Targeting zinc homeostasis to combat Aspergillus fumigatus infections

Frontiers in Microbiology

Volumn 6, Issue FEB, 2015, Pages

  Vicentefranqueira, Rocío ^a,b   Amich, Jorge ^a,b,d   Laskaris, Paris ^c   Ibrahim Granet, Oumaima ^c   Latgé, Jean P ^c   Toledo, Héctor ^a,b   Leal, Fernando ^a,b   Calera, José A ^a,b  

^a Instituto de Biología Funcional y Genómica and Departamento de Microbiología y Genética   (Spain)

^b UNIVERSITY OF SALAMANCA   (Spain)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

Aspergillus fumigatus; Drug discovery; Fungal pathogenesis; Transcription factors; Zinc homeostasis; Zinc transporters

Indexed keywords

ANTIFUNGAL AGENT; CALGRANULIN; HEAT SHOCK TRANSCRIPTION FACTOR 1; TRANSCRIPTION FACTOR ZAFA; TRANSCRIPTION FACTOR ZRFB; TRANSCRIPTION FACTOR ZRFC; UNCLASSIFIED DRUG; ZINC TRANSPORTER;

ARTICLE; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; FILAMENTOUS FUNGUS; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS GROWTH; GENE EXPRESSION; GROWTH INHIBITION; HISTOLOGY; HOMEOSTASIS AND REGULATION; HUMAN; IMMUNOCYTOCHEMISTRY; MYCELIAL GROWTH; NONHUMAN; PHAGOCYTE; TRANSCRIPTION REGULATION; ZINC HOMEOSTASIS;

ANIMALIA; ASPERGILLUS; ASPERGILLUS FUMIGATUS;

EID: 84927551636     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00160     Document Type: Article

References (45)

1. Alloway, B. J. (2008). Zinc in Soils and Crop Nutrition. Brussels and Paris: International Zinc Association and the International Fertilizer Industry Association.
2. Amich, J., and Calera, J. A. (2014). Zinc acquisition: a key aspect in Aspergillus fumigatus virulence. Mycopathologia 178, 379-385. doi: 10.1007/s11046-014-9764-2.
3. Amich, J., Leal, F., and Calera, J. A. (2009). Repression of the acid ZrfA/ZrfB zinc-uptake system of Aspergillus fumigatus mediated by PacC under neutral, zinc-limiting conditions. Int. Microbiol. 12, 39-47. doi: 10.2436/20.1501.01.80.
4. Amich, J., Vicentefranqueira, R., Leal, F., and Calera, J. A. (2010). 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 9, 424-437. doi: 10.1128/EC.00348-09.
5. Amich, J., Vicentefranqueira, R., Mellado, E., Ruiz-Carmuega, A., Leal, F., and Calera, J. A. (2014). 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. 16, 548-564. doi: 10.1111/cmi.12238.
6. Andreini, C., Bertini, I., Cavallaro, G., Holliday, G. L., and Thornton, J. M. (2008). Metal ions in biological catalysis: from enzyme databases to general principles. J. Biol. Inorg. Chem. 13, 1205-1218. doi: 10.1007/s00775-008-0404-5.
7. Botella, H., Peyron, P., Levillain, F., Poincloux, R., Poquet, Y., Brandli, I., et al. (2011). Mycobacterial p1-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 10, 248-259. doi: 10.1016/j.chom.2011.08.006.
8. Bruns, S., Kniemeyer, O., Hasenberg, M., Aimanianda, V., Nietzsche, S., Thywissen, A., et al. (2010). Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog. 6:e1000873. doi: 10.1371/journal.ppat.1000873.
9. Corbin, B. D., Seeley, E. H., Raab, A., Feldmann, J., Miller, M. R., Torres, V. J., et al. (2008). Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319, 962-965. doi: 10.1126/science.1152449.
10. Cottarel, G., and Wierzbowski, J. (2007). Combination drugs, an emerging option for antibacterial therapy. Trends Biotechnol. 25, 547-555. doi: 10.1016/j.tibtech.2007.09.004.
11. Cousins, R. J., Liuzzi, J. P., and Lichten, L. A. (2006). Mammalian zinc transport, trafficking, and signals. J. Biol. Chem. 281, 24085-24089. doi: 10.1074/jbc.R600011200.
12. Eide, D. J. (2011). The oxidative stress of zinc deficiency. Metallomics 3, 1124-1129. doi: 10.1039/c1mt00064k.
13. Fatfat, M., Merhi, R. A., Rahal, O., Stoyanovsky, D. A., Zaki, A., Haidar, H., et al. (2014). Copper chelation selectively kills colon cancer cells through redox cycling and generation of reactive oxygen species. BMC Cancer 14:527. doi: 10.1186/1471-2407-14-527.
14. Gunther, V., Lindert, U., and Schaffner, W. (2012). The taste of heavy metals: gene regulation by MTF-1. Biochim. Biophys. Acta 1823, 1416-1425. doi: 10.1016/j.bbamcr.2012.01.005.
15. Hachem, R., Bahna, P., Hanna, H., Stephens, L. C., and Raad, I. (2006). EDTA as an adjunct antifungal agent for invasive pulmonary aspergillosis in a rodent model. Antimicrob. Agents Chemother. 50, 1823-1827. doi: 10.1128/AAC.50.5.1823-1827.2006.
16. Hashemi, M., Ghavami, S., Eshraghi, M., Booy, E. P., and Los, M. (2007). Cytotoxic effects of intra and extracellular zinc chelation on human breast cancer cells. Eur. J. Pharmacol. 557, 9-19. doi: 10.1016/j.ejphar.2006.11.010.
17. Hood, M. I., and Skaar, E. P. (2012). Nutritional immunity: transition metals at the pathogen-host interface. Nat. Rev. Microbiol. 10, 525-537. doi: 10.1038/nrmicro2836.
18. Huesca, M., Lock, L. S., Khine, A. A., Viau, S., Peralta, R., Cukier, I. H., et al. (2009). A novel small molecule with potent anticancer activity inhibits cell growth by modulating intracellular labile zinc homeostasis. Mol. Cancer Ther. 8, 2586-2596. doi: 10.1158/1535-7163.MCT-08-1104.
19. Ibrahim, A. S., Gebremariam, T., French, S. W., Edwards, J. E. Jr., and Spellberg, B. (2010). The iron chelator deferasirox enhances liposomal amphotericin B efficacy in treating murine invasive pulmonary aspergillosis. J. Antimicrob. Chemother. 65, 289-292. doi: 10.1093/jac/dkp426.
20. Iyengar, V., and Woittiez, J. (1988). Trace elements in human clinical specimens: evaluation of literature data to identify reference values. Clin. Chem. 34, 474-481.
21. Kontoghiorghes, G. J., Kolnagou, A., Peng, C. T., Shah, S. V., and Aessopos, A. (2010). Safety issues of iron chelation therapy in patients with normal range iron stores including thalassaemia, neurodegenerative, renal and infectious diseases. Expert Opin. Drug Saf. 9, 201-206. doi: 10.1517/14740330903535845.
22. Kousha, M., Tadi, R., and Soubani, A. O. (2011). Pulmonary aspergillosis: a clinical review. Eur. Respir. Rev. 20, 156-174. doi: 10.1183/09059180.00001011.
23. Leal, S. M. Jr., Roy, S., Vareechon, C., Carrion, S., Clark, H., Lopez-Berges, M. S., et al. (2013). Targeting iron acquisition blocks infection with the fungal pathogens Aspergillus fumigatus and Fusarium oxysporum. PLoS Pathog. 9:e1003436. doi: 10.1371/journal.ppat.1003436.
24. Lui, G. Y., Obeidy, P., Ford, S. J., Tselepis, C., Sharp, D. M., Jansson, P. J., et al. (2012). The iron chelator, deferasirox, as a novel strategy for cancer treatment: oral activity against human lung tumor xenografts and molecular mechanism of action. Mol. Pharmacol. 83, 179-190. doi: 10.1124/mol.112.081893.
25. McCormick, A., Heesemann, L., Wagener, J., Marcos, V., Hartl, D., Loeffler, J., et al. (2010). NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microbes Infect. 12, 928-936. doi: 10.1016/j.micinf.2010.06.009.
26. Moreno, M. A., Ibrahim-Granet, O., Vicentefranqueira, R., Amich, J., Ave, P., Leal, F., et al. (2007). The regulation of zinc homeostasis by the ZafA transcriptional activator is essential for Aspergillus fumigatus virulence. Mol. Microbiol. 64, 1182-1197. doi: 10.1111/j.1365-2958.2007.05726.x.
27. Nissen, S. E. (2013). Concerns about reliability in the trial to assess chelation therapy (TACT). JAMA 309, 1293-1294. doi: 10.1001/jama.2013.2778.
28. Nobile, C. J., Nett, J. E., Hernday, A. D., Homann, O. R., Deneault, J. S., Nantel, A., et al. (2009). Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol. 7:e1000133. doi: 10.1371/journal.pbio.1000133.
29. Outten, C. E., and O'Halloran, T. V. (2001). Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292, 2488-2492. doi: 10.1126/science.1060331.
30. Parente, A. F., de Rezende, T. C., de Castro, K. P., Bailao, A. M., Parente, J. A., Borges, C. L., et al. (2013). A proteomic view of the response of Paracoccidioides yeast cells to zinc deprivation. Fungal Biol. 117, 399-410. doi: 10.1016/j.funbio.2013.04.004.
31. Prati, F., Goldman-Pinkovich, A., Lizzi, F., Belluti, F., Koren, R., Zilberstein, D., et al. (2014). Quinone-amino acid conjugates targeting Leishmania amino acid transporters. PLoS ONE 9:e107994. doi: 10.1371/journal.pone.0107994.
32. Ramirez-Ortiz, Z. G., Lee, C. K., Wang, J. P., Boon, L., Specht, C. A., and Levitz, S. M. (2011). A nonredundant role for plasmacytoid dendritic cells in host defense against the human fungal pathogen Aspergillus fumigatus. Cell Host Microbe 9, 415-424. doi: 10.1016/j.chom.2011.04.007.
33. Rybniker, J., Chen, J. M., Sala, C., Hartkoorn, R. C., Vocat, A., Benjak, A., et al. (2014). Anticytolytic screen identifies inhibitors of mycobacterial virulence protein secretion. Cell Host Microbe 16, 538-548. doi: 10.1016/j.chom.2014.09.008.
34. Santos, A. L., Sodre, C. L., Valle, R. S., Silva, B. A., Abi-Chacra, E. A., Silva, L. V., et al. (2012). Antimicrobial action of chelating agents: repercussions on the microorganism development, virulence and pathogenesis. Curr. Med. Chem. 19, 2715-2737. doi: 10.2174/092986712800609788.
35. Schneider, R. O., Fogaca, N., S., Kmetzsch, L., Schrank, A., Vainstein, M. H., and Staats, C. C. (2012). Zap1 regulates zinc homeostasis and modulates virulence in Cryptococcus gattii. PLoS ONE 7:e43773. doi: 10.1371/journal.pone.0043773.
36. Slavic, K., Krishna, S., Derbyshire, E. T., and Staines, H. M. (2011). Plasmodial sugar transporters as anti-malarial drug targets and comparisons with other protozoa. Malar. J. 10, 165. doi: 10.1186/1475-2875-10-165.
37. Song, Y., Leonard, S. W., Traber, M. G., and Ho, E. (2009). Zinc deficiency affects DNA damage, oxidative stress, antioxidant defenses, and DNA repair in rats. J. Nutr. 139, 1626-1631. doi: 10.3945/jn.109.106369.
38. Subramanian Vignesh, K., Landero Figueroa, J. A., Porollo, A., Caruso, J. A., and Deepe, G. S. Jr. (2013). Granulocyte macrophage-colony stimulating factor induced Zn sequestration enhances macrophage superoxide and limits intracellular pathogen survival. Immunity 39, 697-710. doi: 10.1016/j.immuni.2013.09.006.
39. Tekaia, F., and Latge, J. P. (2005). Aspergillus fumigatus: saprophyte or pathogen? Curr. Opin. Microbiol. 8, 385-392. doi: 10.1016/j.mib.2005.06.017.
40. Torti, S. V., Torti, F. M., Whitman, S. P., Brechbiel, M. W., Park, G., and Planalp, R. P. (1998). Tumor cell cytotoxicity of a novel metal chelator. Blood 92, 1384-1389.
41. Urban, C. F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W., et al. (2009). Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog. 5:e1000639. doi: 10.1371/journal.ppat.1000639.
42. Vicentefranqueira, R., Moreno, M. A., Leal, F., and Calera, J. A. (2005). 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 4, 837-848. doi: 10.1128/EC.4.5.837-848.2005.
43. Westerheide, S. D., Kawahara, T. L., Orton, K., and Morimoto, R. I. (2006). Triptolide, an inhibitor of the human heat shock response that enhances stress-induced cell death. J. Biol. Chem. 281, 9616-9622. doi: 10.1074/jbc.M512044200.
44. Zarember, K. A., Cruz, A. R., Huang, C. Y., and Gallin, J. I. (2009). Antifungal activities of natural and synthetic iron chelators alone and in combination with azole and polyene antibiotics against Aspergillus fumigatus. Antimicrob. Agents Chemother. 53, 2654-2656. doi: 10.1128/AAC.01547-08.
45. Zuo, J., Schmitt, S. M., Zhang, Z., Prakash, J., Fan, Y., Bi, C., et al. (2012). Novel polypyridyl chelators deplete cellular zinc and destabilize the X-linked inhibitor of apoptosis protein (XIAP) prior to induction of apoptosis in human prostate and breast cancer cells. J. Cell Biochem. 113, 2567-2575. doi: 10.1002/jcb.24132.