Effects of iron chelators on the formation and development of Aspergillus fumigatus biofilm

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 10, 2015, Pages 6514-6520

  Nazik, Hasan ^a,b,e   Penner, John C ^a,f   Ferreira, Jose A ^a,b,g   Haagensen, Janus A J ^c   Cohen, Kevin ^a,h   Spormann, Alfred M ^c   Martinez, Marife ^a   Chen, Vicky ^a   Hsu, Joe L ^a,d   Clemons, Karl V ^a,b   Stevens, David A ^a,b  

^a CALIFORNIA INSTITUTE FOR MEDICAL RESEARCH   (United States)

^b Division of Infectious Diseases and Geographic Medicine   (United States)

^c Department of Civil and Environmental Engineering ^*  (United States)

^d STANFORD UNIVERSITY   (United States)

^e ISTANBUL UNIVERSITY   (Turkey)

^f GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g School of Medicine Faculdade da Saude e Ecologia   (Brazil)

^h WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEFERASIROX; DEFERIPRONE; DEFEROXAMINE; FERRIC CHLORIDE; IRON CHELATING AGENT; 2,3-BIS(2-METHOXY-4-NITRO-5-SULFOPHENYL)-5-((PHENYLAMINO)CARBONYL)-2H-TETRAZOLIUM HYDROXIDE; ANTIFUNGAL AGENT; BENZOIC ACID DERIVATIVE; CHLORIDE; FERRIC ION; IRON; PYRIDONE DERIVATIVE; TETRAZOLIUM; TRIAZOLE DERIVATIVE;

ARTICLE; ASPERGILLUS FUMIGATUS; BIOFILM; BROTH DILUTION; CONIDIUM; CONTROLLED STUDY; FUNGUS GROWTH; FUNGUS ISOLATION; IRON CHELATION; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PLANKTON; PRIORITY JOURNAL; XTT ASSAY; DRUG EFFECTS; FUNGUS SPORE; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIAL SENSITIVITY TEST;

ANTIFUNGAL AGENTS; ASPERGILLUS FUMIGATUS; BENZOATES; BIOFILMS; CHLORIDES; DEFEROXAMINE; FERRIC COMPOUNDS; IRON; IRON CHELATING AGENTS; MICROBIAL SENSITIVITY TESTS; PLANKTON; PYRIDONES; SPORES, FUNGAL; TETRAZOLIUM SALTS; TRIAZOLES;

EID: 84942922632     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.01684-15     Document Type: Article

References (32)

1. Kousha M, Tadi R, Soubani AO. 2011. Pulmonary aspergillosis: a clinical review. Eur Respir Rev 20:156-174. http://dx.doi.org/10.1183/09059180.00001011.
2. Walsh TJ, Anaissie EJ, Denning DW, Herbrecht R, Kontoyiannis DP, Marr KA, Morrison VA, Segal BH, Steinbach WJ, Stevens DA, van Burik JA, Wingard JR, Patterson TF, Infectious Diseases Society of America. 2008. Treatment of aspergillosis: clinical practice guidelines of the Infectious Diseases Society of America. Clin Infect Dis 46:327-360. http://dx.doi.org/10.1086/525258.
3. Amin R, Dupuis A, Aaron SD, Ratjen F. 2010. The effect of chronic infection with Aspergillus fumigatus on lung function and hospitalization in patients with cystic fibrosis. Chest 137:171-176. http://dx.doi.org/10.1378/chest.09-1103.
4. Hsu JL, Ruoss SJ, Bower ND, Lin M, Holodniy M, Stevens DA. 2011. Diagnosing invasive fungal disease in critically ill patients. Crit Rev Microbiol 37:277-312. http://dx.doi.org/10.3109/1040841X.2011.581223.
5. Lin SJ, Schranz J, Teutsch SM. 2001. Aspergillosis case-fatality rate: systematic review of the literature. Clin Infect Dis 32:358-366. http://dx.doi.org/10.1086/318483.
6. Müller FM, Seidler M, Beauvais A. 2011. Aspergillus fumigatus biofilms in the clinical setting. Med Mycol 49(Suppl 1):S96-S100. http://dx.doi.org/10.3109/13693786.2010.502190.
7. Hissen AH, Wan AN, Warwas ML, Pinto LJ, Moore MM. 2005. The Aspergillus fumigatus siderophore biosynthetic gene sidA, encoding L-ornithine N5-oxygenase, is required for virulence. Infect Immun 73:5493-5503. http://dx.doi.org/10.1128/IAI.73.9.5493-5503.2005.
8. Leal SM, Jr, Roy S, Vareechon C, Carrion S, Clark H, Lopez-Berges MS, Di Pietro A, Schrettl M, Beckmann N, Redl B, Haas H, Pearlman E. 2013. Targeting iron acquisition blocks infection with the fungal pathogens Aspergillus fumigatus and Fusarium oxysporum. PLoS Pathog 9:e1003436. http://dx.doi.org/10.1371/journal.ppat.1003436.
9. Zarember KA, Sugui JA, Chang YC, Kwon-Chung KJ, Gallin JI. 2007. Human polymorphonuclear leukocytes inhibit Aspergillus fumigatus conidial growth by lactoferrin-mediated iron depletion. J Immunol 178:6367-6373. http://dx.doi.org/10.4049/jimmunol.178.10.6367.
10. Zarember KA, Cruz AR, Huang CY, Gallin JI. 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. http://dx.doi.org/10.1128/AAC.01547-08.
11. Ibrahim AS, Gebremariam T, Luo G, Fu Y, French SW, Edwards JE, Jr, Spellberg B. 2011. Combination therapy of murine mucormycosis or aspergillosis with iron chelation, polyenes, and echinocandins. Antimicrob Agents Chemother 55:1768-1770. http://dx.doi.org/10.1128/AAC.01577-10.
12. Penner JC, Ferreira JA, Martinez M, Chen V, Hsu JL, Clemons KV, Stevens DA. 2014. Effect of iron (Fe) chelators on the formation and development of Aspergillus fumigatus (AF) biofilm (BF), abstr M-436. Abstr 54th Intersci Conf Antimicrob Agents Chemother, 5 to 9 September 2014, Washington, DC.
13. Denning DW, Clemons KV, Hanson LH, Stevens DA. 1990. Restriction endonuclease analysis of total cellular DNA of Aspergillus fumigatus isolates of geographically and epidemiologically diverse origin. J Infect Dis 162:1151-1158. http://dx.doi.org/10.1093/infdis/162.5.1151.
14. Denning DW, Stevens DA. 1991. Efficacy of cilofungin alone and in combination with amphotericin B in a murine model of disseminated aspergillosis. Antimicrob Agents Chemother 35:1329-1333. http://dx.doi.org/10.1128/AAC.35.7.1329.
15. Sabino R, Ferreira J A G, Moss R, Valente J, Verissimo C, Carolino E, Clemons KV, Everson C, Banaei N, Penner J, Stevens DA. 2015. Molecular epidemiology of Aspergillus from cystic fibrosis patients. J Cyst Fibros 14:474-481. http://dx.doi.org/10.1016/j.jcf.2014.10.005.
16. Denning DW, Clemons KV, Stevens DA. 1992. Quantitative preservation of viability of Aspergillus fumigatus. J Med Vet Mycol 30:485-488. http://dx.doi.org/10.1080/02681219280000661.
17. Clinical and Laboratory Standards Institute. 2008. Reference method for broth dilution antifungal susceptibility testing of filamentous fungi; approved standard, 2nd ed. CLSI document M38-A2. Clinical and Laboratory Standards Institute, Wayne, PA.
18. Ferreira J A G, Penner JC, Moss RB, Haagensen J A J, Clemons KV, Spormann AM, Nazik H, Cohen K, Banaei N, Carolino E, Stevens DA. 2015. Inhibition of Aspergillus fumigatus and its biofilm by Pseudomonas aeruginosa is dependent on the source, phenotype and growth conditions of the bacterium. PLoS One 10:e0134692. http://dx.doi.org/10.1371/journal.pone.0134692.
19. Pierce CG, Uppuluri P, Tristan AR, Wormley FL, Jr, Mowat E, Ramage G, Lopez-Ribot JL. 2008. A simple and reproducible 96 well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat Protoc 3:1494-1500. http://dx.doi.org/10.1038/nprot.2008.141.
20. Meletiadis J, Mouton JW, Meis J F GM, Bouman BA, Donnelly JP, Verweij PE, EUROFUNG Network. 2001. Colorimetric assay for antifungal susceptibility testing of Aspergillus species. J Clin Microbiol 39:3402-3408. http://dx.doi.org/10.1128/JCM.39.9.3402-3408.2001.
21. Moss BJ, Kim Y, Nandakumar MP, Marten MR. 2008. Quantifying metabolic activity of filamentous fungi using a colorimetric XTT assay. Biotechnol Prog 24:780-783. http://dx.doi.org/10.1021/bp070334t.
22. Mowat E, Butcher J, Lang S, Williams C, Ramage G. 2007. Development of a simple model for studying the effects of antifungal agents on multicellular communities of Aspergillus fumigatus. J Med Microbiol 56:1205-1212. http://dx.doi.org/10.1099/jmm.0.47247-0.
23. Seidler MJ, Salvenmoser S, Muller F M C. 2008. Aspergillus fumigatus forms biofilms with reduced antifungal drug susceptibility on bronchial epithelial cells. Antimicrob Agents Chemother 52:4130-4136. http://dx.doi.org/10.1128/AAC.00234-08.
24. Haas H. 2012. Iron-a key nexus in the virulence of Aspergillus fumigatus. Front Microbiol 3:28. http://dx.doi.org/10.3389/fmicb.2012.00028.
25. Hissen AH, Chow JM, Pinto LJ, Moore MM. 2004. Survival of Aspergillus fumigatus in serum involves removal of iron from transferrin: the role of siderophores. Infect Immun 72:1402-1408. http://dx.doi.org/10.1128/IAI.72.3.1402-1408.2004.
26. Schrettl M, Haas H. 2011. Iron homeostasis-Achilles' heel of Aspergillus fumigatus? Curr Opin Microbiol 14:400-405. http://dx.doi.org/10.1016/j.mib.2011.06.002.
27. Boelaert JR, de Locht M, Van Cutsem J, Kerrels V, Cantinieaux B, Verdonck A, Van Landuyt HW, Schneider YJ. 1993. Mucormycosis during deferoxamine therapy is a siderophore-mediated infection. In vitro and in vivo animal studies. J Clin Invest 91:1979-1986. http://dx.doi.org/10.1172/JCI116419.
28. Chamilos G, Lewis RE, Hu J, Xiao L, Zal T, Gilliet M, Halder G, Kontoyiannis DP. 2008. Drosophila melanogaster as a model host to dissect the immunopathogenesis of zygomycosis. Proc Natl Acad Sci U S A 105:9367-9372. http://dx.doi.org/10.1073/pnas.0709578105.
29. Ibrahim AS, Gebremariam T, French SW, Edwards JE, Jr, Spellberg B. 2010. The iron chelator deferasirox enhances liposomal amphotericin B efficacy in treating murine invasive pulmonary aspergillosis. J Antimicrob Chemother 65:289-292. http://dx.doi.org/10.1093/jac/dkp426.
30. Kaur S, Singh S. 2014. Biofilm formation by Aspergillus fumigatus. Med Mycol 52:2-9. http://dx.doi.org/10.3109/13693786.2013.819592.
31. Kwiatkowski JL. 2011. Real-world use of iron chelators. Hematology Am Soc Hematol Educ Program 2011:451-458. http://dx.doi.org/10.1182/asheducation-2011.1.451.
32. Reichhardt C, Ferreira JA, Joubert LM, Clemons KV, Stevens DA, Cegelski L. 10 July 2015. Analysis of the Aspergillus fumigatus biofilm extracellular matrix by solid-state nuclear magnetic resonance spectroscopy. Eukaryot Cell http://dx.doi.org/10.1128/EC.00050-15.