Skip to main content
Top
Published in: Seminars in Immunopathology 2/2015

Open Access 01-03-2015 | Review

Interference of Aspergillus fumigatus with the immune response

Authors: Thorsten Heinekamp, Hella Schmidt, Katrin Lapp, Vera Pähtz, Iordana Shopova, Nora Köster-Eiserfunke, Thomas Krüger, Olaf Kniemeyer, Axel A. Brakhage

Published in: Seminars in Immunopathology | Issue 2/2015

Login to get access

Abstract

Aspergillus fumigatus is a saprotrophic filamentous fungus and also the most prevalent airborne fungal pathogen of humans. Depending on the host’s immune status, the variety of diseases caused by A. fumigatus ranges from allergies in immunocompetent hosts to life-threatening invasive infections in patients with impaired immunity. In contrast to the majority of other Aspergillus species, which are in most cases nonpathogenic, A. fumigatus features an armory of virulence determinants to establish an infection. For example, A. fumigatus is able to evade the human complement system by binding or degrading complement regulators. Furthermore, the fungus interferes with lung epithelial cells, alveolar macrophages, and neutrophil granulocytes to prevent killing by these immune cells. This chapter summarizes the different strategies of A. fumigatus to manipulate the immune response. We also discuss the potential impact of recent advances in immunoproteomics to improve diagnosis and therapy of an A. fumigatus infection.
Literature
1.
go back to reference Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, White TC (2012) Hidden killers: human fungal infections. Sci Transl Med 4(165):3004404 Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, White TC (2012) Hidden killers: human fungal infections. Sci Transl Med 4(165):3004404
2.
go back to reference Brakhage AA (2005) Systemic fungal infections caused by Aspergillus species: epidemiology, infection process and virulence determinants. Curr Drug Targets 6(8):875–886PubMed Brakhage AA (2005) Systemic fungal infections caused by Aspergillus species: epidemiology, infection process and virulence determinants. Curr Drug Targets 6(8):875–886PubMed
3.
go back to reference Brakhage AA, Langfelder K (2002) Menacing mold: the molecular biology of Aspergillus fumigatus. Annu Rev Microbiol 56:433–455PubMed Brakhage AA, Langfelder K (2002) Menacing mold: the molecular biology of Aspergillus fumigatus. Annu Rev Microbiol 56:433–455PubMed
4.
go back to reference Wasylnka JA, Moore MM (2003) Aspergillus fumigatus conidia survive and germinate in acidic organelles of A549 epithelial cells. J Cell Sci 116(Pt 8):1579–1587PubMed Wasylnka JA, Moore MM (2003) Aspergillus fumigatus conidia survive and germinate in acidic organelles of A549 epithelial cells. J Cell Sci 116(Pt 8):1579–1587PubMed
5.
go back to reference Paris S, Boisvieux-Ulrich E, Crestani B, Houcine O, Taramelli D, Lombardi L, Latge JP (1997) Internalization of Aspergillus fumigatus conidia by epithelial and endothelial cells. Infect Immun 65(4):1510–1514PubMedCentralPubMed Paris S, Boisvieux-Ulrich E, Crestani B, Houcine O, Taramelli D, Lombardi L, Latge JP (1997) Internalization of Aspergillus fumigatus conidia by epithelial and endothelial cells. Infect Immun 65(4):1510–1514PubMedCentralPubMed
6.
go back to reference Berkova N, Lair-Fulleringer S, Femenia F, Huet D, Wagner MC, Gorna K, Tournier F, Ibrahim-Granet O, Guillot J, Chermette R, Boireau P, Latge JP (2006) Aspergillus fumigatus conidia inhibit tumour necrosis factor- or staurosporine-induced apoptosis in epithelial cells. Int Immunol 18(1):139–150PubMed Berkova N, Lair-Fulleringer S, Femenia F, Huet D, Wagner MC, Gorna K, Tournier F, Ibrahim-Granet O, Guillot J, Chermette R, Boireau P, Latge JP (2006) Aspergillus fumigatus conidia inhibit tumour necrosis factor- or staurosporine-induced apoptosis in epithelial cells. Int Immunol 18(1):139–150PubMed
7.
go back to reference Amin S, Thywissen A, Heinekamp T, Saluz HP, Brakhage AA (2014) Melanin dependent survival of Aspergillus fumigatus conidia in lung epithelial cells. Int J Med Microbiol IJMM 304(5–6):626–636. doi:10.1016/j.ijmm.2014.04.009 Amin S, Thywissen A, Heinekamp T, Saluz HP, Brakhage AA (2014) Melanin dependent survival of Aspergillus fumigatus conidia in lung epithelial cells. Int J Med Microbiol IJMM 304(5–6):626–636. doi:10.​1016/​j.​ijmm.​2014.​04.​009
12.
go back to reference Gersuk GM, Underhill DM, Zhu L, Marr KA (2006) Dectin-1 and TLRs permit macrophages to distinguish between different Aspergillus fumigatus cellular states. J Immunol 176(6):3717–3724PubMed Gersuk GM, Underhill DM, Zhu L, Marr KA (2006) Dectin-1 and TLRs permit macrophages to distinguish between different Aspergillus fumigatus cellular states. J Immunol 176(6):3717–3724PubMed
16.
go back to reference Luther K, Torosantucci A, Brakhage AA, Heesemann J, Ebel F (2007) Phagocytosis of Aspergillus fumigatus conidia by murine macrophages involves recognition by the dectin-1 beta-glucan receptor and Toll-like receptor 2. Cell Microbiol 9(2):368–381PubMed Luther K, Torosantucci A, Brakhage AA, Heesemann J, Ebel F (2007) Phagocytosis of Aspergillus fumigatus conidia by murine macrophages involves recognition by the dectin-1 beta-glucan receptor and Toll-like receptor 2. Cell Microbiol 9(2):368–381PubMed
17.
go back to reference Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K, Elluru SR, Clavaud C, Paris S, Brakhage AA, Kaveri SV, Romani L, Latge JP (2009) Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460(7259):1117–1121. doi:10.1038/nature08264 PubMed Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K, Elluru SR, Clavaud C, Paris S, Brakhage AA, Kaveri SV, Romani L, Latge JP (2009) Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460(7259):1117–1121. doi:10.​1038/​nature08264 PubMed
18.
go back to reference Hohl TM, Van Epps HL, Rivera A, Morgan LA, Chen PL, Feldmesser M, Pamer EG (2005) Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display. PLoS Pathog 1(3):18 Hohl TM, Van Epps HL, Rivera A, Morgan LA, Chen PL, Feldmesser M, Pamer EG (2005) Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display. PLoS Pathog 1(3):18
19.
go back to reference Langfelder K, Jahn B, Gehringer H, Schmidt A, Wanner G, Brakhage AA (1998) Identification of a polyketide synthase gene (pksP) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence. Med Microbiol Immunol 187(2):79–89PubMed Langfelder K, Jahn B, Gehringer H, Schmidt A, Wanner G, Brakhage AA (1998) Identification of a polyketide synthase gene (pksP) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence. Med Microbiol Immunol 187(2):79–89PubMed
20.
go back to reference Jahn B, Koch A, Schmidt A, Wanner G, Gehringer H, Bhakdi S, Brakhage AA (1997) Isolation and characterization of a pigmentless-conidium mutant of Aspergillus fumigatus with altered conidial surface and reduced virulence. Infect Immun 65(12):5110–5117PubMedCentralPubMed Jahn B, Koch A, Schmidt A, Wanner G, Gehringer H, Bhakdi S, Brakhage AA (1997) Isolation and characterization of a pigmentless-conidium mutant of Aspergillus fumigatus with altered conidial surface and reduced virulence. Infect Immun 65(12):5110–5117PubMedCentralPubMed
21.
go back to reference Jahn B, Langfelder K, Schneider U, Schindel C, Brakhage AA (2002) PKSP-dependent reduction of phagolysosome fusion and intracellular kill of Aspergillus fumigatus conidia by human monocyte-derived macrophages. Cell Microbiol 4(12):793–803PubMed Jahn B, Langfelder K, Schneider U, Schindel C, Brakhage AA (2002) PKSP-dependent reduction of phagolysosome fusion and intracellular kill of Aspergillus fumigatus conidia by human monocyte-derived macrophages. Cell Microbiol 4(12):793–803PubMed
22.
go back to reference Pihet M, Vandeputte P, Tronchin G, Renier G, Saulnier P, Georgeault S, Mallet R, Chabasse D, Symoens F, Bouchara JP (2009) Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol 9:177. doi:10.1186/1471-2180-9-177 PubMedCentralPubMed Pihet M, Vandeputte P, Tronchin G, Renier G, Saulnier P, Georgeault S, Mallet R, Chabasse D, Symoens F, Bouchara JP (2009) Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol 9:177. doi:10.​1186/​1471-2180-9-177 PubMedCentralPubMed
23.
go back to reference Bayry J, Beaussart A, Dufrene YF, Sharma M, Bansal K, Kniemeyer O, Aimanianda V, Brakhage AA, Kaveri SV, Kwon-Chung KJ, Latge JP, Beauvais A (2014) Surface structure characterization of Aspergillus fumigatus conidia mutated in the melanin synthesis pathway and their human cellular immune response. Infect Immun 82(8):3141–3153PubMedCentralPubMed Bayry J, Beaussart A, Dufrene YF, Sharma M, Bansal K, Kniemeyer O, Aimanianda V, Brakhage AA, Kaveri SV, Kwon-Chung KJ, Latge JP, Beauvais A (2014) Surface structure characterization of Aspergillus fumigatus conidia mutated in the melanin synthesis pathway and their human cellular immune response. Infect Immun 82(8):3141–3153PubMedCentralPubMed
26.
go back to reference Serrano-Gomez D, Dominguez-Soto A, Ancochea J, Jimenez-Heffernan JA, Leal JA, Corbi AL (2004) Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J Immunol 173(9):5635–5643PubMed Serrano-Gomez D, Dominguez-Soto A, Ancochea J, Jimenez-Heffernan JA, Leal JA, Corbi AL (2004) Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J Immunol 173(9):5635–5643PubMed
27.
go back to reference Meier A, Kirschning CJ, Nikolaus T, Wagner H, Heesemann J, Ebel F (2003) Toll-like receptor (TLR) 2 and TLR4 are essential for Aspergillus-induced activation of murine macrophages. Cell Microbiol 5(8):561–570PubMed Meier A, Kirschning CJ, Nikolaus T, Wagner H, Heesemann J, Ebel F (2003) Toll-like receptor (TLR) 2 and TLR4 are essential for Aspergillus-induced activation of murine macrophages. Cell Microbiol 5(8):561–570PubMed
28.
go back to reference Netea MG, Warris A, Van der Meer JW, Fenton MJ, Verver-Janssen TJ, Jacobs LE, Andresen T, Verweij PE, Kullberg BJ (2003) Aspergillus fumigatus evades immune recognition during germination through loss of toll-like receptor-4-mediated signal transduction. J Infect Dis 188(2):320–326. doi:10.1086/376456 PubMed Netea MG, Warris A, Van der Meer JW, Fenton MJ, Verver-Janssen TJ, Jacobs LE, Andresen T, Verweij PE, Kullberg BJ (2003) Aspergillus fumigatus evades immune recognition during germination through loss of toll-like receptor-4-mediated signal transduction. J Infect Dis 188(2):320–326. doi:10.​1086/​376456 PubMed
29.
go back to reference Chai LY, Vonk AG, Kullberg BJ, Verweij PE, Verschueren I, van der Meer JW, Joosten LA, Latge JP, Netea MG (2011) Aspergillus fumigatus cell wall components differentially modulate host TLR2 and TLR4 responses. Microbes Infect Inst Pasteur 13(2):151–159. doi:10.1016/j.micinf.2010.10.005 Chai LY, Vonk AG, Kullberg BJ, Verweij PE, Verschueren I, van der Meer JW, Joosten LA, Latge JP, Netea MG (2011) Aspergillus fumigatus cell wall components differentially modulate host TLR2 and TLR4 responses. Microbes Infect Inst Pasteur 13(2):151–159. doi:10.​1016/​j.​micinf.​2010.​10.​005
31.
go back to reference Bellocchio S, Montagnoli C, Bozza S, Gaziano R, Rossi G, Mambula SS, Vecchi A, Mantovani A, Levitz SM, Romani L (2004) The contribution of the Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol 172(5):3059–3069PubMed Bellocchio S, Montagnoli C, Bozza S, Gaziano R, Rossi G, Mambula SS, Vecchi A, Mantovani A, Levitz SM, Romani L (2004) The contribution of the Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol 172(5):3059–3069PubMed
32.
go back to reference Ramaprakash H, Ito T, Standiford TJ, Kunkel SL, Hogaboam CM (2009) Toll-like receptor 9 modulates immune responses to Aspergillus fumigatus conidia in immunodeficient and allergic mice. Infect Immun 77(1):108–119. doi:10.1128/IAI. 00998-08 PubMedCentralPubMed Ramaprakash H, Ito T, Standiford TJ, Kunkel SL, Hogaboam CM (2009) Toll-like receptor 9 modulates immune responses to Aspergillus fumigatus conidia in immunodeficient and allergic mice. Infect Immun 77(1):108–119. doi:10.​1128/​IAI.​ 00998-08 PubMedCentralPubMed
33.
go back to reference Willment JA, Marshall AS, Reid DM, Williams DL, Wong SY, Gordon S, Brown GD (2005) The human beta-glucan receptor is widely expressed and functionally equivalent to murine Dectin-1 on primary cells. Eur J Immunol 35(5):1539–1547. doi:10.1002/eji.200425725 PubMed Willment JA, Marshall AS, Reid DM, Williams DL, Wong SY, Gordon S, Brown GD (2005) The human beta-glucan receptor is widely expressed and functionally equivalent to murine Dectin-1 on primary cells. Eur J Immunol 35(5):1539–1547. doi:10.​1002/​eji.​200425725 PubMed
34.
go back to reference Philippe B, Ibrahim-Granet O, Prevost MC, Gougerot-Pocidalo MA, Sanchez Perez M, Van der Meeren A, Latge JP (2003) Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infect Immun 71(6):3034–3042PubMedCentralPubMed Philippe B, Ibrahim-Granet O, Prevost MC, Gougerot-Pocidalo MA, Sanchez Perez M, Van der Meeren A, Latge JP (2003) Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infect Immun 71(6):3034–3042PubMedCentralPubMed
35.
go back to reference Ibrahim-Granet O, Philippe B, Boleti H, Boisvieux-Ulrich E, Grenet D, Stern M, Latge JP (2003) Phagocytosis and intracellular fate of Aspergillus fumigatus conidia in alveolar macrophages. Infect Immun 71(2):891–903PubMedCentralPubMed Ibrahim-Granet O, Philippe B, Boleti H, Boisvieux-Ulrich E, Grenet D, Stern M, Latge JP (2003) Phagocytosis and intracellular fate of Aspergillus fumigatus conidia in alveolar macrophages. Infect Immun 71(2):891–903PubMedCentralPubMed
36.
go back to reference Claus V, Jahraus A, Tjelle T, Berg T, Kirschke H, Faulstich H, Griffiths G (1998) Lysosomal enzyme trafficking between phagosomes, endosomes, and lysosomes in J774 macrophages. Enrichment of cathepsin H in early endosomes. J Biol Chem 273(16):9842–9851PubMed Claus V, Jahraus A, Tjelle T, Berg T, Kirschke H, Faulstich H, Griffiths G (1998) Lysosomal enzyme trafficking between phagosomes, endosomes, and lysosomes in J774 macrophages. Enrichment of cathepsin H in early endosomes. J Biol Chem 273(16):9842–9851PubMed
37.
go back to reference Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, Gagnon E, Sadoul R, Rondeau C, Desjardins M (2001) The phagosome proteome: insight into phagosome functions. J Cell Biol 152(1):165–180PubMedCentralPubMed Garin J, Diez R, Kieffer S, Dermine JF, Duclos S, Gagnon E, Sadoul R, Rondeau C, Desjardins M (2001) The phagosome proteome: insight into phagosome functions. J Cell Biol 152(1):165–180PubMedCentralPubMed
38.
go back to reference Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y (1991) Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem 266(26):17707–17712PubMed Yoshimori T, Yamamoto A, Moriyama Y, Futai M, Tashiro Y (1991) Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J Biol Chem 266(26):17707–17712PubMed
39.
go back to reference Thywissen A, Heinekamp T, Dahse HM, Schmaler-Ripcke J, Nietzsche S, Zipfel PF, Brakhage AA (2011) Conidial dihydroxynaphthalene melanin of the human pathogenic fungus Aspergillus fumigatus interferes with the host endocytosis pathway. Front Microbiol 2(96) Thywissen A, Heinekamp T, Dahse HM, Schmaler-Ripcke J, Nietzsche S, Zipfel PF, Brakhage AA (2011) Conidial dihydroxynaphthalene melanin of the human pathogenic fungus Aspergillus fumigatus interferes with the host endocytosis pathway. Front Microbiol 2(96)
40.
go back to reference Levitz SM, Nong SH, Seetoo KF, Harrison TS, Speizer RA, Simons ER (1999) Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect Immun 67(2):885–890PubMedCentralPubMed Levitz SM, Nong SH, Seetoo KF, Harrison TS, Speizer RA, Simons ER (1999) Cryptococcus neoformans resides in an acidic phagolysosome of human macrophages. Infect Immun 67(2):885–890PubMedCentralPubMed
43.
go back to reference Femenia F, Huet D, Lair-Fulleringer S, Wagner MC, Sarfati J, Shingarova L, Guillot J, Boireau P, Chermette R, Berkova N (2009) Effects of conidia of various Aspergillus species on apoptosis of human pneumocytes and bronchial epithelial cells. Mycopathologia 167(5):249–262. doi:10.1007/s11046-008-9175-3 PubMed Femenia F, Huet D, Lair-Fulleringer S, Wagner MC, Sarfati J, Shingarova L, Guillot J, Boireau P, Chermette R, Berkova N (2009) Effects of conidia of various Aspergillus species on apoptosis of human pneumocytes and bronchial epithelial cells. Mycopathologia 167(5):249–262. doi:10.​1007/​s11046-008-9175-3 PubMed
44.
go back to reference Stanzani M, Orciuolo E, Lewis R, Kontoyiannis DP, Martins SL, St John LS, Komanduri KV (2005) Aspergillus fumigatus suppresses the human cellular immune response via gliotoxin-mediated apoptosis of monocytes. Blood 105(6):2258–2265. doi:10.1182/blood-2004-09-3421 PubMed Stanzani M, Orciuolo E, Lewis R, Kontoyiannis DP, Martins SL, St John LS, Komanduri KV (2005) Aspergillus fumigatus suppresses the human cellular immune response via gliotoxin-mediated apoptosis of monocytes. Blood 105(6):2258–2265. doi:10.​1182/​blood-2004-09-3421 PubMed
45.
go back to reference Pardo J, Urban C, Galvez EM, Ekert PG, Muller U, Kwon-Chung J, Lobigs M, Mullbacher A, Wallich R, Borner C, Simon MM (2006) The mitochondrial protein Bak is pivotal for gliotoxin-induced apoptosis and a critical host factor of Aspergillus fumigatus virulence in mice. J Cell Biol 174(4):509–519. doi:10.1083/jcb.200604044 PubMedCentralPubMed Pardo J, Urban C, Galvez EM, Ekert PG, Muller U, Kwon-Chung J, Lobigs M, Mullbacher A, Wallich R, Borner C, Simon MM (2006) The mitochondrial protein Bak is pivotal for gliotoxin-induced apoptosis and a critical host factor of Aspergillus fumigatus virulence in mice. J Cell Biol 174(4):509–519. doi:10.​1083/​jcb.​200604044 PubMedCentralPubMed
46.
go back to reference Brakhage AA, Bruns S, Thywissen A, Zipfel PF, Behnsen J (2010) Interaction of phagocytes with filamentous fungi. Curr Opin Microbiol 13(4):409–415PubMed Brakhage AA, Bruns S, Thywissen A, Zipfel PF, Behnsen J (2010) Interaction of phagocytes with filamentous fungi. Curr Opin Microbiol 13(4):409–415PubMed
48.
go back to reference Pillay J, den Braber I, Vrisekoop N, Kwast LM, de Boer RJ, Borghans JAM, Tesselaar K, Koenderman L (2010) In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 116(4):625–627. doi:10.1182/blood-2010-01-259028 PubMed Pillay J, den Braber I, Vrisekoop N, Kwast LM, de Boer RJ, Borghans JAM, Tesselaar K, Koenderman L (2010) In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days. Blood 116(4):625–627. doi:10.​1182/​blood-2010-01-259028 PubMed
50.
go back to reference Chignard M (2009) In: Latgé J-P, Steinbach WJ (eds) Aspergillus fumigatus and aspergillosis. ASM Press, Washington DC, pp 229–238 Chignard M (2009) In: Latgé J-P, Steinbach WJ (eds) Aspergillus fumigatus and aspergillosis. ASM Press, Washington DC, pp 229–238
51.
go back to reference Mircescu MM, Lipuma L, van Rooijen N, Pamer EG, Hohl TM (2009) Essential role for neutrophils but not alveolar macrophages at early time points following Aspergillus fumigatus infection. J Infect Dis 200(4):647–656. doi:10.1086/600380 PubMedCentralPubMed Mircescu MM, Lipuma L, van Rooijen N, Pamer EG, Hohl TM (2009) Essential role for neutrophils but not alveolar macrophages at early time points following Aspergillus fumigatus infection. J Infect Dis 200(4):647–656. doi:10.​1086/​600380 PubMedCentralPubMed
52.
go back to reference Braedel S, Radsak M, Einsele H, Latge JP, Michan A, Loeffler J, Haddad Z, Grigoleit U, Schild H, Hebart H (2004) Aspergillus fumigatus antigens activate innate immune cells via toll-like receptors 2 and 4. Br J Haematol 125(3):392–399. doi:10.1111/j.1365-2141.2004.04922.x PubMed Braedel S, Radsak M, Einsele H, Latge JP, Michan A, Loeffler J, Haddad Z, Grigoleit U, Schild H, Hebart H (2004) Aspergillus fumigatus antigens activate innate immune cells via toll-like receptors 2 and 4. Br J Haematol 125(3):392–399. doi:10.​1111/​j.​1365-2141.​2004.​04922.​x PubMed
53.
go back to reference Kennedy AD, Willment JA, Dorward DW, Williams DL, Brown GD, DeLeo FR (2007) Dectin-1 promotes fungicidal activity of human neutrophils. Eur J Immunol 37(2):467–478. doi:10.1002/eji.200636653 PubMed Kennedy AD, Willment JA, Dorward DW, Williams DL, Brown GD, DeLeo FR (2007) Dectin-1 promotes fungicidal activity of human neutrophils. Eur J Immunol 37(2):467–478. doi:10.​1002/​eji.​200636653 PubMed
54.
go back to reference Werner JL, Metz AE, Horn D, Schoeb TR, Hewitt MM, Schwiebert LM, Faro-Trindade I, Brown GD, Steele C (2009) Requisite role for the dectin-1 beta-glucan receptor in pulmonary defense against Aspergillus fumigatus. J Immunol 182(8):4938–4946. doi:10.4049/jimmunol.0804250 PubMedCentralPubMed Werner JL, Metz AE, Horn D, Schoeb TR, Hewitt MM, Schwiebert LM, Faro-Trindade I, Brown GD, Steele C (2009) Requisite role for the dectin-1 beta-glucan receptor in pulmonary defense against Aspergillus fumigatus. J Immunol 182(8):4938–4946. doi:10.​4049/​jimmunol.​0804250 PubMedCentralPubMed
56.
go back to reference 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(10):6367–6373PubMed 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(10):6367–6373PubMed
59.
go back to reference Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, Cassatella MA (2000) The neutrophil as a cellular source of chemokines. Immunol Rev 177:195–203PubMed Scapini P, Lapinet-Vera JA, Gasperini S, Calzetti F, Bazzoni F, Cassatella MA (2000) The neutrophil as a cellular source of chemokines. Immunol Rev 177:195–203PubMed
61.
go back to reference Diamond RD, Clark RA (1982) Damage to Aspergillus fumigatus and Rhizopus oryzae hyphae by oxidative and nonoxidative microbicidal products of human neutrophils in vitro. Infect Immun 38(2):487–495PubMedCentralPubMed Diamond RD, Clark RA (1982) Damage to Aspergillus fumigatus and Rhizopus oryzae hyphae by oxidative and nonoxidative microbicidal products of human neutrophils in vitro. Infect Immun 38(2):487–495PubMedCentralPubMed
62.
go back to reference Pollock JD, Williams DA, Gifford MA, Li LL, Du X, Fisherman J, Orkin SH, Doerschuk CM, Dinauer MC (1995) Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 9(2):202–209. doi:10.1038/ng0295-202 PubMed Pollock JD, Williams DA, Gifford MA, Li LL, Du X, Fisherman J, Orkin SH, Doerschuk CM, Dinauer MC (1995) Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 9(2):202–209. doi:10.​1038/​ng0295-202 PubMed
64.
65.
go back to reference Lessing F, Kniemeyer O, Wozniok I, Loeffler J, Kurzai O, Haertl A, Brakhage AA (2007) The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot Cell 6(12):2290–2302. doi:10.1128/EC.00267-07 PubMedCentralPubMed Lessing F, Kniemeyer O, Wozniok I, Loeffler J, Kurzai O, Haertl A, Brakhage AA (2007) The Aspergillus fumigatus transcriptional regulator AfYap1 represents the major regulator for defense against reactive oxygen intermediates but is dispensable for pathogenicity in an intranasal mouse infection model. Eukaryot Cell 6(12):2290–2302. doi:10.​1128/​EC.​00267-07 PubMedCentralPubMed
66.
go back to reference Lambou K, Lamarre C, Beau R, Dufour N, Latge JP (2010) Functional analysis of the superoxide dismutase family in Aspergillus fumigatus. Mol Microbiol 75(4):910–923PubMed Lambou K, Lamarre C, Beau R, Dufour N, Latge JP (2010) Functional analysis of the superoxide dismutase family in Aspergillus fumigatus. Mol Microbiol 75(4):910–923PubMed
67.
go back to reference Bogdan C (2011) Reactive oxygen and reactive nitrogen intermediates in the immune system. Immunology of infectious diseases. ASM Press, Washington, DC Bogdan C (2011) Reactive oxygen and reactive nitrogen intermediates in the immune system. Immunology of infectious diseases. ASM Press, Washington, DC
68.
go back to reference Lapp K, Vödisch M, Kroll K, Strassburger M, Kniemeyer O, Heinekamp T, Brakhage AA (2014) Characterization of the Aspergillus fumigatus detoxification systems for reactive nitrogen intermediates and their impact on virulence. Front Microbiol 5. doi:10.3389/fmicb.2014.00469 Lapp K, Vödisch M, Kroll K, Strassburger M, Kniemeyer O, Heinekamp T, Brakhage AA (2014) Characterization of the Aspergillus fumigatus detoxification systems for reactive nitrogen intermediates and their impact on virulence. Front Microbiol 5. doi:10.​3389/​fmicb.​2014.​00469
70.
go back to reference Levitz SM, Selsted ME, Ganz T, Lehrer RI, Diamond RD (1986) In vitro killing of spores and hyphae of Aspergillus fumigatus and Rhizopus oryzae by rabbit neutrophil cationic peptides and bronchoalveolar macrophages. J Infect Dis 154(3):483–489PubMed Levitz SM, Selsted ME, Ganz T, Lehrer RI, Diamond RD (1986) In vitro killing of spores and hyphae of Aspergillus fumigatus and Rhizopus oryzae by rabbit neutrophil cationic peptides and bronchoalveolar macrophages. J Infect Dis 154(3):483–489PubMed
72.
go back to reference Reeves EP, Lu H, Jacobs HL, Messina CG, Bolsover S, Gabella G, Potma EO, Warley A, Roes J, Segal AW (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416(6878):291–297. doi:10.1038/416291a PubMed Reeves EP, Lu H, Jacobs HL, Messina CG, Bolsover S, Gabella G, Potma EO, Warley A, Roes J, Segal AW (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416(6878):291–297. doi:10.​1038/​416291a PubMed
73.
go back to reference Prufer S, Weber M, Stein P, Bosmann M, Stassen M, Kreft A, Schild H, Radsak MP (2014) Oxidative burst and neutrophil elastase contribute to clearance of Aspergillus fumigatus pneumonia in mice. Immunobiology 219(2):87–96. doi:10.1016/j.imbio.2013.08.010 PubMed Prufer S, Weber M, Stein P, Bosmann M, Stassen M, Kreft A, Schild H, Radsak MP (2014) Oxidative burst and neutrophil elastase contribute to clearance of Aspergillus fumigatus pneumonia in mice. Immunobiology 219(2):87–96. doi:10.​1016/​j.​imbio.​2013.​08.​010 PubMed
74.
go back to reference Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303(5663):1532–1535. doi:10.1126/science.1092385 PubMed Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A (2004) Neutrophil extracellular traps kill bacteria. Science 303(5663):1532–1535. doi:10.​1126/​science.​1092385 PubMed
75.
go back to reference Bruns S, Kniemeyer O, Hasenberg M, Aimanianda V, Nietzsche S, Thywissen A, Jeron A, Latge JP, Brakhage AA, Gunzer M (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(4):1000873 Bruns S, Kniemeyer O, Hasenberg M, Aimanianda V, Nietzsche S, Thywissen A, Jeron A, Latge JP, Brakhage AA, Gunzer M (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(4):1000873
77.
go back to reference Brinkmann V, Zychlinsky A (2012) Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 198(5):773–783PubMedCentralPubMed Brinkmann V, Zychlinsky A (2012) Neutrophil extracellular traps: is immunity the second function of chromatin? J Cell Biol 198(5):773–783PubMedCentralPubMed
78.
go back to reference Hakkim A, Fuchs TA, Martinez NE, Hess S, Prinz H, Zychlinsky A, Waldmann H (2011) Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat Chem Biol 7(2):75–77PubMed Hakkim A, Fuchs TA, Martinez NE, Hess S, Prinz H, Zychlinsky A, Waldmann H (2011) Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat Chem Biol 7(2):75–77PubMed
79.
go back to reference Jaillon S, Peri G, Delneste Y, Frémaux I, Doni A, Moalli F, Garlanda C, Romani L, Gascan H, Bellocchio S, Bozza S, Cassatella MA, Jeannin P, Mantovani A (2007) The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J Exp Med 204(4):793–804. doi:10.1084/jem.20061301 PubMedCentralPubMed Jaillon S, Peri G, Delneste Y, Frémaux I, Doni A, Moalli F, Garlanda C, Romani L, Gascan H, Bellocchio S, Bozza S, Cassatella MA, Jeannin P, Mantovani A (2007) The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J Exp Med 204(4):793–804. doi:10.​1084/​jem.​20061301 PubMedCentralPubMed
80.
go back to reference Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 5(10):e1000639. doi:10.1371/journal.ppat.1000639 PubMedCentralPubMed Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, Nacken W, Brinkmann V, Jungblut PR, Zychlinsky A (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 5(10):e1000639. doi:10.​1371/​journal.​ppat.​1000639 PubMedCentralPubMed
81.
go back to reference von Köckritz-Blickwede M, Goldmann O, Thulin P, Heinemann K, Norrby-Teglund A, Rohde M, Medina E (2008) Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111(6):3070–3080. doi:10.1182/blood-2007-07-104018 von Köckritz-Blickwede M, Goldmann O, Thulin P, Heinemann K, Norrby-Teglund A, Rohde M, Medina E (2008) Phagocytosis-independent antimicrobial activity of mast cells by means of extracellular trap formation. Blood 111(6):3070–3080. doi:10.​1182/​blood-2007-07-104018
82.
go back to reference Garlanda C, Hirsch E, Bozza S, Salustri A, De Acetis M, Nota R, Maccagno A, Riva F, Bottazzi B, Peri G, Doni A, Vago L, Botto M, De Santis R, Carminati P, Siracusa G, Altruda F, Vecchi A, Romani L, Mantovani A (2002) Non-redundant role of the long pentraxin PTX3 in anti-fungal innate immune response. Nature 420(6912):182–186. doi:10.1038/nature01195 PubMed Garlanda C, Hirsch E, Bozza S, Salustri A, De Acetis M, Nota R, Maccagno A, Riva F, Bottazzi B, Peri G, Doni A, Vago L, Botto M, De Santis R, Carminati P, Siracusa G, Altruda F, Vecchi A, Romani L, Mantovani A (2002) Non-redundant role of the long pentraxin PTX3 in anti-fungal innate immune response. Nature 420(6912):182–186. doi:10.​1038/​nature01195 PubMed
83.
go back to reference D’Angelo C, De Luca A, Zelante T, Bonifazi P, Moretti S, Giovannini G, Iannitti RG, Zagarella S, Bozza S, Campo S, Salvatori G, Romani L (2009) Exogenous pentraxin 3 restores antifungal resistance and restrains inflammation in murine chronic granulomatous disease. J Immunol 183(7):4609–4618. doi:10.4049/jimmunol.0900345 PubMed D’Angelo C, De Luca A, Zelante T, Bonifazi P, Moretti S, Giovannini G, Iannitti RG, Zagarella S, Bozza S, Campo S, Salvatori G, Romani L (2009) Exogenous pentraxin 3 restores antifungal resistance and restrains inflammation in murine chronic granulomatous disease. J Immunol 183(7):4609–4618. doi:10.​4049/​jimmunol.​0900345 PubMed
84.
go back to reference Cunha C, Aversa F, Lacerda JF, Busca A, Kurzai O, Grube M, Loffler J, Maertens JA, Bell AS, Inforzato A, Barbati E, Almeida B, Santos e Sousa P, Barbui A, Potenza L, Caira M, Rodrigues F, Salvatori G, Pagano L, Luppi M, Mantovani A, Velardi A, Romani L, Carvalho A (2014) Genetic PTX3 deficiency and aspergillosis in stem-cell transplantation. N Engl J Med 370(5):421–432. doi:10.1056/NEJMoa1211161 PubMed Cunha C, Aversa F, Lacerda JF, Busca A, Kurzai O, Grube M, Loffler J, Maertens JA, Bell AS, Inforzato A, Barbati E, Almeida B, Santos e Sousa P, Barbui A, Potenza L, Caira M, Rodrigues F, Salvatori G, Pagano L, Luppi M, Mantovani A, Velardi A, Romani L, Carvalho A (2014) Genetic PTX3 deficiency and aspergillosis in stem-cell transplantation. N Engl J Med 370(5):421–432. doi:10.​1056/​NEJMoa1211161 PubMed
85.
go back to reference McCormick A, Heesemann L, Wagener J, Marcos V, Hartl D, Loeffler J, Heesemann J, Ebel F (2010) NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microbes Infect Inst Pasteur 12(12–13):928–936. doi:10.1016/j.micinf.2010.06.009 McCormick A, Heesemann L, Wagener J, Marcos V, Hartl D, Loeffler J, Heesemann J, Ebel F (2010) NETs formed by human neutrophils inhibit growth of the pathogenic mold Aspergillus fumigatus. Microbes Infect Inst Pasteur 12(12–13):928–936. doi:10.​1016/​j.​micinf.​2010.​06.​009
86.
go back to reference Zipfel PF, Skerka C (2009) Complement regulators and inhibitory proteins. Nat Rev Immunol 9(10):729–740PubMed Zipfel PF, Skerka C (2009) Complement regulators and inhibitory proteins. Nat Rev Immunol 9(10):729–740PubMed
87.
go back to reference Ricklin D, Hajishengallis G, Yang K, Lambris JD (2010) Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11(9):785–797PubMedCentralPubMed Ricklin D, Hajishengallis G, Yang K, Lambris JD (2010) Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11(9):785–797PubMedCentralPubMed
88.
go back to reference Hector RF, Yee E, Collins MS (1990) Use of DBA/2N mice in models of systemic candidiasis and pulmonary and systemic aspergillosis. Infect Immun 58(5):1476–1478PubMedCentralPubMed Hector RF, Yee E, Collins MS (1990) Use of DBA/2N mice in models of systemic candidiasis and pulmonary and systemic aspergillosis. Infect Immun 58(5):1476–1478PubMedCentralPubMed
89.
go back to reference Svirshchevskaya EV, Shevchenko MA, Huet D, Femenia F, Latge JP, Boireau P, Berkova NP (2009) Susceptibility of mice to invasive aspergillosis correlates with delayed cell influx into the lungs. Int J Immunogenet 36(5):289–299PubMed Svirshchevskaya EV, Shevchenko MA, Huet D, Femenia F, Latge JP, Boireau P, Berkova NP (2009) Susceptibility of mice to invasive aspergillosis correlates with delayed cell influx into the lungs. Int J Immunogenet 36(5):289–299PubMed
90.
go back to reference Henwick S, Hetherington SV, Patrick CC (1993) Complement binding to Aspergillus conidia correlates with pathogenicity. J Lab Clin Med 122(1):27–35PubMed Henwick S, Hetherington SV, Patrick CC (1993) Complement binding to Aspergillus conidia correlates with pathogenicity. J Lab Clin Med 122(1):27–35PubMed
91.
go back to reference Kozel TR, Wilson MA, Farrell TP, Levitz SM (1989) Activation of C3 and binding to Aspergillus fumigatus conidia and hyphae. Infect Immun 57(11):3412–3417PubMedCentralPubMed Kozel TR, Wilson MA, Farrell TP, Levitz SM (1989) Activation of C3 and binding to Aspergillus fumigatus conidia and hyphae. Infect Immun 57(11):3412–3417PubMedCentralPubMed
92.
go back to reference Tsai HF, Chang YC, Washburn RG, Wheeler MH, Kwon-Chung KJ (1998) The developmentally regulated alb1 gene of Aspergillus fumigatus: its role in modulation of conidial morphology and virulence. J Bacteriol 180(12):3031–3038PubMedCentralPubMed Tsai HF, Chang YC, Washburn RG, Wheeler MH, Kwon-Chung KJ (1998) The developmentally regulated alb1 gene of Aspergillus fumigatus: its role in modulation of conidial morphology and virulence. J Bacteriol 180(12):3031–3038PubMedCentralPubMed
93.
go back to reference Neth O, Jack DL, Dodds AW, Holzel H, Klein NJ, Turner MW (2000) Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect Immun 68(2):688–693PubMedCentralPubMed Neth O, Jack DL, Dodds AW, Holzel H, Klein NJ, Turner MW (2000) Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect Immun 68(2):688–693PubMedCentralPubMed
94.
go back to reference Crosdale DJ, Poulton KV, Ollier WE, Thomson W, Denning DW (2001) Mannose-binding lectin gene polymorphisms as a susceptibility factor for chronic necrotizing pulmonary aspergillosis. J Infect Dis 184(5):653–656PubMed Crosdale DJ, Poulton KV, Ollier WE, Thomson W, Denning DW (2001) Mannose-binding lectin gene polymorphisms as a susceptibility factor for chronic necrotizing pulmonary aspergillosis. J Infect Dis 184(5):653–656PubMed
95.
go back to reference Kaur S, Gupta VK, Thiel S, Sarma PU, Madan T (2007) Protective role of mannan-binding lectin in a murine model of invasive pulmonary aspergillosis. Clin Exp Immunol 148(2):382–389PubMedCentralPubMed Kaur S, Gupta VK, Thiel S, Sarma PU, Madan T (2007) Protective role of mannan-binding lectin in a murine model of invasive pulmonary aspergillosis. Clin Exp Immunol 148(2):382–389PubMedCentralPubMed
96.
go back to reference Ma YJ, Doni A, Hummelshoj T, Honore C, Bastone A, Mantovani A, Thielens NM, Garred P (2009) Synergy between ficolin-2 and pentraxin 3 boosts innate immune recognition and complement deposition. J Biol Chem 284(41):28263–28275PubMedCentralPubMed Ma YJ, Doni A, Hummelshoj T, Honore C, Bastone A, Mantovani A, Thielens NM, Garred P (2009) Synergy between ficolin-2 and pentraxin 3 boosts innate immune recognition and complement deposition. J Biol Chem 284(41):28263–28275PubMedCentralPubMed
97.
go back to reference Moalli F, Doni A, Deban L, Zelante T, Zagarella S, Bottazzi B, Romani L, Mantovani A, Garlanda C (2010) Role of complement and Fcγ receptors in the protective activity of the long pentraxin PTX3 against Aspergillus fumigatus. Blood 116(24):5170–5180PubMed Moalli F, Doni A, Deban L, Zelante T, Zagarella S, Bottazzi B, Romani L, Mantovani A, Garlanda C (2010) Role of complement and Fcγ receptors in the protective activity of the long pentraxin PTX3 against Aspergillus fumigatus. Blood 116(24):5170–5180PubMed
98.
go back to reference Behnsen J, Hartmann A, Schmaler J, Gehrke A, Brakhage AA, Zipfel PF (2008) The opportunistic human pathogenic fungus Aspergillus fumigatus evades the host complement system. Infect Immun 76(2):820–827PubMedCentralPubMed Behnsen J, Hartmann A, Schmaler J, Gehrke A, Brakhage AA, Zipfel PF (2008) The opportunistic human pathogenic fungus Aspergillus fumigatus evades the host complement system. Infect Immun 76(2):820–827PubMedCentralPubMed
99.
go back to reference Washburn RG, DeHart DJ, Agwu DE, Bryant-Varela BJ, Julian NC (1990) Aspergillus fumigatus complement inhibitor: production, characterization, and purification by hydrophobic interaction and thin-layer chromatography. Infect Immun 58(11):3508–3515PubMedCentralPubMed Washburn RG, DeHart DJ, Agwu DE, Bryant-Varela BJ, Julian NC (1990) Aspergillus fumigatus complement inhibitor: production, characterization, and purification by hydrophobic interaction and thin-layer chromatography. Infect Immun 58(11):3508–3515PubMedCentralPubMed
100.
go back to reference Rambach G, Dum D, Mohsenipour I, Hagleitner M, Wurzner R, Lass-Florl C, Speth C (2010) Secretion of a fungal protease represents a complement evasion mechanism in cerebral aspergillosis. Mol Immunol 47(7–8):1438–1449PubMed Rambach G, Dum D, Mohsenipour I, Hagleitner M, Wurzner R, Lass-Florl C, Speth C (2010) Secretion of a fungal protease represents a complement evasion mechanism in cerebral aspergillosis. Mol Immunol 47(7–8):1438–1449PubMed
101.
go back to reference Behnsen J, Lessing F, Schindler S, Wartenberg D, Jacobsen ID, Thoen M, Zipfel PF, Brakhage AA (2010) Secreted Aspergillus fumigatus protease Alp1 degrades human complement proteins C3, C4, and C5. Infect Immun 78(8):3585–3594PubMedCentralPubMed Behnsen J, Lessing F, Schindler S, Wartenberg D, Jacobsen ID, Thoen M, Zipfel PF, Brakhage AA (2010) Secreted Aspergillus fumigatus protease Alp1 degrades human complement proteins C3, C4, and C5. Infect Immun 78(8):3585–3594PubMedCentralPubMed
102.
go back to reference Kniemeyer O (2011) Proteomics of eukaryotic microorganisms: the medically and biotechnologically important fungal genus Aspergillus. Proteomics 11(15):3232–3243PubMed Kniemeyer O (2011) Proteomics of eukaryotic microorganisms: the medically and biotechnologically important fungal genus Aspergillus. Proteomics 11(15):3232–3243PubMed
103.
go back to reference Albrecht D, Guthke R, Brakhage AA, Kniemeyer O (2010) Integrative analysis of the heat shock response in Aspergillus fumigatus. BMC Genomics 11(32):1471–2164 Albrecht D, Guthke R, Brakhage AA, Kniemeyer O (2010) Integrative analysis of the heat shock response in Aspergillus fumigatus. BMC Genomics 11(32):1471–2164
104.
go back to reference Barker BM, Kroll K, Vodisch M, Mazurie A, Kniemeyer O, Cramer RA (2012) Transcriptomic and proteomic analyses of the Aspergillus fumigatus hypoxia response using an oxygen-controlled fermenter. BMC Genomics 13(62):1471–2164 Barker BM, Kroll K, Vodisch M, Mazurie A, Kniemeyer O, Cramer RA (2012) Transcriptomic and proteomic analyses of the Aspergillus fumigatus hypoxia response using an oxygen-controlled fermenter. BMC Genomics 13(62):1471–2164
105.
go back to reference Bruns S, Seidler M, Albrecht D, Salvenmoser S, Remme N, Hertweck C, Brakhage AA, Kniemeyer O, Muller FM (2010) Functional genomic profiling of Aspergillus fumigatus biofilm reveals enhanced production of the mycotoxin gliotoxin. Proteomics 10(17):3097–3107PubMed Bruns S, Seidler M, Albrecht D, Salvenmoser S, Remme N, Hertweck C, Brakhage AA, Kniemeyer O, Muller FM (2010) Functional genomic profiling of Aspergillus fumigatus biofilm reveals enhanced production of the mycotoxin gliotoxin. Proteomics 10(17):3097–3107PubMed
106.
go back to reference Vodisch M, Scherlach K, Winkler R, Hertweck C, Braun HP, Roth M, Haas H, Werner ER, Brakhage AA, Kniemeyer O (2011) Analysis of the Aspergillus fumigatus proteome reveals metabolic changes and the activation of the pseurotin A biosynthesis gene cluster in response to hypoxia. J Proteome Res 10(5):2508–2524PubMedCentralPubMed Vodisch M, Scherlach K, Winkler R, Hertweck C, Braun HP, Roth M, Haas H, Werner ER, Brakhage AA, Kniemeyer O (2011) Analysis of the Aspergillus fumigatus proteome reveals metabolic changes and the activation of the pseurotin A biosynthesis gene cluster in response to hypoxia. J Proteome Res 10(5):2508–2524PubMedCentralPubMed
107.
go back to reference Kniemeyer O, Schmidt AD, Vodisch M, Wartenberg D, Brakhage AA (2011) Identification of virulence determinants of the human pathogenic fungi Aspergillus fumigatus and Candida albicans by proteomics. Int J Med Microbiol IJMM 301(5):368–377 Kniemeyer O, Schmidt AD, Vodisch M, Wartenberg D, Brakhage AA (2011) Identification of virulence determinants of the human pathogenic fungi Aspergillus fumigatus and Candida albicans by proteomics. Int J Med Microbiol IJMM 301(5):368–377
108.
go back to reference Asif AR, Oellerich M, Amstrong VW, Riemenschneider B, Monod M, Reichard U (2006) Proteome of conidial surface associated proteins of Aspergillus fumigatus reflecting potential vaccine candidates and allergens. J Proteome Res 5(4):954–962PubMed Asif AR, Oellerich M, Amstrong VW, Riemenschneider B, Monod M, Reichard U (2006) Proteome of conidial surface associated proteins of Aspergillus fumigatus reflecting potential vaccine candidates and allergens. J Proteome Res 5(4):954–962PubMed
109.
go back to reference Ouyang H, Luo Y, Zhang L, Li Y, Jin C (2010) Proteome analysis of Aspergillus fumigatus total membrane proteins identifies proteins associated with the glycoconjugates and cell wall biosynthesis using 2D LC-MS/MS. Mol Biotechnol 44(3):177–189PubMed Ouyang H, Luo Y, Zhang L, Li Y, Jin C (2010) Proteome analysis of Aspergillus fumigatus total membrane proteins identifies proteins associated with the glycoconjugates and cell wall biosynthesis using 2D LC-MS/MS. Mol Biotechnol 44(3):177–189PubMed
110.
go back to reference Bruneau JM, Magnin T, Tagat E, Legrand R, Bernard M, Diaquin M, Fudali C, Latge JP (2001) Proteome analysis of Aspergillus fumigatus identifies glycosylphosphatidylinositol-anchored proteins associated to the cell wall biosynthesis. Electrophoresis 22(13):2812–2823PubMed Bruneau JM, Magnin T, Tagat E, Legrand R, Bernard M, Diaquin M, Fudali C, Latge JP (2001) Proteome analysis of Aspergillus fumigatus identifies glycosylphosphatidylinositol-anchored proteins associated to the cell wall biosynthesis. Electrophoresis 22(13):2812–2823PubMed
111.
go back to reference Fekkar A, Balloy V, Pionneau C, Marinach-Patrice C, Chignard M, Mazier D (2012) Secretome of human bronchial epithelial cells in response to the fungal pathogen Aspergillus fumigatus analyzed by differential in-gel electrophoresis. J Infect Dis 205(7):1163–1172PubMed Fekkar A, Balloy V, Pionneau C, Marinach-Patrice C, Chignard M, Mazier D (2012) Secretome of human bronchial epithelial cells in response to the fungal pathogen Aspergillus fumigatus analyzed by differential in-gel electrophoresis. J Infect Dis 205(7):1163–1172PubMed
112.
go back to reference Morton CO, Bouzani M, Loeffler J, Rogers TR (2012) Direct interaction studies between Aspergillus fumigatus and human immune cells; what have we learned about pathogenicity and host immunity? Front Microbiol 3(413) Morton CO, Bouzani M, Loeffler J, Rogers TR (2012) Direct interaction studies between Aspergillus fumigatus and human immune cells; what have we learned about pathogenicity and host immunity? Front Microbiol 3(413)
113.
go back to reference McDonagh A, Fedorova ND, Crabtree J, Yu Y, Kim S, Chen D, Loss O, Cairns T, Goldman G, Armstrong-James D, Haynes K, Haas H, Schrettl M, May G, Nierman WC, Bignell E (2008) Sub-telomere directed gene expression during initiation of invasive aspergillosis. PLoS Pathog 4(9):1000154 McDonagh A, Fedorova ND, Crabtree J, Yu Y, Kim S, Chen D, Loss O, Cairns T, Goldman G, Armstrong-James D, Haynes K, Haas H, Schrettl M, May G, Nierman WC, Bignell E (2008) Sub-telomere directed gene expression during initiation of invasive aspergillosis. PLoS Pathog 4(9):1000154
114.
go back to reference Curty N, Kubitschek-Barreira PH, Neves GW, Gomes D, Pizzatti L, Abdelhay E, Souza GH, Lopes-Bezerra LM (2014) Discovering the infectome of human endothelial cells challenged with Aspergillus fumigatus applying a mass spectrometry label-free approach. J Proteomics 97:126–140PubMed Curty N, Kubitschek-Barreira PH, Neves GW, Gomes D, Pizzatti L, Abdelhay E, Souza GH, Lopes-Bezerra LM (2014) Discovering the infectome of human endothelial cells challenged with Aspergillus fumigatus applying a mass spectrometry label-free approach. J Proteomics 97:126–140PubMed
115.
go back to reference Knutsen AP, Slavin RG (2011) Allergic bronchopulmonary aspergillosis in asthma and cystic fibrosis. Clin Dev Immunol 843763(10):5 Knutsen AP, Slavin RG (2011) Allergic bronchopulmonary aspergillosis in asthma and cystic fibrosis. Clin Dev Immunol 843763(10):5
116.
go back to reference Gautam P, Sundaram CS, Madan T, Gade WN, Shah A, Sirdeshmukh R, Sarma PU (2007) Identification of novel allergens of Aspergillus fumigatus using immunoproteomics approach. Clin Exp Allergy 37(8):1239–1249PubMed Gautam P, Sundaram CS, Madan T, Gade WN, Shah A, Sirdeshmukh R, Sarma PU (2007) Identification of novel allergens of Aspergillus fumigatus using immunoproteomics approach. Clin Exp Allergy 37(8):1239–1249PubMed
117.
go back to reference Singh B, Oellerich M, Kumar R, Kumar M, Bhadoria DP, Reichard U, Gupta VK, Sharma GL, Asif AR (2010) Immuno-reactive molecules identified from the secreted proteome of Aspergillus fumigatus. J Proteome Res 9(11):5517–5529PubMed Singh B, Oellerich M, Kumar R, Kumar M, Bhadoria DP, Reichard U, Gupta VK, Sharma GL, Asif AR (2010) Immuno-reactive molecules identified from the secreted proteome of Aspergillus fumigatus. J Proteome Res 9(11):5517–5529PubMed
118.
go back to reference Chow LP, Liu SL, Yu CJ, Liao HK, Tsai JJ, Tang TK (2000) Identification and expression of an allergen Asp f 13 from Aspergillus fumigatus and epitope mapping using human IgE antibodies and rabbit polyclonal antibodies. Biochem J 2:423–431 Chow LP, Liu SL, Yu CJ, Liao HK, Tsai JJ, Tang TK (2000) Identification and expression of an allergen Asp f 13 from Aspergillus fumigatus and epitope mapping using human IgE antibodies and rabbit polyclonal antibodies. Biochem J 2:423–431
119.
go back to reference Gautam P, Madan T, Gade WN, Sarma PU (2006) Immunoproteomic analysis of secretory proteins of Aspergillus fumigatus with specific IGE immunoreactivity. Indian J Clin Biochem 21(2):12–19PubMedCentralPubMed Gautam P, Madan T, Gade WN, Sarma PU (2006) Immunoproteomic analysis of secretory proteins of Aspergillus fumigatus with specific IGE immunoreactivity. Indian J Clin Biochem 21(2):12–19PubMedCentralPubMed
120.
go back to reference Glaser AG, Kirsch AI, Zeller S, Menz G, Rhyner C, Crameri R (2009) Molecular and immunological characterization of Asp f 34, a novel major cell wall allergen of Aspergillus fumigatus. Allergy 64(8):1144–1151PubMed Glaser AG, Kirsch AI, Zeller S, Menz G, Rhyner C, Crameri R (2009) Molecular and immunological characterization of Asp f 34, a novel major cell wall allergen of Aspergillus fumigatus. Allergy 64(8):1144–1151PubMed
121.
go back to reference Singh B, Singh S, Asif AR, Oellerich M, Sharma GL (2014) Allergic Aspergillosis and the antigens of Aspergillus fumigatus. Curr Protein Pept Sci 12:12 Singh B, Singh S, Asif AR, Oellerich M, Sharma GL (2014) Allergic Aspergillosis and the antigens of Aspergillus fumigatus. Curr Protein Pept Sci 12:12
122.
go back to reference Shi LN, Li FQ, Huang M, Lu JF, Kong XX, Wang SQ, Shao HF (2012) Immunoproteomics based identification of thioredoxin reductase GliT and novel Aspergillus fumigatus antigens for serologic diagnosis of invasive aspergillosis. BMC Microbiol 12(11):1471–2180 Shi LN, Li FQ, Huang M, Lu JF, Kong XX, Wang SQ, Shao HF (2012) Immunoproteomics based identification of thioredoxin reductase GliT and novel Aspergillus fumigatus antigens for serologic diagnosis of invasive aspergillosis. BMC Microbiol 12(11):1471–2180
123.
go back to reference Shi LN, Li FQ, Lu JF, Kong XX, Wang SQ, Huang M, Shao HF, Shao SH (2012) Antibody specific to thioredoxin reductase as a new biomarker for serodiagnosis of invasive aspergillosis in non-neutropenic patients. Clin Chim Acta 413(9–10):938–943PubMed Shi LN, Li FQ, Lu JF, Kong XX, Wang SQ, Huang M, Shao HF, Shao SH (2012) Antibody specific to thioredoxin reductase as a new biomarker for serodiagnosis of invasive aspergillosis in non-neutropenic patients. Clin Chim Acta 413(9–10):938–943PubMed
124.
go back to reference Reichard U, Herrmann S, Asif AR (2014) Vaccination approaches against opportunistic fungal infections caused by Aspergillus fumigatus. Curr Protein Pept Sci 12:12 Reichard U, Herrmann S, Asif AR (2014) Vaccination approaches against opportunistic fungal infections caused by Aspergillus fumigatus. Curr Protein Pept Sci 12:12
125.
go back to reference Asif AR, Oellerich M, Amstrong VW, Gross U, Reichard U (2010) Analysis of the cellular Aspergillus fumigatus proteome that reacts with sera from rabbits developing an acquired immunity after experimental aspergillosis. Electrophoresis 31(12):1947–1958PubMed Asif AR, Oellerich M, Amstrong VW, Gross U, Reichard U (2010) Analysis of the cellular Aspergillus fumigatus proteome that reacts with sera from rabbits developing an acquired immunity after experimental aspergillosis. Electrophoresis 31(12):1947–1958PubMed
126.
go back to reference Mech F, Thywissen A, Guthke R, Brakhage AA, Figge MT (2011) Automated image analysis of the host-pathogen interaction between phagocytes and Aspergillus fumigatus. PLoS One 6(5):0019591 Mech F, Thywissen A, Guthke R, Brakhage AA, Figge MT (2011) Automated image analysis of the host-pathogen interaction between phagocytes and Aspergillus fumigatus. PLoS One 6(5):0019591
127.
go back to reference Albrecht D, Kniemeyer O, Mech F, Gunzer M, Brakhage A, Guthke R (2011) On the way toward systems biology of Aspergillus fumigatus infection. Int J Med Microbiol IJMM 301(5):453–459 Albrecht D, Kniemeyer O, Mech F, Gunzer M, Brakhage A, Guthke R (2011) On the way toward systems biology of Aspergillus fumigatus infection. Int J Med Microbiol IJMM 301(5):453–459
128.
go back to reference Horn F, Heinekamp T, Kniemeyer O, Pollmacher J, Valiante V, Brakhage AA (2012) Systems biology of fungal infection. Front Microbiol 3(108) Horn F, Heinekamp T, Kniemeyer O, Pollmacher J, Valiante V, Brakhage AA (2012) Systems biology of fungal infection. Front Microbiol 3(108)
Metadata
Title
Interference of Aspergillus fumigatus with the immune response
Authors
Thorsten Heinekamp
Hella Schmidt
Katrin Lapp
Vera Pähtz
Iordana Shopova
Nora Köster-Eiserfunke
Thomas Krüger
Olaf Kniemeyer
Axel A. Brakhage
Publication date
01-03-2015
Publisher
Springer Berlin Heidelberg
Published in
Seminars in Immunopathology / Issue 2/2015
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-014-0465-1

Other articles of this Issue 2/2015

Seminars in Immunopathology 2/2015 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.