A Polysaccharide Virulence Factor from Aspergillus fumigatus Elicits Anti-inflammatory Effects through Induction of Interleukin-1 Receptor Antagonist

PLoS Pathogens

Volumn 10, Issue 3, 2014, Pages

  Gresnigt, Mark S ^a   Bozza, Silvia ^b   Becker, Katharina L ^a   Joosten, Leo A B ^a   Abdollahi Roodsaz, Shahla ^a   van der Berg, Wim B ^a   Dinarello, Charles A ^a,c   Netea, Mihai G ^a   Fontaine, Thierry ^d   De Luca, Antonella ^b   Moretti, Silvia ^b   Romani, Luigina ^b   Latge, Jean Paul ^d   van de Veerdonk, Frank L ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF PERUGIA   (Italy)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 5; INTERLEUKIN 6; INTERLEUKIN 8; INTERLEUKIN 9; TUMOR NECROSIS FACTOR ALPHA; VIRULENCE FACTOR;

ALLERGY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; CELL STIMULATION; COLITIS; CONTROLLED STUDY; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; HISTOPATHOLOGY; IMMUNOMODULATION; INFLAMMATORY DISEASE; MOUSE; MYCOSIS; NONHUMAN;

ANIMALS; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; CYTOKINES; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FUNGAL POLYSACCHARIDES; HUMANS; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; LEUKOCYTES, MONONUCLEAR; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; POLYSACCHARIDES; VIRULENCE FACTORS;

EID: 84897373901     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003936     Document Type: Article

References (35)

1. Chai LY, Hsu LY, (2011) Recent advances in invasive pulmonary aspergillosis. Curr Opin Pulm Med 17: 160-166.
2. Romani L, (2011) Immunity to fungal infections. Nat Rev Immunol 11: 275-288.
3. Chai LY, Netea MG, Vonk AG, Kullberg BJ, (2009) Fungal strategies for overcoming host innate immune response. Med Mycol 47: 227-236.
4. Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K, et al. (2009) Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460: 1117-1121.
5. Chai LY, Netea MG, Sugui J, Vonk AG, van de Sande WW, et al. (2010) Aspergillus fumigatus conidial melanin modulates host cytokine response. Immunobiology 215: 915-920.
6. Chai LY, Kullberg BJ, Vonk AG, Warris A, Cambi A, et al. (2009) Modulation of Toll-like receptor 2 (TLR2) and TLR4 responses by Aspergillus fumigatus. Infect Immun 77: 2184-2192.
7. Fontaine T, Delangle A, Simenel C, Coddeville B, van Vliet SJ, et al. (2011) Galactosaminogalactan, a new immunosuppressive polysaccharide of Aspergillus fumigatus. PLoS Pathog 7: e1002372.
8. Loussert C, Schmitt C, Prevost MC, Balloy V, Fadel E, et al. (2010) In vivo biofilm composition of Aspergillus fumigatus. Cell Microbiol 12: 405-410.
9. Gravelat FN, Beauvais A, Liu H, Lee MJ, Snarr BD, et al. (2013) Aspergillus Galactosaminogalactan Mediates Adherence to Host Constituents and Conceals Hyphal beta-Glucan from the Immune System. PLoS Pathog 9: e1003575.
10. Sheppard DC, (2011) Molecular mechanism of Aspergillus fumigatus adherence to host constituents. Curr Opin Microbiol 14: 375-379.
11. Guo L, Wei G, Zhu J, Liao W, Leonard WJ, et al. (2009) IL-1 family members and STAT activators induce cytokine production by Th2, Th17, and Th1 cells. Proc Natl Acad Sci U S A 106: 13463-13468.
12. Ben-Sasson SZ, Hu-Li J, Quiel J, Cauchetaux S, Ratner M, et al. (2009) IL-1 acts directly on CD4 T cells to enhance their antigen-driven expansion and differentiation. Proc Natl Acad Sci U S A 106: 7119-7124.
13. Dinarello CA, (2011) Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 117: 3720-3732.
14. van de Veerdonk FL, Netea MG, Dinarello CA, van der Meer JW, (2011) Anakinra for the inflammatory complications of chronic granulomatous disease. Neth J Med 69: 95.
15. Groux H, O′Garra A, Bigler M, Rouleau M, Antonenko S, et al. (1997) A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389: 737-742.
16. Glocker EO, Kotlarz D, Klein C, Shah N, Grimbacher B, (2011) IL-10 and IL-10 receptor defects in humans. Ann N Y Acad Sci 1246: 102-107.
17. van de Veerdonk FL, Netea MG, Dinarello CA, Joosten LA, (2011) Inflammasome activation and IL-1beta and IL-18 processing during infection. Trends Immunol 32: 110-116.
18. Sainz J, Perez E, Gomez-Lopera S, Jurado M, (2008) IL1 gene cluster polymorphisms and its haplotypes may predict the risk to develop invasive pulmonary aspergillosis and modulate C-reactive protein level. J Clin Immunol 28: 473-485.
19. Werner JL, Metz AE, Horn D, Schoeb TR, Hewitt MM, et al. (2009) Requisite role for the dectin-1 beta-glucan receptor in pulmonary defense against Aspergillus fumigatus. J Immunol 182: 4938-4946.
20. Marr KA, Carter RA, Boeckh M, Martin P, Corey L, (2002) Invasive aspergillosis in allogeneic stem cell transplant recipients: changes in epidemiology and risk factors. Blood 100: 4358-4366.
21. Schaffner A, Douglas H, Braude A, (1982) Selective protection against conidia by mononuclear and against mycelia by polymorphonuclear phagocytes in resistance to Aspergillus. Observations on these two lines of defense in vivo and in vitro with human and mouse phagocytes. J Clin Invest 69: 617-631.
22. Koenders MI, Devesa I, Marijnissen RJ, Abdollahi-Roodsaz S, Boots AM, et al. (2008) Interleukin-1 drives pathogenic Th17 cells during spontaneous arthritis in interleukin-1 receptor antagonist-deficient mice. Arthritis Rheum 58: 3461-3470.
23. Aksentijevich I, Masters SL, Ferguson PJ, Dancey P, Frenkel J, et al. (2009) An autoinflammatory disease with deficiency of the interleukin-1-receptor antagonist. N Engl J Med 360: 2426-2437.
24. Lilly LM, Gessner MA, Dunaway CW, Metz AE, Schwiebert L, et al. (2012) The beta-Glucan Receptor Dectin-1 Promotes Lung Immunopathology during Fungal Allergy via IL-22. J Immunol 189(7): 3653-60.
25. Dinarello CA, Simon A, van der Meer JW, (2012) Treating inflammation by blocking interleukin-1 in a broad spectrum of diseases. Nat Rev Drug Discov 11: 633-652.
26. Chai LY, van de Veerdonk F, Marijnissen RJ, Cheng SC, Khoo AL, et al. (2010) Anti-Aspergillus human host defence relies on type 1 T helper (Th1), rather than type 17 T helper (Th17), cellular immunity. Immunology 130: 46-54.
27. Netea MG, Warris A, Van der Meer JW, Fenton MJ, Verver-Janssen TJ, et al. (2003) Aspergillus fumigatus evades immune recognition during germination through loss of toll-like receptor-4-mediated signal transduction. J Infect Dis 188: 320-326.
28. van de Veerdonk FL, Marijnissen RJ, Kullberg BJ, Koenen HJ, Cheng SC, et al. (2009) The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe 5: 329-340.
29. Gearing AJ, Bird CR, Bristow A, Poole S, Thorpe R, (1987) A simple sensitive bioassay for interleukin-1 which is unresponsive to 10(3) U/ml of interleukin-2. J Immunol Methods 99: 7-11.
30. Bonifazi P, D′Angelo C, Zagarella S, Zelante T, Bozza S, et al. (2010) Intranasally delivered siRNA targeting PI3K/Akt/mTOR inflammatory pathways protects from aspergillosis. Mucosal Immunol 3: 193-205.
31. Bozza S, Perruccio K, Montagnoli C, Gaziano R, Bellocchio S, et al. (2003) A dendritic cell vaccine against invasive aspergillosis in allogeneic hematopoietic transplantation. Blood 102: 3807-3814.
32. Takedatsu H, Michelsen KS, Wei B, Landers CJ, Thomas LS, et al. (2008) TL1A (TNFSF15) regulates the development of chronic colitis by modulating both T-helper 1 and T-helper 17 activation. Gastroenterology 135: 552-567.
33. Engel MA, Leffler A, Niedermirtl F, Babes A, Zimmermann K, et al. (2011) TRPA1 and substance P mediate colitis in mice. Gastroenterology 141: 1346-1358.
34. Bellocchio S, Moretti S, Perruccio K, Fallarino F, Bozza S, et al. (2004) TLRs govern neutrophil activity in aspergillosis. J Immunol 173: 7406-7415.
35. You Y, Richer EJ, Huang T, Brody SL, (2002) Growth and differentiation of mouse tracheal epithelial cells: selection of a proliferative population. Am J Physiol Lung Cell Mol Physiol 283: L1315-1321.