Copper at the fungal pathogen-host axis

Journal of Biological Chemistry

Volumn 290, Issue 31, 2015, Pages 18945-18953

  García Santamarina, Sarela ^a   Thiele, Dennis J ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COPPER; FUNGI; MACHINERY; TRACE ELEMENTS;

ANTIFUNGAL DRUGS; DEPENDENT PROCESS; FUNGAL INFECTION; FUNGAL PATHOGEN; INNATE IMMUNES; TOXIC TRACE ELEMENTS; TOXICITY MECHANISMS;

PATHOGENS;

COPPER; IONOPHORE; LACCASE; MELANIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE DISMUTASE; FUNGAL PROTEIN; METALLOPROTEIN;

BINDING AFFINITY; BIOACCUMULATION; BIOSYNTHESIS; CANDIDA ALBICANS; CELL COMPARTMENTALIZATION; CRYPTOCOCCUS NEOFORMANS; CYTOTOXICITY; ENZYME ACTIVITY; FUNGAL VIRULENCE; HOMEOSTASIS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOCOMPETENT CELL; INFECTION SENSITIVITY; INNATE IMMUNITY; MYCOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; ANIMAL; IMMUNOLOGY; MICROBIOLOGY; PHYSIOLOGY; VIRULENCE;

ANIMALS; COPPER; FUNGAL PROTEINS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; METALLOPROTEINS; MYCOSES; VIRULENCE;

EID: 84940563178     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R115.649129     Document Type: Review

References (88)

1. O'Brien, H. E., Parrent, J. L., Jackson, J. A., Moncalvo, J. M., and Vilgalys, R. (2005) Fungal community analysis by large-scale sequencing of environmental samples. Appl. Environ. Microbiol. 71, 5544-5550
2. Brown, G. D., Denning, D. W., Gow, N. A., Levitz, S. M., Netea, M. G., and White, T. C. (2012) Hidden killers: Human fungal infections. Sci. Transl. Med. 4, 165rv13
3. Park B. J. Wannemuehler K. A. Marston B. J. Govender N. Pappas P. G. Chiller T. M. 2009 Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. Aids 23 525-530
4. Richardson, M. D. (2005) Changing patterns and trends in systemic fungal infections. J. Antimicrob. Chemother. 56, Suppl. 1, i5-i11, 10.1093/jac/dki218
5. Brown, G. D., Denning, D. W., and Levitz, S. M. (2012) Tackling human fungal infections. Science 336, 647
6. Gray, K. C., Palacios, D. S., Dailey, I., Endo, M. M., Uno, B. E., Wilcock, B. C., and Burke, M. D. (2012) Amphotericin primarily kills yeast by simply binding ergosterol. Proc. Natl. Acad. Sci. U.S.A. 109, 2234-2239
7. Lass-Flö rl, C. (2011) Triazole antifungal agents in invasive fungal infections: A comparative review. Drugs 71, 2405-2419
8. Mukherjee, P. K., Sheehan, D., Puzniak, L., Schlamm, H., and Ghannoum, M. A. (2011) Echinocandins: Are they all the same? J. Chemother. 23, 319-325
9. Roemer, T., and Krysan, D. J. (2014) Antifungal drug development: Challenges, unmet clinical needs, and new approaches. Cold Spring Harb. Perspect. Med. 4, a019703
10. Kim, B. E., Nevitt, T., and Thiele, D. J. (2008) Mechanisms for copper acquisition, distribution and regulation. Nat. Chem. Biol. 4, 176-185
11. Lutsenko, S. (2010) Human copper homeostasis: A network of interconnected pathways. Curr. Opin. Chem. Biol. 14, 211-217
12. Ding, C., Festa, R. A., Sun, T. S., and Wang, Z. Y. (2014) Iron and copper as virulence modulators in human fungal pathogens. Mol. Microbiol. 93, 10-23
13. Nevitt, T., Ohrvik, H., and Thiele, D. J. (2012) Charting the travels of copper in eukaryotes from yeast to mammals. Biochim. Biophys. Acta 1823, 1580-1593
14. Chaturvedi, K. S., and Henderson, J. P. (2014) Pathogenic adaptations to host-derived antibacterial copper. Front. Cell Infect. Microbiol. 4, 3
15. Dupont, C. L., Grass, G., and Rensing, C. (2011) Copper toxicity and the origin of bacterial resistance: New insights and applications. Metallomics 3, 1109-1118
16. Ladomersky, E., and Petris, M. J. (2015) Copper tolerance and virulence in bacteria. Metallomics 7, 957-964
17. Samanovic, M. I., Ding, C., Thiele, D. J., and Darwin, K. H. (2012) Copper in microbial pathogenesis: Meddling with the metal. Cell Host. Microbe. 11, 106-115
18. Festa, R. A., and Thiele, D. J. (2011) Copper: An essential metal in biology. Curr. Biol. 21, R877-R883
19. Burq, V. (1867) Choléra; De l'immunité Acquise par les Ouvriers en Cuivre: Par Rapport au Choléra Enquêtes Faites à ce Sujet en France et en Italie; Pré servation et Traitement par les Armatures et les Sels De Cuivre, Observations et Expériences Depuis, G. Baillière, Paris
20. Dollwet, H. H. A., and Sorenson J. R. J. (1985) Historic uses of copper compounds in medicine. Trace Elem. Med. 2, 80-87
21. Millardet, P. M. A. (1933) The Discovery of Bordeaux Mixture: Three Papers, American Phytopathological Society, Ithaca, NY
22. Lazary, A., Weinberg, I., Vatine, J. J., Jefidoff, A., Bardenstein, R., Borkow, G., and Ohana, N. (2014) Reduction of healthcare-associated infections in a long-term care brain injury ward by replacing regular linens with biocidal copper oxide impregnated linens. Int. J. Infect. Dis. 24, 23-29
23. Casey, A. L., Adams, D., Karpanen, T. J., Lambert, P. A., Cookson, B. D., Nightingale, P., Miruszenko, L., Shillam, R., Christian, P., and Elliott, T. S. (2010) Role of copper in reducing hospital environment contamination. J. Hosp. Infect. 74, 72-77
24. Hood M. I. Skaar, E. P.(2012) Nutritional immunity: Transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10 525-537
25. Potrykus, J., Ballou, E. R., Childers, D. S., and Brown, A. J. (2 014) Conflicting interests in the pathogen-host tug of war: Fungal micronutrient scavenging versus mammalian nutritional immunity. PLoS Pathog. 10, e1003910
26. Hodgkinson, V., and Petris, M. J. (2012) Copper hom eostasis at the hostpathogen interface. J. Biol. Chem. 287, 13549-13555
27. Ding, C., Festa, R. A., Chen, Y. L., Espart, A., Palacios, Ò., Espín, J., Capdevila, M., Atrian, S., Heitman, J., and Thiel e, D. J. (2013) Cryptococcus neoformans copper detoxification machinery is critical for fungal virulence. Cell Host. Microbe. 13, 265-276
28. Sun, T. S., Ju, X., Gao, H. L., Wang, T., Thiele, D. J., Li, J. Y., Wang, Z. Y., and Ding, C. (2014) Reciprocal functions of Cryptococcus neoformans copper homeostasis machinery during pulmonary infectio n and meningoencephalitis. Nat. Commun. 5, 5550
29. Ding, C., Yin, J., Tovar, E. M., Fitzpatrick, D. A., Higgins, D. G., and Thiele, D. J. (2011) The copper regulon of the human fungal pathogen Cryptococcus neoformans H99. Mol. Microbiol. 81, 1560-1576
30. Banci, L., Bertini, I., Ciofi-Baffoni, S., Kozyreva, T., Zovo, K., and Palumaa, P. (2010) Affinity gradients drive copper to cellular destinations. Nature 465, 645-648
31. Culotta, V. C., Klomp, L. W., Strain, J., Casareno, R. L., Krems, B., and Gitlin, J. D. (1997) The copper chaperone for superoxide dismutase. J. Biol. Chem. 272, 23469-23472
32. Lin, S. J., Pufahl, R. A., Dancis, A., O'Halloran, T. V., and Culotta, V. C. (1997) A role for the Saccharomyces cerevisiae ATX1 gene in copper trafficking and iron transport. J. Biol. C hem. 272, 9215-9220
33. Walton, F. J., Idnurm, A., and Heitman, J. (2005) Novel gene functions required for melanization of the human pathogen Cryptococcus neoformans. Mol. Microbiol. 57, 1381-1396
34. Vest, K. E., Leary, S. C., Winge, D. R., and Cobine, P. A. (2013) Copper import into the mitochondrial matrix in Saccharomyces cerevisiae is mediated by Pic2, a mitochondrial carrier family protein. J. Biol. Chem. 288, 23884-23892
35. Dickinson, E. K., Adams, D. L., Schon, E. A., and Glerum, D. M. (2000) A human SCO2 mutation helps define the role of Sco1p in the cytochrome oxidase assembly pathway. J. Biol. Chem. 275, 26780-26785
36. Thrower, A. R., Byrd, J., Tarbet, E. B., Mehra, R. K., Hamer, D. H., and Winge, D. R. (1988) Effect of mutation of cysteinyl residues in yeast Cumetallothionein. J. Biol. Chem. 263, 7037-7042
37. Rees, E. M., Lee, J., and Thiele, D. J. (2004) Mobilization of intracellular copper stores by the Ctr2 vacuolar copper transporter. J. Biol. Chem. 279, 54221-54229
38. Weissman, Z., Berdicevsky, I., Cavari, B. Z., and Kornitzer, D. (2000) The high copper tolerance of Candida albicans is mediated by a P-type ATPase. Proc. Natl. Acad. Sci. U.S.A. 97, 3520-3525
39. Keller, G., Bird, A., and Winge, D. R. (2005) Independent metalloregulation of Ace1 and Mac1 in Saccharomyces cerevisiae. Eukaryot. Cell 4, 1863-1871
40. Yamaguchi-Iw ai, Y., Serpe, M., Haile, D., Yang, W., Kosman, D. J., Klausner, R. D., and Dancis, A. (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, 17711-17718
41. Dameron, C. T., Winge, D. R., George, G. N., Sansone, M., Hu, S., and Hamer, D. (1991) A copper-thiolate polynuclear cluster in the ACE1 transcription factor. Proc. Natl. Acad. Sci. U.S.A. 88, 6127-6131
42. Macomber, L., Rensing, C., and Imlay, J. A. (2007) Intracellular copper does not catalyze the formation of oxidative DNA damage in Escherichia coli. J. Bacteriol. 189, 1616-1626
43. Macomber, L., and Imlay, J. A. (2009) The iron-sulfur clusters of dehydratases are primary intracellular targets of copper toxicity. Proc. Natl. Acad. Sci. U.S.A. 106, 8344-8349
44. Stehling, O., Vashisht, A. A., Mascarenhas, J., Jonsson, Z. O., Sharma, T., Netz, D. J., Pierik, A. J., Wohlschlegel, J. A., and Lill, R. (2012) MMS19 assembles iron-sulfur proteins required for DNA metabolism and genomic integrity. Science 337, 195-199
45. Zhou, B., and Gitschier, J. (1997) hC TR1: A human gene for copper uptake identified by complementation in yeast. Proc. Natl. Acad. Sci. U.S.A. 94, 7481-7486
46. Rae T. D. Torres A. S. Pufahl R. A. O'Halloran T. V.(2001) Mechanism of Cu,Zn-superoxide dismutase activation by the human metallochaperone hCCS. J. Biol. Chem. 276 5166-5176
47. Hung, I. H., Suzuki, M., Yamaguchi, Y., Yuan, D. S., Klausner, R. D., and Gitlin, J. D. (1997) Biochemical characterization of the Wilson disease protein and functional expression in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 272, 21461-21466
48. Klomp, L. W., Lin, S. J., Yuan, D. S., Klausner, R. D., Culotta, V. C., and Gitlin, J. D. (1997) Identification and functional expression of HAH1, a novel human gene involved in copper homeostasis. J. Biol. Chem. 272, 9221-9226
49. Wagner, D., Maser, J., Lai, B., Cai, Z., Barry, C. E., 3rd, Höner Zu Bentrup, K., Russell, D. G., and Bermudez, L. E. (2005) Elemental analysis of Mycobacterium avium-, Mycobacterium tuberculosis-, and M ycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J. Immunol. 174, 1491-1500
50. White, C., Lee, J., Kambe, T., Fritsche, K., and Petris, M. J. (2009) A role for the ATP7A copper-transporting ATPase in macrophage bactericidal activity. J. Biol. Chem. 284, 33949-33956
51. Wolschendorf, F., Ackart, D., Shrestha, T. B., Hascall-Dove, L., Nolan S.Lamichhane, G., Wang, Y., Bossmann, S. H., Basaraba, R. J., and Niederweis, M. (2011) Copper resistance is essential for virulence of Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. U.S.A. 108, 1621-1626
52. Achard, M. E., Tree, J. J., Holden, J. A., Simpfendorfer, K. R., Wijburg, O. L., Strugnell, R. A., Schembri, M. A., Sweet, M. J., Jennings, M. P., and McEwan, A. G. (2010) The multi-copper-ion oxidase CueO of Salmonella enterica serovar Typhimurium is required for systemic virulence. Infect. Immun. 78, 2312-2319
53. Palacios, Ò., Espart, A., Espín, J., Ding, C., Thiel e, D. J., Atrian, S., and Capdevila, M. (2014) Full characterization of the Cu-, Zn-, and Cd-binding properties of CnMT1 and CnMT2, two metallothioneins of the pathogenic fungus Cryptococcus neoformans acting as virulence factors. Metallomics 6, 279-291
54. Mehra, R. K., Garey, J. R., Butt, T. R., Gray, W. R., and Winge, D. R. (1989) Candida glabrata metallothioneins: Cloning and sequence of the genes and characterization of proteins. J. Biol. Chem. 264, 19747-19753
55. Mehra, R. K., Thorvaldsen, J. L., Macreadie, I. G., and Winge, D. R. (1992) Disruption analysis of metallothionein-encoding genes in Candida glabrata. Gene. 114, 75-80
56. Gitlin, J. D. (1988) Transcriptional regulation of ceruloplasmin gene expression during inflammation. J. Biol. Chem. 263, 6281-6287
57. Cabrera, A., Alonzo, E., Sauble, E., Chu, Y. L., Nguyen, D., Linder, M. C., Sato, D. S., and Mason, A. Z. (2008) Copper binding components of blood plasma and organs, and their responses to influx of large doses of 65Cu, in the mouse. Biometa ls 21, 525-543
58. Linder, M. C. (2001) Copper and genomic stability in mammals. Mutat. Res. 475, 141-152
59. Ö hrvik, H., Nose, Y., Wood, L. K., Kim, B. E., Gleber, S. C., Ralle, M., and Thiele, D. J. (2013) Ctr2 regulates biogenesis of a cleaved form of mammalian Ctr1 metal transporter lacking the copper-and cisplatin-binding ecto-domain. Proc. Natl. Acad. Sci. U.S.A. 110, E4279-E4288
60. Manso, Y., Adlard, P. A., Carrasco, J., Vas?ák, M., and Hidalgo, J. (2011) Metallothionein and brain inflammation. J. Biol. Inorg. Chem. 16, 1103-1113
61. Chung, R. S., Penkowa, M., Dittman n, J., King, C. E., Bartlett, C., Asmussen, J. W., Hidalgo, J., Carrasco, J., Leung, Y. K., Walker, A. K., Fung, S. J., Dunlop, S. A., Fitzgerald, M., Beazley, L. D., Chuah, M. I., Vickers, J. C., and West, A. K. (2008) Redefining the role of metallothionein within the injured brain: Extracellular metallothioneins play an important role in the astrocyte-neuron response to injury. J. Biol. Chem. 283, 15349-15358
62. Patel, B. N., and David, S. (1997) A novel glycosylphosphatidylinositolanchored form of ceruloplasmin is expressed by mammalian astrocytes. J. Biol. Chem. 272, 20185-20190
63. Butler, M. J., and Da y, A. W. (1998) Fungal melanins: A review. Can. J. Microbiol. 44, 1115-1136
64. Dixon, D. M., Polak, A., and Szaniszlo, P. J. (1987) Pathogenicity and virulence of wild-type and melanin-deficient Wangiella dermatitidis. J. Med. Vet. Mycol. 25, 97-106
65. Silva, M. B., Thomaz, L., Marques, A. F., Svidzinski, A. E., Nosanchuk, J. D., Casadevall, A., Travassos, L. R., and Taborda, C. P. ( 2009) Resistance of melanized yeast cells of Paracoccidioides brasiliensis to antimicrobial oxidants and inhibition of phagocytosis using carbohydrates and monoclonal antibody to CD18. Mem. Inst. Oswaldo Cruz 104, 644-648
66. Morris-Jones, R., Youngchim, S., Gomez, B. L., Aisen, P., Hay, R. J., Nosanchuk, J. D., Casadevall, A., and Hamilton, A. J. (2003) Synthesis of melanin-like pigments by Sporothrix schenckii in vitro and du ring mammalian infection. Infect. Immun. 71, 4026-4033
67. Ngamskulrungroj P. Price J. Sorrell T. Perfect J. R. Meyer W. 2011 Cryptococcus gattii virulence composite: Candidate genes re vealed by microarray analysis of high and less virulent Vancouver island outbreak strains. PLoS One 6 e16076
68. Kwon-Chung, K. J., Polacheck, I., and Popkin, T. J. (1982) Melanin-lacking mutants of Cryptococcus neoformans and their virulence for mice. J. Bacteriol. 150, 1414-1421
69. Wang, Y., Aisen, P., and Casadevall, A. (1995) Cryptococcus neoformans melanin and virulence: Mechanisms of action. Infect. Immun. 63, 3131-3136
70. Nosanchuk, J. D., Valadon, P., Feldmesser, M., and Casadevall, A. (1999) Melanization of Cryptococcus neoformans in murine infection. Mol. Cell Biol. 19, 745-750
71. Nosanchuk, J. D., Rosas, A. L., Lee, S. C., and Casadevall, A. (2000) Melanisation of Cryptococcus neoformans in human brain tissue. Lancet 355, 2049-2050
72. Salas, S. D., Bennett, J. E., Kwon-Chung, K. J., Perfect, J. R., and Williamson, P. R. (1996) Effect of the laccase gene CNLAC1 on virulence of Cryptococcus neoformans. J. Exp. Med. 184, 377-386
73. Waterman, S. R., Hacham, M., Panepinto, J., Hu, G., Shin, S., and Williamson, P. R. (2007) Cell wall targeting of laccase of Cryptococcus neoformans during infection of mice. Infect. Immun. 75, 714-722
74. Upadhyay, S., Torres, G., and Lin, X. (2013) Laccases involved in 1,8-dihydroxynaphthalene melanin biosynthesis in Aspergillus fumigatus are regulated by developmental factors and copper homeostasis. Eukaryot. Cell 12, 1641-1652
75. Pihet, M., Vandeputte, P., Tronchin, G., Renier, G., Saulnier, P., Georgeault, S., Mallet, R., Chabasse, D., Symoens, F., and Bouchara, J. P. (2009) Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol. 9, 177 76.
76. Thywiß en, A., Heinekamp, T., Dahse, H. M., Schmaler-Ripcke, J., Nietzsche, S., Zipfel, P. F., and Brakhage, A. A. (2011) Conidial dihydroxynapththalene melanin of the human pthogenic fungus Asperg illus fumigatus interferes with the host endocytosis pathway. Front. Microbiol. 2, 96
77. Cox, G. M., Harrison, T. S., McDade, H. C., Taborda, C. P., Heinrich, G., Casadevall, A., and Perfect, J. R. (2003) Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Infect. Immun. 71, 173-180
78. Hwang, C. S., Rhie, G. E., Oh, J. H., Huh, W. K., Yim, H. S., and Kang, S. O. (2002) 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 148, 3705-3713
79. Martchenko, M., Alarco, A. M., Harcus, D., and Whiteway, M. (2004) Superoxide dismutases in Candida albicans: Transcriptional regulation and functional characterization of the hyphal-in duced SOD5 gene. Mol. Biol. Cell 15, 456-467
80. Youseff, B. H., Holbrook, E. D., Smolnycki, K. A., and Rappleye, C. A. (2012) Extracellular superoxide dismutase protects Histoplasma yeast from host-derived oxidative stress. PLoS Pathog. 8, e1002713
81. Gleason, J. E., Galaleldeen, A., Peterson, R. L., Taylor, A. B., Holloway, S. P., Waninger-Saroni, J., Cormack, B. P., Cabelli, D. E., Hart, P. J., and Culotta, V. C. (2014) Candida albicans SOD5 represents the prototype of an unprecedented class of Cu-only superoxide dismutases required for pathogen defense. Proc. Natl. Acad. Sci. U.S.A. 111, 5866-5871
82. Boekhout, T., Gué ho-Kellermann, E., Mayser, P., Velegraki, A., eds (2010) Malassezia and the Skin, pp. 6-11, Springer, Heidelberg
83. Reeder, N. L., Kaplan, J., Xu, J., Youngquist, R. S., Wallace, J., Hu, P., Juhlin, K. D., Schwartz, J. R., Grant, R. A., Fieno, A., Nemeth, S., Reichling, T., Tiesman, J. P., Mills, T. , Steinke, M., Wang, S. L., and Saunders, C. W. (2011) Zinc pyrithione inhibits yeast growth through copper influx and inactivation of iron-sulfur proteins. Antimicrob. Agents Chemother. 55, 5753-5760
84. Foster, A. W., Dainty, S. J., Patterson, C. J., Pohl, E., Blackburn, H., Wilson, C., Hess, C. R., Rutherford, J. C., Quaranta, L., Corran, A., and Robinson, N. J. (2014)Achemical potentiator of copper-acc umulation used to investigate the iron-regulons of Saccharomyces cerevisiae. Mol. Microbiol. 93, 317-330
85. Festa, R. A., Helsel, M. E., Franz, K. J., and Thiele, D. J. (2014) Exploiting innate immune cell activation of a copper-dependent antimicrobial agent during infection. Chem. Biol. 21, 977-987
86. Homann, O. R., Dea, J., Noble, S. M., and Johnson, A. D. (2009) A phenotypic profile of the Candida albicans regulatory network. PLoS Genet. 5, e1000783
87. Douglas, L. M., Wang, H. X., Keppler-Ross, S., Dean, N., and Konopka, J. B. (2012) Sur7 promotes plasma membrane organization and is nee ded for resistance to stressful conditions and to the invasive growth and virulence of Candida albicans. MBio 3, e00254-11
88. White T. C. Findley K. Dawson T. L. Jr. Scheynius A. Boekhout T. Cuomo C. A. Xu, J. and Saunders C. W. (2014) Fungi on the skin: Dermatophytes and Malassezia. Cold Spring Harb. Perspect. Med. 4, a019802