β-1,3-glucan-lacking Aspergillus fumigatus mediates an efficient antifungal immune response by activating complement and dendritic cells

References

• Romani L. Immunity to fungal infections. Nat Rev Immunol. 2004;4(1):1–23.
   PubMed Web of Science ®Google Scholar
• Braem SG, Rooijakkers SH, van Kessel KP, et al. Effective neutrophil phagocytosis of Aspergillus fumigatus is mediated by classical pathway complement activation. J Innate Immun. 2015;7(4):364–374.
   PubMed Web of Science ®Google Scholar
• Tsai HF, Washburn RG, Chang YC, et al. Aspergillus fumigatus arp1 modulates conidial pigmentation and complement deposition. Mol Microbiol. 1997;26(1):175–183.
   PubMed Web of Science ®Google Scholar
• Latge JP. Tasting the fungal cell wall. Cell Microbiol. 2010;12(7):863–872.
   PubMed Web of Science ®Google Scholar
• Heinekamp T, Schmidt H, Lapp K, et al. Interference of Aspergillus fumigatus with the immune response. Semin Immunopathol. 2015;37(2):141–152.
   PubMed Web of Science ®Google Scholar
• Henwick S, Hetherington SV, Patrick CC. Complement binding to Aspergillus conidia correlates with pathogenicity. J Lab Clin Med. 1993;122(1):27–35.
   PubMed Web of Science ®Google Scholar
• Brakhage AA, Liebmann B. Aspergillus fumigatus conidial pigment and cAMP signal transduction: significance for virulence. Med Mycol. 2005;43(Suppl 1):S75–82.
   PubMed Web of Science ®Google Scholar
• Tsai HF, Chang YC, Washburn RG, et al. The developmentally regulated alb1 gene of Aspergillus fumigatus: its role in modulation of conidial morphology and virulence. J Bacteriol. 1998;180(12):3031–3038.
   PubMed Web of Science ®Google Scholar
• Hohl TM, Van Epps HL, Rivera A, et al. Aspergillus fumigatus triggers inflammatory responses by stage-specific β-glucan display. PLoS Pathog. 2005;1(3):e30.
   PubMed Web of Science ®Google Scholar
• Lother J, Breitschopf T, Krappmann S, et al. Human dendritic cell subsets display distinct interactions with the pathogenic mould Aspergillus fumigatus. Int J Med Microbiol. 2014;304(8):1160–1168.
   PubMed Web of Science ®Google Scholar
• Dichtl K, Samantaray S, Aimanianda V, et al. Aspergillus fumigatus devoid of cell wall β-1,3-glucan is viable, massively sheds galactomannan and is killed by septum formation inhibitors. Mol Microbiol. 2015;95(3):458–471.
   PubMed Web of Science ®Google Scholar
• Beyda ND, Liao G, Endres BT, et al. Innate inflammatory response and immunopharmacologic activity of micafungin, caspofungin, and voriconazole against wild-type and FKS mutant Candida glabrata isolates. Antimicrob Agents Chemother. 2015;59(9):5405–5412.
   PubMed Web of Science ®Google Scholar
• Lin J, Wester MJ, Graus MS, et al. Nanoscopic cell-wall architecture of an immunogenic ligand in Candida albicans during antifungal drug treatment. Mol Biol Cell. 2016;27(6):1002–1014.
   PubMed Web of Science ®Google Scholar
• Romani L. Immunity to fungal infections. Nat Rev Immunol. 2011;11(4):275–288.
   PubMed Web of Science ®Google Scholar
• Wuthrich M, Deepe GS Jr., Klein B. Adaptive immunity to fungi. Annu Rev Immunol. 2012;30:115–148.
   PubMed Web of Science ®Google Scholar
• Thakur R, Anand R, Tiwari S, et al. Cytokines induce effector T-helper cells during invasive aspergillosis; what we have learned about T-helper cells? Front Microbiol. 2015;6:429.
   PubMed Web of Science ®Google Scholar
• Mech F, Thywissen A, Guthke R, et al. Automated image analysis of the host-pathogen interaction between phagocytes and Aspergillus fumigatus. PLoS One. 2011;6(5):e19591.
   PubMed Web of Science ®Google Scholar
• Pruenster M, Wilflingseder D, Banki Z, et al. C-type lectin-independent interaction of complement opsonized HIV with monocyte-derived dendritic cells. Eur J Immunol. 2005;35(9):2691–2698.
   PubMed Web of Science ®Google Scholar
• Geijtenbeek TB, Gringhuis SI. C-type lectin receptors in the control of T helper cell differentiation. Nat Rev Immunol. 2016;16(7):433–448.
   PubMed Web of Science ®Google Scholar
• van de Veerdonk FL, Marijnissen RJ, Kullberg BJ, et al. The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe. 2009;5(4):329–340.
   PubMed Web of Science ®Google Scholar
• Barreto-Bergter E, Figueiredo RT. Fungal glycans and the innate immune recognition. Front Cell Infect Microbiol. 2014;4:145.
   PubMed Web of Science ®Google Scholar
• Amarsaikhan N, Templeton SP. Co-recognition of β-glucan and chitin and programming of adaptive immunity to Aspergillus fumigatus. Front Microbiol. 2015;6:344.
   PubMed Web of Science ®Google Scholar
• Merle NS, Church SE, Fremeaux-Bacchi V, et al. Complement system Part I - molecular mechanisms of activation and regulation. Front Immunol. 2015;6:262.
   PubMed Web of Science ®Google Scholar
• Chotirmall SH, Mirkovic B, Lavelle GM, et al. Immunoevasive Aspergillus virulence factors. Mycopathologia. 2014;178(5–6):363–370.
   PubMed Web of Science ®Google Scholar
• Roy RM, Paes HC, Nanjappa SG, et al. Complement component 3C3 and C3a receptor are required in chitin-dependent allergic sensitization to Aspergillus fumigatus but dispensable in chitin-induced innate allergic inflammation. MBio. 2013;4(2).
   Web of Science ®Google Scholar
• Gringhuis SI, Den Dunnen J, Litjens M, et al. Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappaB activation through Raf-1 and Syk. Nat Immunol. 2009;10(2):203–213.
   PubMed Web of Science ®Google Scholar
• Gringhuis SI, Den Dunnen J, Litjens M, et al. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity. 2007;26(5):605–616.
   PubMed Web of Science ®Google Scholar
• Gringhuis SI, Den Dunnen J, Litjens M, et al. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat Immunol. 2009;10(10):1081–1088.
   PubMed Web of Science ®Google Scholar
• Wilflingseder D, Schroll A, Hackl H, et al. Immediate T-Helper 17 polarization upon triggering CD11b/c on HIV-exposed dendritic cells. J Infect Dis. 2015;212(1):44–56.
   PubMed Web of Science ®Google Scholar
• Raingeaud J, Gupta S, Rogers JS, et al. Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J Biol Chem. 1995;270(13):7420–7426.
   PubMed Web of Science ®Google Scholar
• Chai LY, Vonk AG, Kullberg BJ, et al. Aspergillus fumigatus cell wall components differentially modulate host TLR2 and TLR4 responses. Microbes Infect. 2011;13(2):151–159.
   PubMed Web of Science ®Google Scholar
• Geijtenbeek TB, Gringhuis SI. Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol. 2009;9(7):465–479.
   PubMed Web of Science ®Google Scholar
• Cambi A, Netea MG, Mora-Montes HM, et al. Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J Biol Chem. 2008;283(29):20590–20599.
   PubMed Web of Science ®Google Scholar
• Means TK, Mylonakis E, Tampakakis E, et al. Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. J Exp Med. 2009;206(3):637–653.
   PubMed Web of Science ®Google Scholar
• Posch W, Cardinaud S, Hamimi C, et al. Antibodies attenuate the capacity of dendritic cells to stimulate HIV-specific cytotoxic T lymphocytes. J Allergy Clin Immunol. 2012;130(6):1368–1374 e1362.
   PubMed Web of Science ®Google Scholar
• Wilflingseder D, Banki Z, Garcia E, et al. IgG opsonization of HIV impedes provirus formation in and infection of dendritic cells and subsequent long-term transfer to T cells. J Immunol. 2007;178(12):7840–7848.
   PubMed Web of Science ®Google Scholar
• Hsu PD, Scott DA, Weinstein JA, et al. DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol. 2013;31(9):827–832.
   PubMed Web of Science ®Google Scholar
• Sanjana NE, Shalem O, Zhang F. Improved vectors and genome-wide libraries for CRISPR screening. Nat Methods. 2014;11(8):783–784.
   PubMed Web of Science ®Google Scholar
• Langfelder K, Jahn B, Gehringer H, et al. Identification of a polyketide synthase gene (pksP) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence. Med Microbiol Immunol. 1998;187(2):79–89.
   PubMed Web of Science ®Google Scholar
• Krappmann S, Sasse C, Braus GH. Gene targeting in Aspergillus fumigatus by homologous recombination is facilitated in a nonhomologous end- joining-deficient genetic background. Eukaryot Cell. 2006;5(1):212–215.
   PubMedGoogle Scholar
• Beauvais A, Latge JP. Membrane and cell wall targets in Aspergillus fumigatus. Drug Resist Updat. 2001;4(1):38–49.
   PubMed Web of Science ®Google Scholar
• Beauvais A, Bruneau JM, Mol PC, et al. Glucan synthase complex of Aspergillus fumigatus. J Bacteriol. 2001;183(7):2273–2279.
   PubMed Web of Science ®Google Scholar
• Fontaine T, Simenel C, Dubreucq G, et al. Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem. 2000;275(52):41528.
   PubMed Web of Science ®Google Scholar
• Helmschrott C, Sasse A, Samantaray S, et al. Upgrading fungal gene expression on demand: improved systems for doxycycline-dependent silencing in Aspergillus fumigatus. Appl Environ Microbiol. 2013;79(5):1751–1754.
   PubMed Web of Science ®Google Scholar
• Santander SP, Aoki M, Hernandez JF, et al. Galactomannan from Caesalpinia spinosa induces phenotypic and functional maturation of human dendritic cells. Int Immunopharmacol. 2011;11(6):652–660.
   PubMed Web of Science ®Google Scholar
• Becker KL, Aimanianda V, Wang X, et al. Aspergillus cell wall chitin induces anti- and proinflammatory cytokines in human PBMCs via the Fc-gamma receptor/Syk/PI3K pathway. MBio. 2016;7(3).
   Web of Science ®Google Scholar