FleA Expression in Aspergillus fumigatus Is Recognized by Fucosylated Structures on Mucins and Macrophages to Prevent Lung Infection

PLoS Pathogens

Volumn 12, Issue 4, 2016, Pages

  Kerr, Sheena C ^a   Fischer, Gregory J ^b   Sinha, Meenal ^c   McCabe, Orla ^d   Palmer, Jonathan M ^b   Choera, Tsokyi ^b   Yun Lim, Fang ^b   Wimmerova, Michaela ^e   Carrington, Stephen D ^d   Yuan, Shaopeng ^a   Lowell, Clifford A ^c   Oscarson, Stefan ^d   Keller, Nancy P ^b   Fahy, John V ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY COLLEGE DUBLIN   (Ireland)

^e MASARYK UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

FUCOSE; FUCOSE BINDING LECTIN PROTEIN; FUCOSYLTRANSFERASE; LECTIN; MUCIN; UNCLASSIFIED DRUG; FUCOSE-BINDING LECTIN; FUNGAL PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASPERGILLUS FUMIGATUS; CARBOHYDRATE SYNTHESIS; CONIDIUM; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; FUCOSYLATION; FUNGAL STRAIN; HUMAN; IMMUNOFLUORESCENCE; LUNG INFECTION; MACROPHAGE; MALE; MOUSE; NONHUMAN; NORMAL HUMAN; PHAGOCYTOSIS; PHYLOGENY; PROTEIN LOCALIZATION; SOUTHERN BLOTTING; SPUTUM ANALYSIS; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; FUNGUS SPORE; IMMUNOLOGY; LUNG ASPERGILLOSIS; METABOLISM; MIDDLE AGED; MUCOSAL IMMUNITY; PATHOGENICITY;

ADULT; ANIMALS; ASPERGILLUS FUMIGATUS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; FUCOSE; FUNGAL PROTEINS; HUMANS; IMMUNITY, MUCOSAL; LECTINS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; MUCINS; PULMONARY ASPERGILLOSIS; SPORES, FUNGAL;

EID: 84964862371     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1005555     Document Type: Article

References (44)

1. Dagenais TR, Keller NP, Pathogenesis of Aspergillus fumigatus in Invasive Aspergillosis. Clinical Microbiology Reviews. 2009;22(3):447–65. doi: 10.1128/CMR.00055-0819597008
2. Bhatia S, Fei M, Yarlagadda M, Qi Z, Akira S, Saijo S, et al. Rapid host defense against Aspergillus fumigatus involves alveolar macrophages with a predominance of alternatively activated phenotype. PLoS One. 2011;6(1):e15943. doi: 10.1371/journal.pone.001594321246055
3. Dubourdeau M, Athman R, Balloy V, Huerre M, Chignard M, Philpott DJ, et al. Aspergillus fumigatus induces innate immune responses in alveolar macrophages through the MAPK pathway independently of TLR2 and TLR4. J Immunol. 2006;177(6):3994–4001. 16951362
4. Philippe B, Ibrahim-Granet O, Prevost MC, Gougerot-Pocidalo MA, Sanchez Perez M, Van der Meeren A, et al. Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infection and Immunity. 2003;71(6):3034–42. 12761080
5. Saijo S, Iwakura Y, Dectin-1 and Dectin-2 in innate immunity against fungi. International Immunology. 2011;23(8):467–72. doi: 10.1093/intimm/dxr04621677049
6. Luther K, Torosantucci A, Brakhage AA, Heesemann J, Ebel F, Phagocytosis of Aspergillus fumigatus conidia by murine macrophages involves recognition by the Dectin-1 β-glucan receptor and Toll-like receptor 2. Cellular Microbiology. 2007;9(2):368–81. 16953804
7. Underhill DM, Toll-like receptors and microbes take aim at each other. Curr Opin Immunol. 2004;16(4):483–7. 15245743
8. Willment JA, Brown GD, C-type lectin receptors in antifungal immunity. Trends in Microbiology. 2008;16(1):27–32. 18160296
9. Slesiona S, Gressler M, Mihlan M, Zaehle C, Schaller M, Barz D, et al. Persistence versus escape: Aspergillus terreus and Aspergillus fumigatus employ different strategies during interactions with macrophages. PLoS One. 2012;7(2):e31223. doi: 10.1371/journal.pone.003122322319619
10. Gilboa-Garber N, Pseudomonas aeruginosa lectins. Methods Enzymol. 1982;83:378–85. 6808301
11. Kostlanova N, Mitchell EP, Lortat-Jacob H, Oscarson S, Lahmann M, Gilboa-Garber N, et al. The fucose-binding lectin from Ralstonia solanacearum. A new type of β-propeller architecture formed by oligomerization and interacting with fucoside, fucosyllactose, and plant xyloglucan. J Biol Chem. 2005;280(30):27839–49. 15923179
12. Ramphal R, Arora SK, Recognition of mucin components by Pseudomonas aeruginosa. Glycoconj J. 2001;18(9):709–13. 12386456
13. Sulak O, Cioci G, Delia M, Lahmann M, Varrot A, Imberty A, et al. A TNF-like trimeric lectin domain from Burkholderia cenocepacia with specificity for fucosylated human histo-blood group antigens. Structure. 2010;18(1):59–72.: doi: 10.1016/j.str.2009.10.02120152153.
14. Zinger-Yosovich K, Sudakevitz D, Imberty A, Garber NC, Gilboa-Garber N, Production and properties of the native Chromobacterium violaceum fucose-binding lectin (CV-IIL) compared to homologous lectins of Pseudomonas aeruginosa (PA-IIL) and Ralstonia solanacearum (RS-IIL). Microbiology. 2006;152(Pt 2):457–63. 16436433
15. Fukumori F, Takeuchi N, Hagiwara T, Ohbayashi H, Endo T, Kochibe N, et al. Primary structure of a fucose-specific lectin obtained from a mushroom, Aleuria aurantia. Journal of Biochemistry. 1990;107(2):190–6. 2193930
16. Ishida H, Moritani T, Hata Y, Kawato A, Suginami K, Abe Y, et al. Molecular cloning and overexpression of fleA gene encoding a fucose-specific lectin of Aspergillus oryzae. Bioscience, Biotechnology, and Biochemistry. 2002;66(5):1002–8. 12092808.
17. Matsumura K, Higashida K, Hata Y, Kominami J, Nakamura-Tsuruta S, Hirabayashi J, Comparative analysis of oligosaccharide specificities of fucose-specific lectins from Aspergillus oryzae and Aleuria aurantia using frontal affinity chromatography. Anal Biochem. 2009;386(2):217–21. doi: 10.1016/j.ab.2008.11.04419109923
18. Houser J, Komarek J, Kostlanova N, Cioci G, Varrot A, Kerr SC, et al. A soluble fucose-specific lectin from Aspergillus fumigatus conidia—structure, specificity and possible role in fungal pathogenicity. PLoS One. 2013;8(12):e83077. doi: 10.1371/journal.pone.008307724340081
19. Wimmerova M, Mitchell E, Sanchez JF, Gautier C, Imberty A, Crystal structure of fungal lectin: six-bladed β-propeller fold and novel fucose recognition mode for Aleuria aurantia lectin. J Biol Chem. 2003;278(29):27059–67. 12732625
20. Houser J, Komarek J, Cioci G, Varrot A, Imberty A, Wimmerova M, Structural insights into Aspergillus fumigatus lectin specificity: AFL binding sites are functionally non-equivalent. Acta Crystallogr D Biol Crystallogr. 2015;71(Pt 3):442–53. doi: 10.1107/S139900471402659525760594
21. Audfray A, Claudinon J, Abounit S, Ruvoen-Clouet N, Larson G, Smith DF, et al. Fucose-binding lectin from opportunistic pathogen Burkholderia ambifaria binds to both plant and human oligosaccharidic epitopes. J Biol Chem. 2012;287(6):4335–47. doi: 10.1074/jbc.M111.31483122170069
22. Rose MC, Mucins: structure, function, and role in pulmonary diseases. Am J Physiol. 1992;263(4 Pt 1):L413–29. 1415719
23. Thornton DJ, Rousseau K, McGuckin MA, Structure and function of the polymeric mucins in airways mucus. Annu Rev Physiol. 2008;70:459–86. 17850213
24. Xu X, Padilla MT, Li B, Wells A, Kato K, Tellez C, et al. MUC1 in macrophage: contributions to cigarette smoke-induced lung cancer. Cancer Research. 2014;74(2):460–70. doi: 10.1158/0008-5472.CAN-13-171324282280
25. Roy MG, Livraghi-Butrico A, Fletcher AA, McElwee MM, Evans SE, Boerner RM, et al. Muc5b is required for airway defence. Nature. 2014;505(7483):412–6. doi: 10.1038/nature1280724317696
26. Kim KC, Role of epithelial mucins during airway infection. Pulmonary Pharmacology & Therapeutics. 2012;25(6):415–9.
27. Petersen TN, Brunak S, von Heijne G, Nielsen H, SignalP 4.0: discriminating signal peptides from transmembrane regions. Nature Methods. 2011;8(10):785–6. doi: 10.1038/nmeth.170121959131
28. Bouckaert J, Berglund J, Schembri M, De Genst E, Cools L, Wuhrer M, et al. Receptor binding studies disclose a novel class of high-affinity inhibitors of the Escherichia coli FimH adhesin. Molecular Microbiology. 2005;55(2):441–55. 15659162
29. Bouchara JP, Sanchez M, Chevailler A, Marot-Leblond A, Lissitzky JC, Tronchin G, et al. Sialic acid-dependent recognition of laminin and fibrinogen by Aspergillus fumigatus conidia. Infection and Immunity. 1997;65(7):2717–24. 9199441
30. Bromley IM, Donaldson K, Binding of Aspergillus fumigatus spores to lung epithelial cells and basement membrane proteins: relevance to the asthmatic lung. Thorax. 1996;51(12):1203–9. 8994516
31. Tronchin G, Bouchara JP, Larcher G, Lissitzky JC, Chabasse D, Interaction between Aspergillus fumigatus and basement membrane laminin: binding and substrate degradation. Biology of the cell / under the auspices of the European Cell Biology Organization. 1993;77(2):201–8. 8364400
32. Wasylnka JA, Moore MM, Adhesion of Aspergillus species to extracellular matrix proteins: evidence for involvement of negatively charged carbohydrates on the conidial surface. Infection and immunity. 2000;68(6):3377–84. 10816488
33. Bonnett CR, Cornish EJ, Harmsen AG, Burritt JB, Early neutrophil recruitment and aggregation in the murine lung inhibit germination of Aspergillus fumigatus conidia. Infection and Immunity. 2006;74(12):6528–39. 16920786
34. Cunha C, Kurzai O, Loffler J, Aversa F, Romani L, Carvalho A, Neutrophil responses to aspergillosis: new roles for old players. Mycopathologia. 2014;178(5–6):387–93. doi: 10.1007/s11046-014-9796-725106756
35. Taylor PR, Tsoni SV, Willment JA, Dennehy KM, Rosas M, Findon H, et al. Dectin-1 is required for β-glucan recognition and control of fungal infection. Nat Immunol. 2007;8(1):31–8. 17159984
36. Hohl TM, Van Epps HL, Rivera A, Morgan LA, Chen PL, Feldmesser M, et al. Aspergillus fumigatus triggers inflammatory responses by stage-specific β-glucan display. PLoS Pathogens. 2005;1(3):e30. 16304610
37. Carrion Sde J, Leal SM, Jr.Ghannoum MA, Aimanianda V, Latge JP, Pearlman E, The RodA hydrophobin on Aspergillus fumigatus spores masks Dectin-1- and Dectin-2-dependent responses and enhances fungal survival in vivo. J Immunol. 2013;191(5):2581–8. doi: 10.4049/jimmunol.130074823926321
38. Gersuk GM, Underhill DM, Zhu L, Marr KA, Dectin-1 and TLRs permit macrophages to distinguish between different Aspergillus fumigatus cellular states. J Immunol. 2006;176(6):3717–24. 16517740
39. Peters MC, Mekonnen ZK, Yuan S, Bhakta NR, Woodruff PG, Fahy JV, Measures of gene expression in sputum cells can identify TH2-high and TH2-low subtypes of asthma. J Allergy Clin Immunol. 2014;133(2):388–94. doi: 10.1016/j.jaci.2013.07.03624075231
40. Kerr SC, Carrington SD, Oscarson S, Gallagher ME, Solon M, Yuan S, et al. Intelectin-1 is a prominent protein constituent of pathologic mucus associated with eosinophilic airway inflammation in asthma. Am J Respir Crit Care Med. 2014;189(8):1005–7. doi: 10.1164/rccm.201312-2220LE24735037
41. Royle L, Matthews E, Corfield A, Berry M, Rudd PM, Dwek RA, et al. Glycan structures of ocular surface mucins in man, rabbit and dog display species differences. Glycoconj J. 2008;25(8):763–73. doi: 10.1007/s10719-008-9136-618465222
42. Lemieux RU, Hendriks KB, Stick RV, James K, Halide ion catalyzed glycosidation reactions. Synthesis of α-linked disaccharides. Journal of the American Chemical Society. 1975;97:4056–62.
43. Shimizu K, Keller NP, Genetic involvement of a cAMP-dependent protein kinase in a G protein signaling pathway regulating morphological and chemical transitions in Aspergillus nidulans. Genetics. 2001;157(2):591–600. 11156981
44. Chang PK, Scharfenstein LL, Wei Q, Bhatnagar D, Development and refinement of a high-efficiency gene-targeting system for Aspergillus flavus. Journal of Microbiological Methods. 2010;81(3):240–6. doi: 10.1016/j.mimet.2010.03.01020298723