The ZrfC alkaline zinc transporter is required for Aspergillus fumigatus virulence and its growth in the presence of the Zn/Mn-chelating protein calprotectin

Cellular Microbiology

Volumn 16, Issue 4, 2014, Pages 548-564

  Amich, Jorge ^a,c   Vicentefranqueira, Rocío ^a   Mellado, Emilia ^b   Ruiz Carmuega, Ana ^a,b   Leal, Fernando ^a   Calera, José Antonio ^a  

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

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSITY HOSPITAL WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALGRANULIN; UNCLASSIFIED DRUG; ZINC TRANSPORTER; ZRFA PROTEIN; ZRFB PROTEIN; ZRFC PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASPERGILLUS FUMIGATUS; CELL MEMBRANE; CONTROLLED STUDY; FUNGAL VIRULENCE; FUNGUS GROWTH; GERMINATION; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; INFLAMMATION; LUNG PARENCHYMA; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SURVIVAL RATE; TISSUE INJURY;

ASPERGILLUS FUMIGATUS; CARRIER PROTEINS; LEUKOCYTE L1 ANTIGEN COMPLEX; MANGANESE; VIRULENCE; ZINC;

EID: 84896396487     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12238     Document Type: Article

References (50)

1. 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.
2. 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.
3. Askew, D.S. (2008) Aspergillus fumigatus: virulence genes in a street-smart mold. Curr Opin Microbiol 11: 331-337.
4. Balloy, V., Huerre, M., Latge, J.P., and Chignard, M. (2005) Differences in patterns of infection and inflammation for corticosteroid treatment and chemotherapy in experimental invasive pulmonary aspergillosis. Infect Immun 73: 494-503.
5. Banerjee, B., Greenberger, P.A., Fink, J.N., and Kurup, V.P. (1998) Immunological characterization of Asp f 2, a major allergen from Aspergillus fumigatus associated with allergic bronchopulmonary aspergillosis. Infect Immun 66: 5175-5182.
6. Berenguer, J., Allende, M.C., Lee, J.W., Garrett, K., Lyman, C., Ali, N.M., etal. (1995) Pathogenesis of pulmonary aspergillosis. Granulocytopenia versus cyclosporine and methylprednisolone-induced immunosuppression. Am J Respir Crit Care Med 152: 1079-1086.
7. Bianchi, M., Niemiec, M.J., Siler, U., Urban, C.F., and Reichenbach, J. (2011) Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. J Allergy Clin Immunol 127: 1243-1252 e1247.
8. Bignell, E., Negrete-Urtasun, S., Calcagno, A.M., Haynes, K., Arst, H.N., Jr, and Rogers, T. (2005) The Aspergillus pH-responsive transcription factor PacC regulates virulence. Mol Microbiol 55: 1072-1084.
9. Bruns, S., Kniemeyer, O., Hasenberg, M., Aimanianda, V., Nietzsche, S., Thywissen, A., etal. (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.
10. Calera, J.A., and Haas, H. (2009) Cations (Zn, Fe). In Aspergillus fumigatus and Aspergillosis. Latgé, J.P., and Steinbach, W.J. (eds). Washington, DC: ASM press, pp. 107-129.
11. Citiulo, F., Jacobsen, I.D., Miramon, P., Schild, L., Brunke, S., Zipfel, P., etal. (2012) Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathog 8: e1002777.
12. Corbin, B.D., Seeley, E.H., Raab, A., Feldmann, J., Miller, M.R., Torres, V.J., etal. (2008) Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319: 962-965.
13. Dagenais, T.R., and Keller, N.P. (2009) Pathogenesis of Aspergillus fumigatus in Invasive Aspergillosis. Clin Microbiol Rev 22: 447-465.
14. Foote, J.W., and Delves, H.T. (1984) Albumin bound and alpha 2-macroglobulin bound zinc concentrations in the sera of healthy adults. J Clin Pathol 37: 1050-1054.
15. Foote, J.W., and Delves, H.T. (1988) Determination of non-protein-bound zinc in human serum using ultrafiltration and atomic absorption spectrometry with electrothermal atomisation. Analyst 113: 911-915.
16. Fuchs, T.A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., etal. (2007) Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 176: 231-241.
17. Gaither, L.A., and Eide, D.J. (2001) Eukaryotic zinc transporters and their regulation. Biometals 14: 251-270.
18. Hayden, J.A., Brophy, M.B., Cunden, L.S., and Nolan, E.M. (2013) High-affinity manganese coordination by human calprotectin is calcium-dependent and requires the histidine-rich site formed at the dimer interface. J Am Chem Soc 135: 775-787.
19. Himeno, S., Yanagiya, T., and Fujishiro, H. (2009) The role of zinc transporters in cadmium and manganese transport in mammalian cells. Biochimie 91: 1218-1222.
20. Hsu, S.M., Raine, L., and Fanger, H. (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29: 577-580.
21. Huppert, M., Oliver, D.J., and Sun, S.H. (1978) Combined methenamine-silver nitrate and hematoxylin & eosin stain for fungi in tissues. J Clin Microbiol 8: 598-603.
22. 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.
23. Jakubovics, N.S., Smith, A.W., and Jenkinson, H.F. (2002) Oxidative stress tolerance is manganese (Mn(2+)) regulated in Streptococcus gordonii. Microbiology 148: 3255-3263.
24. Kehl-Fie, T.E., Chitayat, S., Hood, M.I., Damo, S., Restrepo, N., Garcia, C., etal. (2011) Nutrient metal sequestration by calprotectin inhibits bacterial superoxide defense, enhancing neutrophil killing of Staphylococcus aureus. Cell Host Microbe 10: 158-164.
25. Korndörfer, I.P., Brueckner, F., and Skerra, A. (2007) The crystal structure of the human (S100A8/S100A9)2 heterotetramer, calprotectin, illustrates how conformational changes of interacting alpha-helices can determine specific association of two EF-hand proteins. J Mol Biol 370: 887-898.
26. Kousha, M., Tadi, R., and Soubani, A.O. (2011) Pulmonary aspergillosis: a clinical review. Eur Respir Rev 20: 156-174.
27. Kwon-Chung, K.J., and Sugui, J.A. (2009) What do we know about the role of gliotoxin in the pathobiology of Aspergillus fumigatus? Med Mycol 47 (Suppl. 1): S97-S103.
28. Lech, T., and Sadlik, J.K. (2011) Zinc in postmortem body tissues and fluids. Biol Trace Elem Res 142: 11-17.
29. Liu, J.Z., Jellbauer, S., Poe, A.J., Ton, V., Pesciaroli, M., Kehl-Fie, T.E., etal. (2012) Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 11: 227-239.
30. McCormick, A., Heesemann, L., Wagener, J., Marcos, V., Hartl, D., Loeffler, J., etal. (2010) NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microbes Infect 12: 928-936.
31. Miyasaki, K.T., Bodeau, A.L., Murthy, A.R., and Lehrer, R.I. (1993) In vitro antimicrobial activity of the human neutrophil cytosolic S-100 protein complex, calprotectin, against Capnocytophaga sputigena. J Dent Res 72: 517-523.
32. Moreno, M.A., Ibrahim-Granet, O., Vicentefranqueira, R., Amich, J., Ave, P., Leal, F., etal. (2007) The regulation of zinc homeostasis by the ZafA transcriptional activator is essential for Aspergillus fumigatus virulence. Mol Microbiol 64: 1182-1197.
33. Sambrook, J., and Russell, D.W. (2001) Molecular Cloning. A laboratory manual. Cold Spring, NY: Cold Spring Harbor Laboratory Press.
34. Sandrin, T.R., and Maier, R.M. (2003) Impact of metals on the biodegradation of organic pollutants. Environ Health Perspect 111: 1093-1101.
35. Segurado, M., López-Aragon, R., Calera, J.A., Fernández-Abalos, J.M., and Leal, F. (1999) Zinc-regulated biosynthesis of immunodominant antigens from Aspergillus spp. Infect Immun 67: 2377-2382.
36. Sheppard, D.C., Marr, K.A., Fredricks, D.N., Chiang, L.Y., Doedt, T., and Filler, S.G. (2006) Comparison of three methodologies for the determination of pulmonary fungal burden in experimental murine aspergillosis. Clin Microbiol Infect 12: 376-380.
37. Smith, J.M., Davies, J.E., and Holden, D.W. (1993) Construction and pathogenicity of Aspergillus fumigatus mutants that do not produce the ribotoxin restrictocin. Mol Microbiol 9: 1071-1077.
38. Sohnle, P.G., Hahn, B.L., and Santhanagopalan, V. (1996) Inhibition of Candida albicans growth by calprotectin in the absence of direct contact with the organisms. J Infect Dis 174: 1369-1372.
39. Sohnle, P.G., Hunter, M.J., Hahn, B., and Chazin, W.J. (2000) Zinc-reversible antimicrobial activity of recombinant calprotectin (migration inhibitory factor-related proteins 8 and 14). J Infect Dis 182: 1272-1275.
40. Spikes, S., Xu, R., Nguyen, C.K., Chamilos, G., Kontoyiannis, D.P., Jacobson, R.H., etal. (2008) Gliotoxin production in Aspergillus fumigatus contributes to host-specific differences in virulence. J Infect Dis 197: 479-486.
41. Steinbakk, M., Naess-Andresen, C.F., Lingaas, E., Dale, I., Brandtzaeg, P., and Fagerhol, M.K. (1990) Antimicrobial actions of calcium binding leucocyte L1 protein, calprotectin. Lancet 336: 763-765.
42. Stephens-Romero, S.D., Mednick, A.J., and Feldmesser, M. (2005) The pathogenesis of fatal outcome in murine pulmonary aspergillosis depends on the neutrophil depletion strategy. Infect Immun 73: 114-125.
43. Striz, I., and Trebichavsky, I. (2004) Calprotectin - a pleiotropic molecule in acute and chronic inflammation. Physiol Res 53: 245-253.
44. Taylor, K.M., and Nicholson, R.I. (2003) The LZT proteins; the LIV-1 subfamily of zinc transporters. Biochim Biophys Acta 1611: 16-30.
45. Tekaia, F., and Latge, J.P. (2005) Aspergillus fumigatus: saprophyte or pathogen? Curr Opin Microbiol 8: 385-392.
46. Urban, C.F., Ermert, D., Schmid, M., Abu-Abed, U., Goosmann, C., Nacken, W., etal. (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 5: e1000639.
47. 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.
48. Vogl, T., Leukert, N., Barczyk, K., Strupat, K., and Roth, J. (2006) Biophysical characterization of S100A8 and S100A9 in the absence and presence of bivalent cations. Biochim Biophys Acta 1763: 1298-1306.
49. Weidner, G., d'Enfert, C., Koch, A., Mol, P.C., and Brakhage, A.A. (1998) Development of a homologous transformation system for the human pathogenic fungus Aspergillus fumigatus based on the pyrG gene encoding orotidine 5'-monophosphate decarboxylase. Curr Genet 33: 378-385.
50. Yokus, B., and Cakir, U.D. (2006) Seasonal and physiological variations in serum chemistry and mineral concentrations in cattle. Biol Trace Elem Res 109: 255-266.