Extrinsic extracellular DNA leads to biofilm formation and colocalizes with matrix polysaccharides in the human pathogenic fungus Aspergillus fumigatus

Frontiers in Microbiology

Volumn 4, Issue JUN, 2013, Pages

  Shopova, Iordana ^a,b   Bruns, Sandra ^a,b   Thywissen, Andreas ^a,b   Kniemeyer, Olaf ^a,b,c   Brakhage, Axel A ^a,b   Hillmann, Falk ^a,b  

^a HANS KNÖLL INSTITUTE   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^c JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

Aspergillus; Cystic fibrosis; Extracellular DNA; Extracellular matrix; Fungal biofilm

Indexed keywords

DNA; EXTRACELLULAR DNA; POLYSACCHARIDE; UNCLASSIFIED DRUG;

AGAR GEL ELECTROPHORESIS; ANTIFUNGAL SUSCEPTIBILITY; ARTICLE; ASPERGILLUS FUMIGATUS; BIOFILM; BIOMASS PRODUCTION; COLONY FORMING UNIT; CONFOCAL LASER MICROSCOPY; CONIDIUM; CONTROLLED STUDY; CYSTIC FIBROSIS; DNA ISOLATION; ENVIRONMENTAL FACTOR; ENZYMATIC DEGRADATION; EXTRACELLULAR MATRIX; FETAL CALF SERUM; FLUORESCENCE MICROSCOPY; FUNGAL VIABILITY; FUNGUS HYPHAE; MICROSCOPY; NONHUMAN; RESAZURIN ASSAY;

ASPERGILLUS; ASPERGILLUS FUMIGATUS; FUNGI;

EID: 84884260563     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2013.00141     Document Type: Article

References (44)

1. Al-Fattani, M. A., and Douglas, L. J. (2006). Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J. Med. Microbiol. 55, 999-1008. doi:10.1099/jmm.0.46569-0
2. Allesen-Holm, M., Barken, K. B., Yang, L., Klausen, M., Webb, J. S., Kjelleberg, S., et al. (2006). A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol. Microbiol. 59, 1114-1128. doi:10.1111/j.1365-2958.2005.05008.x
3. Beauvais, A., Schmidt, C., Guadagnini, S., Roux, P., Perret, E., Henry, C., et al. (2007). An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus. Cell. Microbiol. 9, 1588-1600. doi:10.1111/j.1462-5822.2007.00895.x
4. Brakhage, A. A. (2005). Systemic fungal infections caused by Aspergillus species: epidemiology, infection process and virulence determinants. Curr. Drug Targets 6, 875-886. doi:10.2174/138945005774912717
5. Brandt, T., Breitenstein, S., von der Hardt, H., and Tümmler, B. (1995). DNA concentration and length in sputum of patients with cystic fibrosis during inhalation with recombinant human DNase. Thorax 50, 880-882.
6. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., et al. (2004). Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535. doi:10.1126/science.1092385
7. Bruns, S., Kniemeyer, O., Hasenberg, M., Aimanianda, V., Nietzsche, S., Thywissen, A., et al. (2010a). 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
8. Bruns, S., Seidler, M., Albrecht, D., Salvenmoser, S., Remme, N., Hertweck, C., et al. (2010b). Functional genomic profiling of Aspergillus fumigatus biofilm reveals enhanced production of the mycotoxin gliotoxin. Proteomics 10, 3097-3107. doi:10.1002/pmic.201000129
9. Cantin, A. M. (1998). DNase I acutely increases cystic fibrosis sputum elastase activity and its potential to induce lung hemorrhage in mice. Am. J. Respir. Crit. Care Med. 157, 464-469. doi:10.1164/ajrccm.157.2.9608033
10. Chandra, J., Mukherjee, P. K., and Ghannoum, M. A. (2008). In vitro growth and analysis of Candida biofilms. Nat. Protoc. 3, 1909-1924. doi:10.1038/nprot.2008.192
11. d'Enfert, C. (1996). Selection of multiple disruption events in Aspergillus fumigatus using the orotidine-5'-decarboxylase gene, pyrG, as a unique transformation marker. Curr. Genet. 30, 76-82.
12. Da Silva Ferreira, M. E., Kress, M. R., Savoldi, M., Goldman, M. H., Hartl, A., Heinekamp, T., et al. (2006). The akuB(KU80) mutant deficient for nonhomologous end joining is a powerful tool for analyzing pathogenicity in Aspergillus fumigatus. Eukaryot. Cell. 5, 207-211. doi:10.1128/EC.5.1.207-211.2006
13. Flemming, H. C., and Wingender, J. (2010). The biofilm matrix. Nat. Rev. Microbiol. 8, 623-633. doi:10.1038/nrmicro2415
14. Fontaine, T., Beauvais, A., Loussert, C., Thevenard, B., Fulgsang, C. C., Ohno, N., et al. (2010). Cell wall alpha1-3glucans induce the aggregation of germinating conidia of Aspergillus fumigatus. Fungal Genet. Biol. 47, 707-712. doi:10.1016/j.fgb.2010.04.006
15. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., et al. (2007). Novel cell death program leads to neutrophil extracellular traps. J. Cell. Biol. 176, 231-241. doi:10.1083/jcb.200606027
16. Gibbons, J. G., Beauvais, A., Beau, R., McGary, K. L., Latgé, J. P., and Rokas, A. (2012). Global transcriptome changes underlying colony growth in the opportunistic human pathogen Aspergillus fumigatus. Eukaryot. Cell. 11, 68-78. doi:10.1128/EC.05102-11
17. Jöchl, C., Loh, E., Ploner, A., Haas, H., and Hüttenhofer, A. (2009). Development-dependent scavenging of nucleic acids in the filamentous fungus Aspergillus fumigatus. RNA Biol. 6, 179-186.
18. Latgé, J. P. (2001). The pathobiology of Aspergillus fumigatus. Trends Microbiol. 9, 382-389. doi:10.1016/S0966-842X(01)02104-7
19. Lethem, M. I., James, S. L., Marriott, C., and Burke, J. F. (1990). The origin of DNA associated with mucus glycoproteins in cystic fibrosis sputum. Eur. Respir. J. 3, 19-23.
20. Loussert, C., Schmitt, C., Prevost, M. C., Balloy, V., Fadel, E., Philippe, B., et al. (2010). In vivo biofilm composition of Aspergillus fumigatus. Cell Microbiol. 12, 405-410. doi:10.1111/j.1462-5822.2009.01409.x
21. Mariscal, A., Lopez-Gigosos, R. M., Carnero-Varo, M., and Fernandez-Crehuet, J. (2009). Fluorescent assay based on resazurin for detection of activity of disinfectants against bacterial biofilm. Appl. Microbiol. Biotechnol. 82, 773-783. doi:10.1007/s00253-009-1879-x
22. Martins, M., Henriques, M., Lopez-Ribot, J. L., and Oliveira, R. (2012). Addition of DNase improves the in vitro activity of antifungal drugs against Candida albicans biofilms. Mycoses 55, 80-85. doi:10.1111/j.1439-0507.2011.02047.x
23. Martins, M., Uppuluri, P., Thomas, D. P., Cleary, I. A., Henriques, M., Lopez-Ribot, J. L., et al. (2010). Presence of extracellular DNA in the Candida albicans biofilm matrix and its contribution to biofilms. Mycopathologia 169, 323-331. doi:10.1007/s11046-009-9264-y
24. Mowat, E., Butcher, J., Lang, S., Williams, C., and 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. doi:10.1099/jmm.0.47247-0
25. Mowat, E., Williams, C., Jones, B., McChlery, S., and Ramage, G. (2009). The characteristics of Aspergillus fumigatus mycetoma development: is this a biofilm? Med. Mycol. 47(Suppl. 1), S120-S126. doi:10.1080/13693780802238834
26. Mulcahy, H., Charron-Mazenod, L., and Lewenza, S. (2008). Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4:e1000213. doi:10.1371/journal.ppat.1000213
27. Muszkieta, L., Beauvais, A., Pahtz, V., Gibbons, J. G., Anton Leberre, V., Beau, R., et al. (2013). Investigation of Aspergillus fumigatus biofilm formation by various "omics" approaches. Front. Microbiol. 4:13. doi:10.3389/fmicb.2013.00013
28. Nivoix, Y., Velten, M., Letscher-Bru, V., Moghaddam, A., Natarajan-Ame, S., Fohrer, C., et al. (2008). Factors associated with overall and attributable mortality in invasive aspergillosis. Clin. Infect. Dis. 47, 1176-1184. doi:10.1086/592255
29. Papayannopoulos, V., Staab, D., and Zychlinsky, A. (2011). Neutrophil elastase enhances sputum solubilization in cystic fibrosis patients receiving DNase therapy. PLoS ONE 6:e28526. doi:10.1371/journal.pone.0028526
30. Pierce, C. G., Uppuluri, P., Tristan, A. R., Wormley, F. L. Jr., Mowat, E., Ramage, G., et al. (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. doi:10.1038/nport.2008.141
31. Pihet, M., Carrere, J., Cimon, B., Chabasse, D., Delhaes, L., Symoens, F., et al. (2009). Occurrence and relevance of filamentous fungi in respiratory secretions of patients with cystic fibrosis-a review. Med. Mycol. 47, 387-397. doi:10.1080/13693780802609604
32. Rajendran, R., Williams, C., Lappin, D. F., Millington, O., Martins, M., and Ramage, G. (2013). Extracellular DNA release acts as an antifungal resistance mechanism in mature Aspergillus fumigatus biofilms. Eukaryot. Cell. 12, 420-429. doi:10.1128/EC.00287-12
33. Ramage, G., Mowat, E., Jones, B., Williams, C., and Lopez-Ribot, J. (2009). Our current understanding of fungal biofilms. Crit. Rev. Microbiol. 35, 340-355. doi:10.3109/10408410903241436
34. Sambrook, J., and Russell, D. W. (2001) Molecular cloning: A Laboratory Manual, 3rd Edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
35. Scharf, D. H., Heinekamp, T., Remme, N., Hortschansky, P., Brakhage, A. A., and Hertweck, C. (2012). Biosynthesis and function of gliotoxin in Aspergillus fumigatus. Appl. Microbiol. Biotechnol. 93, 467-472. doi:10.1007/s00253-011-3689-1
36. Seidler, M. J., Salvenmoser, S., and Muller, F. M. (2008). Aspergillus fumigatus forms biofilms with reduced antifungal drug susceptibility on bronchial epithelial cells. Antimicrob. Agents Chemother. 52, 4130-4136. doi:10.1128/AAC.00234-08
37. Shak, S., Capon, D. J., Hellmiss, R., Marsters, S. A., and Baker, C. L. (1990). Recombinant human DNase I reduces the viscosity of cystic fibrosis sputum. Proc. Natl. Acad. Sci. U.S.A. 87, 9188-9192. doi:10.1073/pnas.87.23.9188
38. Spikes, S., Xu, R., Nguyen, C. K., Chamilos, G., Kontoyiannis, D. P., Jacobson, R. H., et al. (2008). Gliotoxin production in Aspergillus fumigatus contributes to host-specific differences in virulence. J. Infect. Dis. 197, 479-486. doi:10.1086/525044
39. Tekaia, F., and Latgé, J. P. (2005). Aspergillus fumigatus: saprophyte or pathogen? Curr. Opin. Microbiol. 8, 385-392. doi:10.1016/j.mib.2005.06.017
40. Toyotome, T., Yamaguchi, M., Iwasaki, A., Watanabe, A., Taguchi, H., Qin, L., et al. (2012). Fetuin A, a serum component, promotes growth and biofilm formation by Aspergillus fumigatus. Int. J. Med. Microbiol. 302, 108-116. doi:10.1016/j.ijmm.2011.12.001
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. 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.
43. Whitchurch, C. B., Tolker-Nielsen, T., Ragas, P. C., and Mattick, J. S. (2002). Extracellular DNA required for bacterial biofilm formation. Science 295, 1487. doi:10.1126/science.295.5559.1487
44. Yang, Y., Sreenivasan, P. K., Subramanyam, R., and Cummins, D. (2006). Multiparameter assessments to determine the effects of sugars and antimicrobials on a polymicrobial oral biofilm. Appl. Environ. Microbiol. 72, 6734-6742. doi:10.1128/AEM.01013-06