Deletion of the α-(1,3)-Glucan Synthase Genes Induces a Restructuring of the Conidial Cell Wall Responsible for the Avirulence of

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α-(1,3)-Glucan is a major component of the cell wall of Aspergillus fumigatus, an opportunistic human fungal pathogen. There are three genes (AGS1, AGS2 and AGS3) controlling the biosynthesis of α-(1,3)-glucan in this fungal species. Deletion of all the three AGS genes resulted in a triple mutant that was devoid of α-(1,3)-glucan in its cell wall; however, its growth and germination was identical to that of the parental strain in vitro. In the experimental murine aspergillosis model, this mutant was less pathogenic than the parental strain. The AGS deletion resulted in an extensive structural modification of the conidial cell wall, especially conidial surface where the rodlet layer was covered by an amorphous glycoprotein matrix. This surface modification was responsible for viability reduction of conidia in vivo, which explains decrease in the virulence of triple agsΔ mutant.

Vyšlo v časopise: Deletion of the α-(1,3)-Glucan Synthase Genes Induces a Restructuring of the Conidial Cell Wall Responsible for the Avirulence of. PLoS Pathog 9(11): e32767. doi:10.1371/journal.ppat.1003716
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1003716

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Zdroje

1. RappleyeCA, EissenbergLG, GoldmanWE (2007) Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor. 2007 104: 1366–1370.

2. ReeseAJ, YonedaA, BregerJA, BeauvaisA, LiuH, et al. (2007) Loss of cell wall alpha(1–3) glucan affects Cryptococcus neoformans from ultrastructure to virulence. Mol Microbiol 63: 1385–1398.

3. MaubonD, ParkS, TanguyM, HuerreM, SchmittC, et al. (2006) AGS3, an alpha(1–3)glucan synthase gene family member of Aspergillus fumigatus, modulates mycelium growth in the lung of experimentally infected mice. Fungal Genet Biol 43: 366–375.

4. BeauvaisA, SchmidtC, GuadagniniS, RouxP, PerretE, et al. (2007) An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus. Cell Microbiol 9: 1588–1600.

5. FontaineT, BeauvaisA, LoussertC, ThevenardB, FulgsangCC, et al. (2010) Cell wall alpha1-3glucans induce the aggregation of germinating conidia of Aspergillus fumigatus. Fungal Genet Biol 47: 707–712.

6. BozzaSC, Cecile (2009) GiovanniniGloria (2009) FontaineThierry (2009) BeauvaisAnne (2009) SarfatiJacqueline (2009) et al. Immune sensing of Aspergillus fumigatus proteins, glycolipids and polysaccharides and the impact on Th immunity and vaccination. The Journal of Immunology 183: 2407–2414.

7. BeauvaisA, MaubonD, ParkS, MorelleW, TanguyM, et al. (2005) Two alpha(1–3) glucan synthases with different functions in Aspergillus fumigatus. Appl Environ Microbiol 71: 1531–1538.

8. HenryC, LatgeJP, BeauvaisA (2012) alpha1,3 glucans are dispensable in Aspergillus fumigatus. Eukaryot Cell 11: 26–29.

9. DagueE, DelcorteA, LatgeJP, DufreneYF (2008) Combined use of atomic force microscopy, X-ray photoelectron spectroscopy, and secondary ion mass spectrometry for cell surface analysis. Langmuir 24: 2955–2959.

10. AimaniandaV, BayryJ, BozzaS, KniemeyerO, PerruccioK, et al. (2009) Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460: 1117–1121.

11. LambouK, LamarreC, BeauR, DufourN, LatgeJP (2010) Functional analysis of the superoxide dismutase family in Aspergillus fumigatus. Mol Microbiol 75: 910–923.

12. MorelleW, BernardM, DebeaupuisJP, BuitragoM, TabouretM, et al. (2005) Galactomannoproteins of Aspergillus fumigatus. Eukaryot Cell 4: 1308–1316.

13. MonodM, CapocciaS, LechenneB, ZauggC, HoldomM, et al. (2002) Secreted proteases from pathogenic fungi. Int J Med Microbiol 292: 405–419.

14. SinghB, OellerichM, KumarR, KumarM, BhadoriaDP, et al. (2010) Immuno-reactive molecules identified from the secreted proteome of Aspergillus fumigatus. J Proteome Res 9: 5517–5529.

15. PhilippeB, Ibrahim-GranetO, PrevostMC, Gougerot-PocidaloMA, Sanchez PerezM, et al. (2003) Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infect Immun 71: 3034–3042.

16. BayryJ, AimaniandaV, GuijarroJI, SundeM, LatgeJP (2012) Hydrophobins–unique fungal proteins. PLoS Pathog 8: e1002700.

17. SriranganadaneD, WaridelP, SalaminK, ReichardU, GrouzmannE, et al. (2010) Aspergillus protein degradation pathways with different secreted protease sets at neutral and acidic pH. J Proteome Res 9: 3511–3519.

18. WangZ, LienemannM, QiauM, LinderMB (2010) Mechanisms of protein adhesion on surface films of hydrophobin. Langmuir 26: 8491–8496.

19. Jimenez-OrtigosaC, AimaniandaV, MuszkietaL, MouynaI, AlsteensD, et al. (2012) Chitin synthases with a myosin motor-like domain control the resistance of Aspergillus fumigatus to echinocandins. Antimicrob Agents Chemother 56: 6121–6131.

20. AlsteensD, AimaniandaV, HegdeP, PireS, BeauR, et al. (2013) Unraveling the Nanoscale Surface Properties of Chitin Synthase Mutants of Aspergillus fumigatus and Their Biological Implications. Biophys J 105(2): 320–7.

21. HoganLH, KleinBS (1994) Altered expression of surface alpha-1,3-glucan in genetically related strains of Blastomyces dermatitidis that differ in virulence. Infect Immun 62: 3543–3546.

22. RappleyeCA, GoldmanGH (2006) Defining virulence genes in the dimorphing fungi. Ann Rev Microbiol 60: 281–303.

23. McDonaldJU, RosasM, BrownGD, JonesSA, TaylorPR (2012) Differential dependencies of monocytes and neutrophils on dectin-1, dectin-2 and complement for the recognition of fungal particles in inflammation. PLoS One 7: e45781.

24. HohlTM, FeldmesserM, PerlinDS, PamerEG (2008) Caspofungin modulates inflammatory responses to Aspergillus fumigatus through stage-specific effects on fungal beta-glucan exposure. J Infect Dis 198: 176–185.

25. LamarisGA, LewisRE, ChamilosG, MayGS, SafdarA, et al. (2008) Caspofungin-mediated beta-glucan unmasking and enhancement of human polymorphonuclear neutrophil activity against Aspergillus and non-Aspergillus hyphae. J Infect Dis 198: 186–192.

26. LatgeJP (2010) Tasting the fungal cell wall. Cell Microbiol 12: 863–872.

27. FeriottiC, LouresFV, Frank de AraujoE, da CostaTA, CalichVL (2013) Mannosyl-recognizing receptors induce an M1-like phenotype in macrophages of susceptible mice but an M2-like phenotype in mice resistant to a fungal infection. PLoS One 8: e54845.

28. FujikawaT, SakaguchiA, NishizawaY, KouzaiY, MinamiE, et al. (2012) Surface alpha-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants. PLoS Pathog 8: e1002882.

29. RoilidesE, Dimitriadou-GeorgiadouA, SeinT, KadiltsoglouI, WalshTJ (1998) Tumor necrosis factor alpha enhances antifungal activities of polymorphonuclear and mononuclear phagocytes against Aspergillus fumigatus. Infect Immun 66: 5999–6003.

30. RoilidesE, UhligK, VenzonD, PizzoPA, WalshTJ (1993) Enhancement of oxidative response and damage caused by human neutrophils to Aspergillus fumigatus hyphae by granulocyte colony-stimulating factor and gamma interferon. Infect Immun 61: 1185–1193.

31. HenrietSS, HermansPW, VerweijPE, SimonettiE, HollandSM, et al. (2011) Human leukocytes kill Aspergillus nidulans by reactive oxygen species-independent mechanisms. Infect Immun 79: 767–773.

32. ZaremberKA, SuguiJA, ChangYC, Kwon-ChungKJ, GallinJI (2007) Human polymorphonuclear leukocytes inhibit Aspergillus fumigatus conidial growth by lactoferrin-mediated iron depletion. J Immunol 178: 6367–6373.

33. D'AngeloC, De LucaA, ZelanteT, BonifaziP, MorettiS, et al. (2009) Exogenous pentraxin 3 restores antifungal resistance and restrains inflammation in murine chronic granulomatous disease. J Immunol 183: 4609–4618.

34. KaurS, GuptaVK, ThielS, SarmaPU, MadanT (2007) Protective role of mannan-binding lectin in a murine model of invasive pulmonary aspergillosis. Clin Exp Immunol 148: 382–389.

35. MoalliF, DoniA, DebanL, ZelanteT, ZagarellaS, et al. (2010) Role of complement and Fc{gamma} receptors in the protective activity of the long pentraxin PTX3 against Aspergillus fumigatus. Blood 116: 5170–5180.

36. SpethC, RambachG (2012) Complement Attack against Aspergillus and Corresponding Evasion Mechanisms. Interdiscip Perspect Infect Dis 2012: 463794.

37. ZhangS, FanY, XiaYX, KeyhaniNO (2010) Sulfonylurea resistance as a new selectable marker for the entomopathogenic fungus Beauveria bassiana. Appl Microbiol Biotechnol 87: 1151–1156.

38. ClavaudC, BeauvaisA, BarbinL, Munier-LehmannH, LatgeJP (2012) The composition of the culture medium influences the beta-1,3-glucan metabolism of Aspergillus fumigatus and the antifungal activity of inhibitors of beta-1,3-glucan synthesis. Antimicrob Agents Chemother 56: 3428–3431.

39. ShethCC, HallR, LewisL, BrownAJ, OddsFC, et al. (2011) Glycosylation status of the C. albicans cell wall affects the efficiency of neutrophil phagocytosis and killing but not cytokine signaling. Med Mycol 49: 513–524.

40. ShalerCR, HorvathC, LaiR, XingZ (2012) Understanding delayed T-cell priming, lung recruitment, and airway luminal T-cell responses in host defense against pulmonary tuberculosis. Clin Dev Immunol 2012: 628293.

41. SvirshchevskayaEV, ShevchenkoMA, HuetD, FemeniaF, LatgeJP, et al. (2009) Susceptibility of mice to invasive aspergillosis correlates with delayed cell influx into the lungs. Int J Immunogenet 36: 289–299.

42. BrianPW, DawkinsAW, GroveJF, HemmingHG, LoweD, et al. (1961) Phytotoxic compounds produced by Fusarium equiseti. J Exper Bot 12: 1–12.

43. da Silva FerreiraME, KressMR, SavoldiM, GoldmanMH, HartlA, et al. (2006) The akuB(KU80) mutant deficient for nonhomologous end joining is a powerful tool for analyzing pathogenicity in Aspergillus fumigatus. Eukaryot Cell 5: 207–211.

44. MouynaI, KniemeyerO, JankT, LoussertC, MelladoE, et al. (2010) Members of PMT family in Aspergillus fumigatus differentially affect growth, morphogenesis, and viability. Mol Microbiol 76: 1205–1221.

45. KlimpelKR, GoldmanWE (1988) Cell walls from avirulent variants of Histoplasma capsulatum lack alpha-(1,3)-glucan. Infect Immun 56: 2997–3000.

46. HarrisSD, MorrellJL, HamerJE (1994) Identification and characterization of Aspergillus nidulans mutants defective in cytokinesis. Genetics 136: 517–532.

47. DagueE, JauvertE, LaplatineL, VialletB, ThibaultC, et al. (2011) Assembly of live micro-organisms on microstructured PDMS stamps by convective/capillary deposition for AFM bio-experiments. Nanotechnology 22: 395102.

48. HutterS, HeinritziK, ReichE, EhretW (1993) [Effects of different methods of tooth resection in suckling piglets]. Tierarztl Prax 21: 417–428.

49. BradfordM (1976) A rapide and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. . Anal Biochem 72: 248–254.

50. KniemeyerO, LessingF, ScheibnerO, HertweckC, BrakhageAA (2006) Optimisation of a 2-D gel electrophoresis protocol for the human-pathogenic fungus Aspergillus fumigatus. Curr Genet 49: 178–189.

51. CandianoG, BruschiM, MusanteL, SantucciL, GhiggeriGM, et al. (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327–1333.

52. LamarreC, BeauR, BalloyV, FontaineT, Wong Sak HoiJ, et al. (2009) Galactofuranose attenuates cellular adhesion of Aspergillus fumigatus. Cell Microbiol 11: 1612–1623.

53. FontaineT, DelangleA, SimenelC, CoddevilleB, van VlietSJ, et al. (2011) Galactosaminogalactan, a new immunosuppressive polysaccharide of Aspergillus fumigatus. PLoS Pathog 7: e 1002372.

54. StynenD, SarfatiJ, GorisA, PrevostMC, LesourdM, et al. (1992) Rat monoclonal antibodies against Aspergillus galactomannan. Infect Immun 60: 2237–2245.

55. MishimaY, QuintinJ, AimaniandaV, KellenbergerC, CosteF, et al. (2009) The N-terminal domain of Drosophila Gram-negative binding protein 3 (GNBP3) defines a novel family of fungal pattern recognition receptors. J Biol Chem 284: 28687–28697.

56. TakagiI, YamadaK, SatoT, HanaichiT, IwamotoT, et al. (1990) J Electron Microsc (Tokyo) 39: 67–68.

57. BonifaziP, D'AngeloC, ZagarellaS, ZelanteT, BozzaS, et al. (2010) Intranasally delivered siRNA targeting P13K/Akt/mTOR inflammatory pathways protects from aspergillosis. Mucosal Immnunol 3: 193–205.

58. BozzaS, PerruccioK, MontagnoliC, GazianoR, BellocchioS, et al. (2003) A dendritic cell vaccine against invasive aspergillosis in allogeneic hematopoietic transplantation. Blood 102: 3807–3814.

59. SturtevantJ, LatgeJP (1992) Participation of complement in the phagocytosis of the conidia of Aspergillus fumigatus by human polymorphonuclear cells. J Infect Dis 166: 580–586.