Krems B, Gitlin JD. 36.  1997. The copper chaperone for superoxide dismutase. J. Biol. Chem. 272:23469–72 [Google Scholar]
  37. Dameron CT, Winge DR, George GN, Sansone M, Hu S, Hamer D. 37.  1991. A copper-thiolate polynuclear cluster in the ACE1 transcription factor. PNAS 88:6127–31 [Google Scholar]
  38. Damo SM, Kehl-Fie TE, Sugitani N, Holt ME, Rathi S. 38.  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 [Google Scholar]
  39. Dancis A, Haile D, Yuan DS, Klausner RD. 39.  1994. The Saccharomyces cerevisiae copper transport protein (Ctr1p): biochemical characterization, regulation by copper, and physiologic role in copper uptake. J. Biol. Chem. 269:25660–67 [Google Scholar]
  40. Dancis A, Yuan DS, Haile D, Askwith C, Eide D. 40.  et al. 1994. Molecular characterization of a copper transport protein in S. cerevisiae: an unexpected role for copper in iron transport. Cell 76:393–402 [Google Scholar]
  41. Davis-Kaplan SR, Askwith CC, Bengtzen AC, Radisky D, Kaplan J. 41.  1998. Chloride is an allosteric effector of copper assembly for the yeast multicopper oxidase Fet3p: an unexpected role for intracellular chloride channels. PNAS 95:13641–45 [Google Scholar]
  42. de Bie P, Muller P, Wijmenga C, Klomp LW. 42.  2007. Molecular pathogenesis of Wilson and Menkes disease: Correlation of mutations with molecular defects and disease phenotypes. J. Med. Genet 44:673–88 [Google Scholar]
  43. De Feo CJ, Aller SG, Siluvai GS, Blackburn NJ, Unger VM. 43.  2009. Three-dimensional structure of the human copper transporter hCTR1. PNAS 106:4237–42 [Google Scholar]
  44. Ding C, Festa RA, Chen YL, Espart A, Palacios Ò. 44.  et al. 2013. Cryptococcus neoformans copper detoxification machinery is critical for fungal virulence. Cell Host Microbe 13:265–76 [Google Scholar]
  45. Ding C, Yin J, Tovar EM, Fitzpatrick DA, Higgins DG, Thiele DJ. 45.  2011. The copper regulon of the human fungal pathogen Cryptococcus neoformans H99. Mol. Microbiol. 81:1560–76 [Google Scholar]
  46. Dobi A, Dameron CT, Hu S, Hamer D, Winge DR. 46.  1995. Distinct regions of Cu(I)·ACE1 contact two spatially resolved DNA major groove sites. J. Biol. Chem. 270:10171–78 [Google Scholar]
  47. Ecker DJ, Butt TR, Sternberg EJ, Neeper MP, Debouck C. 47.  et al. 1986. Yeast metallothionein function in metal ion detoxification. J. Biol. Chem. 261:16895–900 [Google Scholar]
  48. Eisenman HC, Mues M, Weber SE, Frases S, Chaskes S. 48.  et al. 2007. Cryptococcus neoformans laccase catalyses melanin synthesis from both d- and l-DOPA. Microbiology 153:3954–62 [Google Scholar]
  49. Evans CF, Engelke DR, Thiele DJ. 49.  1990. ACE1 transcription factor produced in Escherichia coli binds multiple regions within yeast metallothionein upstream activation sequences. Mol. Cell Biol. 10:426–29 [Google Scholar]
  50. Farrell RA, Thorvaldsen JL, Winge DR. 50.  1996. Identification of the Zn(II) site in the copper-responsive yeast transcription factor, AMT1: a conserved Zn module. Biochemistry 35:1571–80 [Google Scholar]
  51. Ferreira AM, Ciriolo MR, Marcocci L, Rotilio G. 51.  1993. Copper(I) transfer into metallothionein mediated by glutathione. Biochem. J. 292:Part 3673–76 [Google Scholar]
  52. Festa RA, Thiele DJ. 52.  2011. Copper: an essential metal in biology. Curr. Biol. 21:R877–83 [Google Scholar]
  53. Fogel S, Welch JW. 53.  1982. Tandem gene amplification mediates copper resistance in yeast. PNAS 79:5342–46 [Google Scholar]
  54. Freedman JH, Ciriolo MR, Peisach J. 54.  1989. The role of glutathione in copper metabolism and toxicity. J. Biol. Chem. 264:5598–605 [Google Scholar]
  55. Freedman JH, Peisach J. 55.  1989. Intracellular copper transport in cultured hepatoma cells. Biochem. Biophys. Res. Commun. 164:134–40 [Google Scholar]
  56. Fridovich I. 56.  1978. The biology of oxygen radicals. Science 201:875–80 [Google Scholar]
  57. Fridovich I. 57.  1983. Superoxide radical: an endogenous toxicant. Annu. Rev. Pharmacol. Toxicol. 23:239–57 [Google Scholar]
  58. Fu D, Beeler TJ, Dunn TM. 58.  1995. Sequence, mapping and disruption of CCC2, a gene that cross-complements the Ca2+-sensitive phenotype of csg1 mutants and encodes a P-type ATPase belonging to the Cu2+-ATPase subfamily. Yeast 11:283–92 [Google Scholar]
  59. Fürst P, Hamer D. 59.  1989. Cooperative activation of a eukaryotic transcription factor: interaction between Cu(I) and yeast ACE1 protein. PNAS 86:5267–71 [Google Scholar]
  60. Fürst P, Hu S, Hackett R, Hamer D. 60.  1988. Copper activates metallothionein gene transcription by altering the conformation of a specific DNA binding protein. Cell 55:705–17 [Google Scholar]
  61. Gamonet F, Lauquin GJ. 61.  1998. The Saccharomyces cerevisiae LYS7 gene is involved in oxidative stress protection. Eur. J. Biochem. 251:716–23 [Google Scholar]
  62. Garber Morales J, Holmes-Hampton GP, Miao R, Guo Y, Munck E, Lindahl PA. 62.  2010. Biophysical characterization of iron in mitochondria isolated from respiring and fermenting yeast. Biochemistry 49:5436–44 [Google Scholar]
  63. García-Santamarina S, Thiele DJ. 63.  2015. Copper at the fungal pathogen-host axis. J. Biol. Chem. 290:18945–53 [Google Scholar]
  64. Gaxiola RA, Yuan DS, Klausner RD, Fink GR. 64.  1998. The yeast CLC chloride channel functions in cation homeostasis. PNAS 95:4046–50 [Google Scholar]
  65. Georgatsou E, Mavrogiannis LA, Fragiadakis GS, Alexandraki D. 65.  1997. The yeast Fre1p/Fre2p cupric reductases facilitate copper uptake and are regulated by the copper-modulated Mac1p activator. J. Biol. Chem. 272:13786–92 [Google Scholar]
  66. George GN, Byrd J, Winge DR. 66.  1988. X-ray absorption studies of yeast copper metallothionein. J. Biol. Chem. 263:8199–203 [Google Scholar]
  67. Germann UA, Lerch K. 67.  1987. Copper accumulation in the cell-wall-deficient slime variant of Neurospora crassa: comparison with a wild-type strain. Biochem. J. 245:479–84 [Google Scholar]
  68. Ghosh A, Trivedi PP, Timbalia SA, Griffin AT, Rahn JJ. 68.  et al. 2014. Copper supplementation restores cytochrome c oxidase assembly defect in a mitochondrial disease model of COA6 deficiency. Hum. Mol. Genet. 23:3596–606 [Google Scholar]
  69. Gleason JE, Galaleldeen A, Peterson RL, Taylor AB, Holloway SP. 69.  et al. 2014. Candida albicans SOD5 represents the prototype of an unprecedented class of Cu-only superoxide dismutases required for pathogen defense. PNAS 111:5866–71 [Google Scholar]
  70. Glerum DM, Shtanko A, Tzagoloff A. 70.  1996. Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J. Biol. Chem. 271:14504–9 [Google Scholar]
  71. Glerum DM, Shtanko A, Tzagoloff A. 71.  1996. SCO1 and SCO2 act as high copy suppressors of a mitochondrial copper recruitment defect in Saccharomyces cerevisiae. J. Biol. Chem. 271:20531–35 [Google Scholar]
  72. Gourdon P, Liu XY, Skjorringe T, Morth JP, Moller LB. 72.  et al. 2011. Crystal structure of a copper-transporting PIB-type ATPase. Nature 475:59–64 [Google Scholar]
  73. Gralla EB, Thiele DJ, Silar P, Valentine JS. 73.  1991. ACE1, a copper-dependent transcription factor, activates expression of the yeast copper, zinc superoxide dismutase gene. PNAS 88:8558–62 [Google Scholar]
  74. Hamer DH, Thiele DJ, Lemontt JE. 74.  1985. Function and autoregulation of yeast copperthionein. Science 228:685–90 [Google Scholar]
  75. Hassett R, Dix DR, Eide DJ, Kosman DJ. 75.  2000. The Fe(II) permease Fet4p functions as a low affinity copper transporter and supports normal copper trafficking in Saccharomyces cerevisiae. Biochem. J. 351:Part 2477–84 [Google Scholar]
  76. Hassett R, Kosman DJ. 76.  1995. Evidence for Cu(II) reduction as a component of copper uptake by Saccharomyces cerevisiae. J. Biol. Chem. 270:128–34 [Google Scholar]
  77. Hellman NE, Gitlin JD. 77.  2002. Ceruloplasmin metabolism and function. Annu. Rev. Nutr. 22:439–58 [Google Scholar]
  78. Hiser L, Di Valentin M, Hamer AG, Hosler JP. 78.  2000. Cox11p is required for stable formation of the CuB and magnesium centers of cytochrome c oxidase. J. Biol. Chem. 275:619–23 [Google Scholar]
  79. Hood MI, Skaar EP. 79.  2012. Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10:525–37 [Google Scholar]
  80. Horecka J, Kinsey PT, Sprague GF Jr.. 80.  1995. Cloning and characterization of the Saccharomyces cerevisiae LYS7 gene: evidence for function outside of lysine biosynthesis. Gene 162:87–92 [Google Scholar]
  81. Horng YC, Cobine PA, Maxfield AB, Carr HS, Winge DR. 81.  2004. Specific copper transfer from the Cox17 metallochaperone to both Sco1 and Cox11 in the assembly of yeast cytochrome c oxidase. J. Biol. Chem. 279:35334–40 [Google Scholar]
  82. Howell SB, Safaei R, Larson CA, Sailor MJ. 82.  2010. Copper transporters and the cellular pharmacology of the platinum-containing cancer drugs. Mol. Pharmacol. 77:887–94 [Google Scholar]
  83. Huffman DL, O'Halloran TV. 83.  2000. Energetics of copper trafficking between the Atx1 metallochaperone and the intracellular copper transporter, Ccc2. J. Biol. Chem. 275:18611–14 [Google Scholar]
  84. Huibregtse JM, Engelke DR, Thiele DJ. 84.  1989. Copper-induced binding of cellular factors to yeast metallothionein upstream activation sequences. PNAS 86:65–69 [Google Scholar]
  85. Iwasaki H, Matsubara T, Mori T. 85.  1967. A fungal laccase, its properties and reconstitution from its protein and copper. J. Biochem. 61:814–16 [Google Scholar]
  86. Jensen LT, Howard WR, Strain JJ, Winge DR, Culotta VC. 86.  1996. Enhanced effectiveness of copper ion buffering by CUP1 metallothionein compared with CRS5 metallothionein in Saccharomyces cerevisiae. J. Biol. Chem. 271:18514–19 [Google Scholar]
  87. Jensen LT, Posewitz MC, Srinivasan C, Winge DR. 87.  1998. Mapping of the DNA binding domain of the copper-responsive transcription factor Mac1 from Saccharomyces cerevisiae. J. Biol. Chem. 273:23805–11 [Google Scholar]
  88. Jensen LT, Winge DR. 88.  1998. Identification of a copper-induced intramolecular interaction in the transcription factor Mac1 from Saccharomyces cerevisiae. EMBO J. 17:5400–8 [Google Scholar]
  89. Jiang N, Liu X, Yang J, Li Z, Pan J, Zhu X. 89.  2011. Regulation of copper homeostasis by Cuf1 associates with its subcellular localization in the pathogenic yeast Cryptococcus neoformans H99. FEMS Yeast Res 11:440–48 [Google Scholar]
  90. Jungmann J, Reins HA, Lee J, Romeo A, Hassett R. 90.  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 12:5051–56 [Google Scholar]
  91. Kidane TZ, Farhad R, Lee KJ, Santos A, Russo E, Linder MC. 91.  2012. Uptake of copper from plasma proteins in cells where expression of CTR1 has been modulated. Biometals 25:697–709 [Google Scholar]
  92. Kloppel C, Suzuki Y, Kojer K, Petrungaro C, Longen S. 92.  et al. 2011. Mia40-dependent oxidation of cysteines in domain I of Ccs1 controls its distribution between mitochondria and the cytosol. Mol. Biol. Cell 22:3749–57 [Google Scholar]
  93. Knight SA, Labbé S, Kwon LF, Kosman DJ, Thiele DJ. 93.  1996. A widespread transposable element masks expression of a yeast copper transport gene. Genes Dev 10:1917–29 [Google Scholar]
  94. Kronstad JW, Attarian R, Cadieux B, Choi J, D'Souza CA. 94.  et al. 2011. Expanding fungal pathogenesis: Cryptococcus breaks out of the opportunistic box. Nat. Rev. Microbiol. 9:193–203 [Google Scholar]
  95. Labbé S, Peña MM, Fernandes AR, Thiele DJ. 95.  1999. A copper-sensing transcription factor regulates iron uptake genes in Schizosaccharomyces pombe. J. Biol. Chem. 274:36252–60 [Google Scholar]
  96. Labbé S, Zhu Z, Thiele DJ. 96.  1997. Copper-specific transcriptional repression of yeast genes encoding critical components in the copper transport pathway. J. Biol. Chem. 272:15951–58 [Google Scholar]
  97. Lamarre C, LeMay JD, Deslauriers N, Bourbonnais Y. 97.  2001. Candida albicans expresses an unusual cytoplasmic manganese-containing superoxide dismutase (SOD3 gene product) upon the entry and during the stationary phase. J. Biol. Chem. 276:43784–91 [Google Scholar]
  98. Lamb AL, Torres AS, O'Halloran TV, Rosenzweig AC. 98.  2000. Heterodimer formation between superoxide dismutase and its copper chaperone. Biochemistry 39:14720–7 [Google Scholar]
  99. Lamb AL, Torres AS, O'Halloran TV, Rosenzweig AC. 99.  2001. Heterodimeric structure of superoxide dismutase in complex with its metallochaperone. Nat. Struct. Biol. 8:751–55 [Google Scholar]
  100. Lamb AL, Wernimont AK, Pufahl RA, Culotta VC, O'Halloran TV, Rosenzweig AC. 100.  1999. Crystal structure of the copper chaperone for superoxide dismutase. Nat. Struct. Biol. 6:724–29 [Google Scholar]
  101. Lerch K. 101.  1980. Copper metallothionein, a copper-binding protein from Neurospora crassa. Nature 284:368–70 [Google Scholar]
  102. Li CX, Gleason JE, Zhang SX, Bruno VM, Cormack BP, Culotta VC. 102.  2015. Candida albicans adapts to host copper during infection by swapping metal cofactors for superoxide dismutase. PNAS 112:E5336–42 [Google Scholar]
  103. Lin CM, Crawford BF, Kosman DJ. 103.  1993. Distribution of 64Cu in Saccharomyces cerevisiae: cellular locale and metabolism. J. Gen. Microbiol. 139:1605–15 [Google Scholar]
  104. Lin SJ, Culotta VC. 104.  1995. The ATX1 gene of Saccharomyces cerevisiae encodes a small metal homeostasis factor that protects cells against reactive oxygen toxicity. PNAS 92:3784–88 [Google Scholar]
  105. Lin SJ, Pufahl RA, Dancis A, O'Halloran TV, Culotta VC. 105.  1997. A role for the Saccharomyces cerevisiae ATX1 gene in copper trafficking and iron transport. J. Biol. Chem. 272:9215–20 [Google Scholar]
  106. Lowe J, Vieyra A, Catty P, Guillain F, Mintz E, Cuillel M. 106.  2004. A mutational study in the transmembrane domain of Ccc2p, the yeast Cu(I)-ATPase, shows different roles for each Cys-Pro-Cys cysteine. J. Biol. Chem. 279:25986–94 [Google Scholar]
  107. Lu SC. 107.  2013. Glutathione synthesis. Biochim. Biophys. Acta 1830:3143–53 [Google Scholar]
  108. Mackie J, Szabo EK, Urgast DS, Ballou ER, Childers DS. 108.  et al. 2016. Host-imposed copper poisoning impacts fungal micronutrient acquisition during systemic Candida albicans infections. PLOS ONE 11:e0158683 [Google Scholar]
  109. Macomber L, Imlay JA. 109.  2009. The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. PNAS 106:8344–49 [Google Scholar]
  110. Marvin ME, Mason RP, Cashmore AM. 110.  2004. The CaCTR1 gene is required for high-affinity iron uptake and is transcriptionally controlled by a copper-sensing transactivator encoded by CaMAC1. Microbiology 150:2197–208 [Google Scholar]
  111. Mattle D, Zhang L, Sitsel O, Pedersen LT, Moncelli MR. 111.  et al. 2015. A sulfur-based transport pathway in Cu+-ATPases. EMBO Rep 16:728–40 [Google Scholar]
  112. Maxfield AB, Heaton DN, Winge DR. 112.  2004. Cox17 is functional when tethered to the mitochondrial inner membrane. J. Biol. Chem. 279:5072–80 [Google Scholar]
  113. Mehra RK, Tarbet EB, Gray WR, Winge DR. 113.  1988. Metal-specific synthesis of two metallothioneins and gamma-glutamyl peptides in Candida glabrata. PNAS 85:8815–19 [Google Scholar]
  114. Mesecke N, Terziyska N, Kozany C, Baumann F, Neupert W. 114.  et al. 2005. A disulfide relay system in the intermembrane space of mitochondria that mediates protein import. Cell 121:1059–69 [Google Scholar]
  115. Miras R, Morin I, Jacquin O, Cuillel M, Guillain F, Mintz E. 115.  2008. Interplay between glutathione, Atx1 and copper: 1. Copper(I) glutathionate induced dimerization of Atx1. J. Biol. Inorg. Chem. 13:195–205 [Google Scholar]
  116. Morin I, Gudin S, Mintz E, Cuillel M. 116.  2009. Dissecting the role of the N-terminal metal-binding domains in activating the yeast copper ATPase in vivo. FEBS J 276:4483–95 [Google Scholar]
  117. Nairz M, Fritsche G, Brunner P, Talasz H, Hantke K, Weiss G. 117.  2008. Interferon-γ limits the availability of iron for intramacrophage Salmonella typhimurium. Eur. J. Immunol. 38:1923–36 [Google Scholar]
  118. Nakashige TG, Zhang B, Krebs C, Nolan EM. 118.  2015. Human calprotectin is an iron-sequestering host-defense protein. Nat. Chem. Biol. 11:765–71 [Google Scholar]
  119. Nevitt T, Ohrvik H, Thiele DJ. 119.  2012. Charting the travels of copper in eukaryotes from yeast to mammals. Biochim. Biophys. Acta 1823:1580–93 [Google Scholar]
  120. Nittis T, George GN, Winge DR. 120.  2001. Yeast Sco1, a protein essential for cytochrome c oxidase function is a Cu(I)-binding protein. J. Biol. Chem. 276:42520–26 [Google Scholar]
  121. Oh KB, Watanabe T, Matsuoka H. 121.  1999. A novel copper-binding protein with characteristics of a metallothionein from a clinical isolate of Candida albicans. Microbiology 145:Part 92423–29 [Google Scholar]
  122. Park YS, Lian H, Chang M, Kang CM, Yun CW. 122.  2014. Identification of high-affinity copper transporters in Aspergillus fumigatus. Fungal Genet. Biol. 73:29–38 [Google Scholar]
  123. Pearce DA, Sherman F. 123.  1999. Toxicity of copper, cobalt, and nickel salts is dependent on histidine metabolism in the yeast Saccharomyces cerevisiae. J. Bacteriol. 181:4774–79 [Google Scholar]
  124. Pena MM, Puig S, Thiele DJ. 124.  2000. Characterization of the Saccharomyces cerevisiae high affinity copper transporter Ctr3. J. Biol. Chem. 275:33244–51 [Google Scholar]
  125. Peter C, Laliberté J, Beaudoin J, Labbé S. 125.  2008. Copper distributed by Atx1 is available to copper amine oxidase 1 in Schizosaccharomyces pombe. Eukaryot. Cell 7:1781–94 [Google Scholar]
  126. Peterson CW, Narula SS, Armitage IM. 126.  1996. 3D solution structure of copper and silver-substituted yeast metallothioneins. FEBS Lett 379:85–93 [Google Scholar]
  127. Peterson RL, Galaleldeen A, Villarreal J, Taylor AB, Cabelli DE. 127.  et al. 2016. The phylogeny and active site design of eukaryotic copper-only superoxide dismutases. J. Biol. Chem. 291:20911–23 [Google Scholar]
  128. Plante S, Ioannoni R, Beaudoin J, Labbé S. 128.  2014. Characterization of Schizosaccharomyces pombe copper transporter proteins in meiotic and sporulating cells. J. Biol. Chem. 289:10168–81 [Google Scholar]
  129. Portnoy ME, Rosenzweig AC, Rae T, Huffman DL, O'Halloran TV, Culotta VC. 129.  1999. Structure-function analyses of the ATX1 metallochaperone. J. Biol. Chem. 274:15041–45 [Google Scholar]
  130. Pufahl RA, Singer CP, Peariso KL, Lin SJ, Schmidt PJ. 130.  et al. 1997. Metal ion chaperone function of the soluble Cu(I) receptor Atx1. Science 278:853–56 [Google Scholar]
  131. Puig S, Lee J, Lau M, Thiele DJ. 131.  2002. Biochemical and genetic analyses of yeast and human high affinity copper transporters suggest a conserved mechanism for copper uptake. J. Biol. Chem. 277:26021–30 [Google Scholar]
  132. Rae TD, Schmidt PJ, Pufahl RA, Culotta VC, O'Halloran TV. 132.  1999. Undetectable intracellular free copper: the requirement of a copper chaperone for superoxide dismutase. Science 284:805–8 [Google Scholar]
  133. Ramírez MA, Lorenz MC. 133.  2007. Mutations in alternative carbon utilization pathways in Candida albicans attenuate virulence and confer pleiotropic phenotypes. Eukaryot. Cell 6:280–90 [Google Scholar]
  134. Ramos D, Mar D, Ishida M, Vargas R, Gaite M. 134.  et al. 2016. Mechanism of copper uptake from blood plasma ceruloplasmin by mammalian cells. PLOS ONE 11:e0149516 [Google Scholar]
  135. Reddehase S, Grumbt B, Neupert W, Hell K. 135.  2009. The disulfide relay system of mitochondria is required for the biogenesis of mitochondrial Ccs1 and Sod1. J. Mol. Biol. 385:331–38 [Google Scholar]
  136. Rees EM, Lee J, Thiele DJ. 136.  2004. Mobilization of intracellular copper stores by the Ctr2 vacuolar copper transporter. J. Biol. Chem. 279:54221–29 [Google Scholar]
  137. Rees EM, Thiele DJ. 137.  2007. Identification of a vacuole-associated metalloreductase and its role in Ctr2-mediated intracellular copper mobilization. J. Biol. Chem. 282:21629–38 [Google Scholar]
  138. Rentzsch A, Krummeck-Weiss G, Hofer A, Bartuschka A, Ostermann K, Rodel G. 138.  1999. Mitochondrial copper metabolism in yeast: mutational analysis of Sco1p involved in the biogenesis of cytochrome c oxidase. Curr. Genet. 35:103–8 [Google Scholar]
  139. Riggle PJ, Kumamoto CA. 139.  2000. Role of a Candida albicans P1-type ATPase in resistance to copper and silver ion toxicity. J. Bacteriol. 182:4899–905 [Google Scholar]
  140. Rosenzweig AC, Huffman DL, Hou MY, Wernimont AK, Pufahl RA, O'Halloran TV. 140.  1999. Crystal structure of the Atx1 metallochaperone protein at 1.02 Å resolution. Structure 7:605–17 [Google Scholar]
  141. Rustici G, van Bakel H, Lackner DH, Holstege FC, Wijmenga C. 141.  et al. 2007. Global transcriptional responses of fission and budding yeast to changes in copper and iron levels: a comparative study. Genome Biol 8:R73 [Google Scholar]
  142. Salas SD, Bennett JE, Kwon-Chung KJ, Perfect JR, Williamson PR. 142.  1996. Effect of the laccase gene CNLAC1, on virulence of Cryptococcus neoformans. J. Exp. Med. 184:377–86 [Google Scholar]
  143. Schaible UE, Sturgill-Koszycki S, Schlesinger PH, Russell DG. 143.  1998. Cytokine activation leads to acidification and increases maturation of Mycobacterium avium-containing phagosomes in murine macrophages. J. Immunol. 160:1290–96 [Google Scholar]
  144. Schulze M, Rodel G. 144.  1988. SCO1, a yeast nuclear gene essential for accumulation of mitochondrial cytochrome c oxidase subunit II. Mol. Gen. Genet. 211:492–98 [Google Scholar]
  145. Schwan WR, Warrener P, Keunz E, Stover CK, Folger KR. 145.  2005. Mutations in the cueA gene encoding a copper homeostasis P-type ATPase reduce the pathogenicity of Pseudomonas aeruginosa in mice. Int. J. Med. Microbiol 295:237–42 [Google Scholar]
  146. Sturtz LA, Diekert K, Jensen LT, Lill R, Culotta VC. 146.  2001. A fraction of yeast Cu,Zn-superoxide dismutase and its metallochaperone, CCS, localize to the intermembrane space of mitochondria: a physiological role for SOD1 in guarding against mitochondrial oxidative damage. J. Biol. Chem. 276:38084–89 [Google Scholar]
  147. Sun TS, Ju X, Gao HL, Wang T, Thiele DJ. 147.  et al. 2014. Reciprocal functions of Cryptococcus neoformans copper homeostasis machinery during pulmonary infection and meningoencephalitis. Nat. Commun. 5:5550 [Google Scholar]
  148. Szczypka MS, Thiele DJ. 148.  1989. A cysteine-rich nuclear protein activates yeast metallothionein gene transcription. Mol. Cell Biol. 9:421–29 [Google Scholar]
  149. Tamai KT, Gralla EB, Ellerby LM, Valentine JS, Thiele DJ. 149.  1993. Yeast and mammalian metallothioneins functionally substitute for yeast copper-zinc superoxide dismutase. PNAS 90:8013–17 [Google Scholar]
  150. Thiele DJ. 150.  1988. ACE1 regulates expression of the Saccharomyces cerevisiae metallothionein gene. Mol. Cell Biol. 8:2745–52 [Google Scholar]
  151. Thiele DJ, Walling MJ, Hamer DH. 151.  1986. Mammalian metallothionein is functional in yeast. Science 231:854–56 [Google Scholar]
  152. Thorvaldsen JL, Sewell AK, McCowen CL, Winge DR. 152.  1993. Regulation of metallothionein genes by the ACE1 and AMT1 transcription factors. J. Biol. Chem. 268:12512–18 [Google Scholar]
  153. Tsukihara T, Aoyama H, Yamashita E, Tomizaki T, Yamaguchi H. 153.  et al. 1995. Structures of metal sites of oxidized bovine heart cytochrome c oxidase at 2.8 Å. Science 269:1069–74 [Google Scholar]
  154. Turner RB, Smith DL, Zawrotny ME, Summers MF, Posewitz MC, Winge DR. 154.  1998. Solution structure of a zinc domain conserved in yeast copper-regulated transcription factors. Nat. Struct. Biol. 5:551–55 [Google Scholar]
  155. Tzagoloff A, Capitanio N, Nobrega MP, Gatti D. 155.  1990. Cytochrome oxidase assembly in yeast requires the product of COX11, a homolog of the P. denitrificans protein encoded by ORF3. EMBO J. 9:2759–64 [Google Scholar]
  156. Upadhyay S, Xu X, Lin X. 156.  2016. Interactions between melanin enzymes and their atypical recruitment to the secretory pathway by palmitoylation. mBio 7:e01925–16 [Google Scholar]
  157. Upadhyay S, Xu X, Lowry D, Jackson JC, Roberson RW, Lin X. 157.  2016. Subcellular compartmentalization and trafficking of the biosynthetic machinery for fungal melanin. Cell Rep 14:2511–18 [Google Scholar]
  158. Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H. 158.  et al. 2010. An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330:219–22 [Google Scholar]
  159. Vest KE, Leary SC, Winge DR, Cobine PA. 159.  2013. Copper import into the mitochondrial matrix in Saccharomyces cerevisiae is mediated by Pic2, a mitochondrial carrier family protein. J. Biol. Chem. 288:23884–92 [Google Scholar]
  160. Via LE, Fratti RA, McFalone M, Pagan-Ramos E, Deretic D, Deretic V. 160.  1998. Effects of cytokines on mycobacterial phagosome maturation. J. Cell Sci. 111:Part 7897–905 [Google Scholar]
  161. Wagner D, Maser J, Moric I, Vogt S, Kern WV, Bermudez LE. 161.  2006. Elemental analysis of the Mycobacterium avium phagosome in Balb/c mouse macrophages. Biochem. Biophys. Res. Commun. 344:1346–51 [Google Scholar]
  162. Waterman SR, Hacham M, Hu G, Zhu X, Park YD. 162.  et al. 2007. Role of a CUF1/CTR4 copper regulatory axis in the virulence of Cryptococcus neoformans. J. Clin. Investig. 117:794–802 [Google Scholar]
  163. Wegner SV, Sun F, Hernandez N, He C. 163.  2011. The tightly regulated copper window in yeast. Chem. Commun. 47:2571–73 [Google Scholar]
  164. Weissman Z, Berdicevsky I, Cavari BZ, Kornitzer D. 164.  2000. The high copper tolerance of Candida albicans is mediated by a P-type ATPase. PNAS 97:3520–25 [Google Scholar]
  165. Welch J, Fogel S, Buchman C, Karin M. 165.  1989. The CUP2 gene product regulates the expression of the CUP1 gene, coding for yeast metallothionein. EMBO J 8:255–60 [Google Scholar]
  166. White C, Lee J, Kambe T, Fritsche K, Petris MJ. 166.  2009. A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol. Chem. 284:33949–56 [Google Scholar]
  167. Williamson PR. 167.  1994. Biochemical and molecular characterization of the diphenol oxidase of Cryptococcus neoformans: identification as a laccase. J. Bacteriol. 176:656–64 [Google Scholar]
  168. Winge DR, Nielson KB, Gray WR, Hamer DH. 168.  1985. Yeast metallothionein: sequence and metal-binding properties. J. Biol. Chem. 260:14464–70 [Google Scholar]
  169. Wu X, Kim H, Seravalli J, Barycki JJ, Hart PJ. 169.  et al. 2016. Potassium and the K+/H+ exchanger Kha1p promote binding of copper to ApoFet3p multi-copper ferroxidase. J. Biol. Chem. 291:9796–806 [Google Scholar]
  170. Xiao Z, Brose J, Schimo S, Ackland SM, La Fontaine S, Wedd AG. 170.  2011. Unification of the copper(I) binding affinities of the metallo-chaperones Atx1, Atox1, and related proteins: detection probes and affinity standards. J. Biol. Chem. 286:11047–55 [Google Scholar]
  171. Yamaguchi-Iwai Y, Serpe M, Haile D, Yang W, Kosman DJ. 171.  et al. 1997. Homeostatic regulation of copper uptake in yeast via direct binding of MAC1 protein to upstream regulatory sequences of FRE1 and CTR1. J. Biol. Chem. 272:17711–18 [Google Scholar]
  172. Yan N. 172.  2015. Structural biology of the major facilitator superfamily transporters. Annu. Rev. Biophys. 44:257–83 [Google Scholar]
  173. Yasokawa D, Murata S, Kitagawa E, Iwahashi Y, Nakagawa R. 173.  et al. 2008. Mechanisms of copper toxicity in Saccharomyces cerevisiae determined by microarray analysis. Environ. Toxicol. 23:599–606 [Google Scholar]
  174. Yuan DS, Dancis A, Klausner RD. 174.  1997. Restriction of copper export in Saccharomyces cerevisiae to a late Golgi or post-Golgi compartment in the secretory pathway. J. Biol. Chem. 272:25787–93 [Google Scholar]
  175. Zhou H, Thiele DJ. 175.  2001. Identification of a novel high affinity copper transport complex in the fission yeast Schizosaccharomyces pombe. J. Biol. Chem. 276:20529–35 [Google Scholar]
  176. Zhou P, Thiele DJ. 176.  1993. Rapid transcriptional autoregulation of a yeast metalloregulatory transcription factor is essential for high-level copper detoxification. Genes Dev 7:1824–35 [Google Scholar]
  177. Zhou PB, Thiele DJ. 177.  1991. Isolation of a metal-activated transcription factor gene from Candidaglabrata by complementation in Saccharomyces cerevisiae. PNAS 88:6112–16 [Google Scholar]
  178. Zhu Z, Labbé S, Peña MM, Thiele DJ. 178.  1998. Copper differentially regulates the activity and degradation of yeast Mac1 transcription factor. J. Biol. Chem. 273:1277–80 [Google Scholar]
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Copper Acquisition and Utilization in Fungi
Annual Review of Microbiology 71, 597 (2017); https://doi.org/10.1146/annurev-micro-030117-020444
/content/journals/10.1146/annurev-micro-030117-020444
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