Galactosaminogalactan, a new immunosuppressive polysaccharide of Aspergillus fumigatus

PLoS Pathogens

Volumn 7, Issue 11, 2011, Pages

  Fontaine, Thierry ^a   Delangle, Aurélie ^a   Simenel, Catherine ^a   Coddeville, Bernadette ^b   van Vliet, Sandra J ^c   van Kooyk, Yvette ^c   Bozza, Silvia ^d   Moretti, Silvia ^d   Schwarz, Flavio ^e   Trichot, Coline ^f   Aebi, Markus ^e   Delepierre, Muriel ^a   Elbim, Carole ^f   Romani, Luigina ^d   Latgé, Jean Paul ^a  

^a INSTITUT PASTEUR   (France)

^b UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF PERUGIA   (Italy)

^e ETH ZURICH   (Switzerland)

^f SORBONNE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; GALACTOSAMINOGALACTAN; GALACTOSE; GLYCAN; MONOSACCHARIDE; N ACETYLGALACTOSAMINE; OLIGOSACCHARIDE; POLYMER; POLYSACCHARIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN ANTIBODY REACTION; ANTIGENICITY; APOPTOSIS; ARTICLE; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; CAMPYLOBACTER JEJUNI; CARBOHYDRATE ANALYSIS; CONTROLLED STUDY; CROSS REACTION; FUNGUS; IMMUNOCOMPETENCE; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOCYTE;

ANIMALS; ANTIBODIES, FUNGAL; ANTIGENS, FUNGAL; APOPTOSIS; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; CARBOHYDRATE CONFORMATION; CARBOHYDRATE SEQUENCE; CELL WALL; CROSS REACTIONS; EPITOPES; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNOSUPPRESSIVE AGENTS; MACROPHAGES; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED C57BL; NEUTROPHIL INFILTRATION; NEUTROPHILS; POLYSACCHARIDES; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

ASPERGILLUS; ASPERGILLUS FUMIGATUS; CAMPYLOBACTER JEJUNI; MUS;

EID: 81755182989     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002372     Document Type: Article

References (62)

1. Morgan J, Wannemuehler KA, Marr KA, Hadley S, Kontoyiannis DP, et al. (2005) Incidence of invasive aspergillosis following hematopoietic stem cell and solid organ transplantation: interim results of a prospective multicenter surveillance program. Med Mycol 43 (Suppl 1): S49-58.
2. Singh N, Paterson DL, (2005) Aspergillus infections in transplant recipients. Clin Microbiol Rev 18: 44-69.
3. Brakhage AA, Bruns S, Thywissen A, Zipfel PF, Behnsen J, (2010) Interaction of phagocytes with filamentous fungi. Curr Opin Microbiol 13: 409-415.
4. Bozza S, Clavaud C, Giovannini G, Fontaine T, Beauvais A, et al. (2009) Immune sensing of Aspergillus fumigatus proteins, glycolipids, and polysaccharides and the impact on Th immunity and vaccination. J Immunol 183: 2407-2414.
5. Mouyna I, Fontaine T, (2009) Cell wall of Aspergillus fumigatus: a dynamic structure In: Latgé JP, Steinbach WJ, editors. Washington, D.C American Society for Microbiology pp. 169-183.
6. Netea MG, Brown GD, Kullberg BJ, Gow NA, (2008) An integrated model of the recognition of Candida albicans by the innate immune system. Nat Rev Microbiol 6: 67-78.
7. Romani L, Puccetti P, (2008) Immune regulation and tolerance to fungi in the lungs and skin. Chem Immunol Allergy 94: 124-137.
8. Rizzetto L, Cavalieri D, (2010) A systems biology approach to the mutual interaction between yeast and the immune system. Immunobiology 215: 762-769.
9. Zaragoza O, Rodrigues ML, De Jesus M, Frases S, Dadachova E, et al. (2009) The capsule of the fungal pathogen Cryptococcus neoformans. Adv Appl Microbiol 68: 133-216.
10. Beauvais A, Schmidt C, Guadagnini S, Roux P, Perret E, et al. (2007) An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus. Cell Microbiol 9: 1588-1600.
11. 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.
12. Latge JP, Kobayashi H, Debeaupuis JP, Diaquin M, Sarfati J, et al. (1994) Chemical and immunological characterization of the extracellular galactomannan of Aspergillus fumigatus. Infect Immun 62: 5424-5433.
13. Fontaine T, Simenel C, Dubreucq G, Adam O, Delepierre M, et al. (2000) Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem 275: 27594-27607.
14. Vinogradov E, Bock K, (1999) The structure of the core part of Proteus vulgaris OX2 lipopolysaccharide. Carbohydr Res 320: 239-243.
15. Young NM, Brisson JR, Kelly J, Watson DC, Tessier L, et al. (2002) Structure of the N-linked glycan present on multiple glycoproteins in the Gram-negative bacterium, Campylobacter jejuni. J Biol Chem 277: 42530-42539.
16. Francois S, El Benna J, Dang PM, Pedruzzi E, Gougerot-Pocidalo MA, et al. (2005) Inhibition of neutrophil apoptosis by TLR agonists in whole blood: involvement of the phosphoinositide 3-kinase/Akt and NF-kappaB signaling pathways, leading to increased levels of Mcl-1, A1, and phosphorylated Bad. J Immunol 174: 3633-3642.
17. Distler JJ, Roseman S, (1960) Galactosamine polymers produced by Aspergillus parasiticus. J Biol Chem 235: 2538-2541.
18. Reissig JL, Glasgow JE, (1971) Mucopolysaccharide which regulates growth in Neurospora. J Bacteriol 106: 882-889.
19. Bardalaye PC, Nordin JH, (1976) Galactosaminogalactan from cell walls of Aspergillus niger. J Bacteriol 125: 655-669.
20. Ruperez P, Leal JA, (1981) Extracelullar galactosaminogalactan from Aspergillus parasiticus. Trans Br Mycol Soc 77: 621-625.
21. Takada H, Araki Y, Ito E, (1981) Structure of polygalactosamine produced by Aspergillus parasiticus. J Biochem 89: 1265-1274.
22. Guerrero C, Prieto A, Leal JA, (1988) Extracellular galactosaminogalactan from Penicillium frequentans. Microbiologia 4: 39-46.
23. Costachel C, Coddeville B, Latge JP, Fontaine T, (2005) Glycosylphosphatidylinositol-anchored fungal polysaccharide in Aspergillus fumigatus. J Biol Chem 280: 39835-39842.
24. Scheller HV, Ulvskov P, (2010) Hemicelluloses. Annu Rev Plant Biol 61: 263-289.
25. Dutton GG, Savage AV, (1980) Structural investigation of the capsular polysaccharide of Klebsiella serotype K12. Carbohydr Res 83: 351-362.
26. Schneider P, Treumann A, Milne KG, McConville MJ, Zitzmann N, et al. (1996) Structural studies on a lipoarabinogalactan of Crithidia fasciculata. Biochem J 313 (Pt 3): 963-971.
27. Kol O, Wieruszeski JM, Strecker G, Fournet B, Zalisz R, et al. (1992) Structure of the O-specific polysaccharide chain of Klebsiella pneumoniae O1K2 (NCTC 5055) lipopolysaccharide. A complementary elucidation. Carbohydr Res 236: 339-344.
28. Moody SF, Handman E, McConville MJ, Bacic A, (1993) The structure of Leishmania major amastigote lipophosphoglycan. J Biol Chem 268: 18457-18466.
29. Leal JA, Prieto A, Bernabe M, Hawksworth DL, (2010) An assessment of fungal wall heteromannans as a phylogenetically informative character in ascomycetes. FEMS Microbiol Rev 34: 986-1014.
30. Lamarre C, Beau R, Balloy V, Fontaine T, Wong Sak Hoi J, et al. (2009) Galactofuranose attenuates cellular adhesion of Aspergillus fumigatus. Cell Microbiol 11: 1612-1623.
31. Letscher-Bru V, Cavalier A, Pernot-Marino E, Koenig H, Eyer D, et al. (1998) Aspergillus galactomannan antigen detection with Platelia-Aspergillus: multiple positive antigemia without Aspergillus infection. J Mycol Med 8: 112-113.
32. Gangneux JP, Lavarde D, Bretagne S, Guiguen C, Gandemer V, (2002) Transient aspergillus antigenaemia: think of milk. Lancet 359: 1251.
33. Szymanski CM, Burr DH, Guerry P, (2002) Campylobacter protein glycosylation affects host cell interactions. Infect Immun 70: 2242-2244.
34. Karlyshev AV, Everest P, Linton D, Cawthraw S, Newell DG, et al. (2004) The Campylobacter jejuni general glycosylation system is important for attachment to human epithelial cells and in the colonization of chicks. Microbiology 150: 1957-1964.
35. Geijtenbeek TB, Gringhuis SI, (2009) Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol 9: 465-479.
36. van de Veerdonk FL, Kullberg BJ, van der Meer JW, Gow NA, Netea MG, (2008) Host-microbe interactions: innate pattern recognition of fungal pathogens. Curr Opin Microbiol 11: 305-312.
37. Levitz SM, (2010) Innate recognition of fungal cell walls. PLoS Pathog 6: e1000758.
38. Pericolini E, Cenci E, Monari C, De Jesus M, Bistoni F, et al. (2006) Cryptococcus neoformans capsular polysaccharide component galactoxylomannan induces apoptosis of human T-cells through activation of caspase-8. Cell Microbiol 8: 267-275.
39. Villena SN, Pinheiro RO, Pinheiro CS, Nunes MP, Takiya CM, et al. (2008) Capsular polysaccharides galactoxylomannan and glucuronoxylomannan from Cryptococcus neoformans induce macrophage apoptosis mediated by Fas ligand. Cell Microbiol 10: 1274-1285.
40. 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: 368-381.
41. Toyotome T, Adachi Y, Watanabe A, Ochiai E, Ohno N, et al. (2008) Activator protein 1 is triggered by Aspergillus fumigatus beta-glucans surface-exposed during specific growth stages. Microb Pathog 44: 141-150.
42. van Vliet SJ, van Liempt E, Saeland E, Aarnoudse CA, Appelmelk B, et al. (2005) Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. Int Immunol 17: 661-669.
43. van Vliet SJ, Paessens LC, Broks-van den Berg VC, Geijtenbeek TB, van Kooyk Y, (2008) The C-type lectin macrophage galactose-type lectin impedes migration of immature APCs. J Immunol 181: 3148-3155.
44. van Vliet SJ, Steeghs L, Bruijns SC, Vaezirad MM, Snijders Blok C, et al. (2009) Variation of Neisseria gonorrhoeae lipooligosaccharide directs dendritic cell-induced T helper responses. PLoS Pathog 5: e1000625.
45. van Sorge NM, Bleumink NM, van Vliet SJ, Saeland E, van der Pol WL, et al. (2009) N-glycosylated proteins and distinct lipooligosaccharide glycoforms of Campylobacter jejuni target the human C-type lectin receptor MGL. Cell Microbiol 11: 1768-1781.
46. Cobb BA, Wang Q, Tzianabos AO, Kasper DL, (2004) Polysaccharide processing and presentation by the MHCII pathway. Cell 117: 677-687.
47. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F, (1956) Colorimetric methods for determination of sugars and related substances. Anal Chem 28: 350-356.
48. Johnson AR, (1971) Improved method of hexosamine determination. Anal Biochem 44: 628-635.
49. Sawardeker JS, Sloneker JH, Jeanes A, (1965) Quantitative determination of monosaccharides as their alditol acetates by gas liquid chromatography. Anal Chem 37: 1602-1604.
50. Fontaine T, Talmont F, Dutton GG, Fournet B, (1991) Analysis of pyruvic acid acetal containing polysaccharides by methanolysis and reductive cleavage methods. Anal Biochem 199: 154-161.
51. Ciucanu I, Kerek F, (1984) A simple and rapid method for permethylation of carbohydrates. Carbohydr Res 131: 209-217.
52. Wishart DS, Bigam CG, Yao J, Abildgaard F, Dyson HJ, et al. (1995) 1H, 13C and 15N chemical shift referencing in biomolecular NMR. J Biomol NMR 6: 135-140.
53. Wagner G, (1983) Two-dimensional relayed coherence transfer spectroscopy of a protein. J Magn Reson 55: 151-156.
54. Willker W, Leibfritz D, Kerssebaum R, Bermel W, (1993) Gradient selection in inverse heteronuclear correlation spectroscopy. Magn Reson Chem 31: 287-292.
55. Macura S, Huang Y, Suter D, Ernst R R, (1981) Two-dimensional chemical exchange and cross-relaxation spectroscopy of coupled nuclear spins. J Magn Reson 43: 259-281.
56. Wacker M, Linton D, Hitchen PG, Nita-Lazar M, Haslam SM, et al. (2002) N-linked glycosylation in Campylobacter jejuni and its functional transfer into E. coli. Science 298: 1790-1793.
57. Kowarik M, Young NM, Numao S, Schulz BL, Hug I, et al. (2006) Definition of the bacterial N-glycosylation site consensus sequence. Embo J 25: 1957-1966.
58. Nato F, Reich K, Lhopital S, Rouyre S, Geoffroy C, et al. (1991) Production and characterization of neutralizing and nonneutralizing monoclonal antibodies against listeriolysin O. Infect Immun 59: 4641-4646.
59. 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.
60. Romani L, Bistoni F, Perruccio K, Montagnoli C, Gaziano R, et al. (2006) Thymosin alpha1 activates dendritic cell tryptophan catabolism and establishes a regulatory environment for balance of inflammation and tolerance. Blood 108: 2265-2274.
61. Zelante T, De Luca A, Bonifazi P, Montagnoli C, Bozza S, et al. (2007) IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur J Immunol 37: 2695-2706.
62. Fournet B, Strecker G, Leroy Y, Montreuil J, (1981) Gas-liquid chromatography and mass spectrometry of methylated and acetylated methyl glycosides. Application to the structural analysis of glycoprotein glycans. Anal Biochem 116: 489-502.