Abstract
Glycosylphosphatidylinositol (GPI) anchored proteins are a class of proteins attached to the extracellular leaflet of the plasma membrane via a post-translational modification, the glycolipid anchor. GPI anchored proteins are expressed in all eukaryotes, from fungi to plants and animals. They display very diverse functions ranging from enzymatic activity, signaling, cell adhesion, cell wall metabolism, and immune response. In this review, we investigated for the first time an exhaustive list of all the GPI anchored proteins present in the Aspergillus fumigatus genome. An A. fumigatus mutant library of all the genes that encode in silico identified GPI anchored proteins has been constructed and the phenotypic analysis of all these mutants has been characterized including their growth, conidial viability or morphology, adhesion and the ability to form biofilms. We showed the presence of different fungal categories of GPI anchored proteins in the A. fumigatus genome associated to their role in cell wall remodeling, adhesion, and biofilm formation.
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References
Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K, Elluru SR et al (2009) Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460:1117–1121
Aimanianda V, Simenel C, Garnaud C, Clavaud C, Tada R, Barbin L et al (2017) The dual activity responsible for the elongation and branching of β-(1,3)-glucan in the fungal cell wall. mBio 8. 8(3):e00619–17
Alcazar-Fuoli L, Clavaud C, Lamarre C, Aimanianda V, Seidl-Seiboth V, Mellado E, Latgé J-P (2011) Functional analysis of the fungal/plant class chitinase family in Aspergillus fumigatus. Fungal Genet Biol 48:418–429
Arroyo J, Farkaš V, Sanz AB, Cabib E (2016) Strengthening the fungal cell wall through chitin-glucan cross-links: effects on morphogenesis and cell integrity. Cell Microbiol 18:1239–1250
Beauvais A, Schmidt C, Guadagnini S, Roux P, Perret E, Henry C et al (2007) An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus. Cell Microbiol 9:1588–1600
Bernard M, Mouyna I, Dubreucq G, Debeaupuis J-P, Fontaine T, Vorgias C et al (2002) Characterization of a cell-wall acid phosphatase (PhoAp) in Aspergillus fumigatus. Microbiol 148:2819–2829
Blanco N, Reidy M, Arroyo J, Cabib E (2012) Crosslinks in the cell wall of budding yeast control morphogenesis at the mother-bud neck. J Cell Sci 125:5781–5789
Bruneau JM, Magnin T, Tagat E, Legrand R, Bernard M, Diaquin M et al (2001) Proteome analysis of Aspergillus fumigatus identifies glycosylphosphatidylinositol-anchored proteins associated to the cell wall biosynthesis. Electrophoresis 22:2812–2823
Cabib E, Farkas V, Kosík O, Blanco N, Arroyo J, McPhie P (2008) Assembly of the yeast cell wall. Crh1p and Crh2p act as transglycosylases in vivo and in vitro. J Biol Chem 283:29859–29872
Cao L, Chan CM, Lee C, Wong SS, Yuen KY (1998) MP1 encodes an abundant and highly antigenic cell wall mannoprotein in the pathogenic fungus Penicillium marneffei. Infect Immun 66:966–973
Cappellaro C, Mrsa V, Tanner W (1998) New potential cell wall glucanases of Saccharomyces cerevisiae and their involvement in mating. J Bacteriol 180:5030–5037
Caro LH, Tettelin H, Vossen JH, Ram AF, van den Ende H, Klis FM (1997) In silicio identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae. Yeast 13:1477–1489
Chabane S, Sarfati J, Ibrahim-Granet O, Du C, Schmidt C, Mouyna I et al (2006) Glycosylphosphatidylinositol-anchored Ecm33p influences conidial cell wall biosynthesis in Aspergillus fumigatus. Appl Environ Microbiol 72:3259–3267
Chong KTK, Woo PCY, Lau SKP, Huang Y, Yuen K (2004) AFMP2 encodes a novel immunogenic protein of the antigenic mannoprotein superfamily in Aspergillus fumigatus. J Clin Microbiol 42:2287–2291
Coluccio A, Bogengruber E, Conrad MN, Dresser ME, Briza P, Neiman AM (2004) Morphogenetic pathway of spore wall assembly in Saccharomyces cerevisiae. Eukaryot Cell 3:1464–1475
Eisenhaber B, Schneider G, Wildpaner M, Eisenhaber F (2004) A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. J Mol Biol 337:243–253
Fang W, Sanz AB, Bartual SG, Wang B, Ferenbach AT, Farkaš V et al (2019) Mechanisms of redundancy and specificity of the Aspergillus fumigatus Crh transglycosylases. Nat Commun 10:1669
Firon A, Aubert S, Iraqui I, Guadagnini S, Goyard S, Prévost M-C et al (2007) The SUN41 and SUN42 genes are essential for cell separation in Candida albicans. Mol Microbiol 66:1256–1275
Fontaine T, Simenel C, Dubreucq G, Adam O, Delepierre M, Lemoine J et al (2000) Molecular organization of the alkali-insoluble fraction of aspergillus fumigatus cell wall. J Biol Chem 275:41528
Fontaine T, Beauvais A, Loussert C, Thevenard B, Fulgsang CC, Ohno N et al (2010) Cell wall alpha1-3glucans induce the aggregation of germinating conidia of Aspergillus fumigatus. Fungal Genet Biol 47:707–712
Frieman MB, McCaffery JM, Cormack BP (2002) Modular domain structure in the Candida glabrata adhesin Epa1p, a beta1,6 glucan-cross-linked cell wall protein. Mol Microbiol 46:479–492
Furukawa T, van Rhijn N, Fraczek M, Gsaller F, Davies E, Carr P et al (2020) The negative cofactor 2 complex is a key regulator of drug resistance in Aspergillus fumigatus. Nat Commun 11:427
Gastebois A, Aimanianda V, Bachellier-Bassi S, Nesseir A, Firon A, Beauvais A et al (2013) SUN proteins belong to a novel family of β-(1,3)-glucan-modifying enzymes involved in fungal morphogenesis. J Biol Chem 288:13387–13396
Gastebois A, Fontaine T, Latgé J-P, Mouyna I (2010a) beta(1-3)Glucanosyltransferase Gel4p is essential for Aspergillus fumigatus. Eukaryot Cell 9:1294–1298
Gastebois A, Mouyna I, Simenel C, Clavaud C, Coddeville B, Delepierre M et al (2010b) Characterization of a new beta(1-3)-glucan branching activity of Aspergillus fumigatus. J Biol Chem 285:2386–2396
Hamada K, Terashima H, Arisawa M, Kitada K (1998) Amino acid sequence requirement for efficient incorporation of glycosylphosphatidylinositol-associated proteins into the cell wall of Saccharomyces cerevisiae. J Biol Chem 273:26946–26953
Hartl L, Gastebois A, Aimanianda V, Latgé J-P (2011) Characterization of the GPI-anchored endo β-1,3-glucanase Eng2 of Aspergillus fumigatus. Fungal Genet Biol 48:185–191
Hartland RP, Fontaine T, Debeaupuis JP, Simenel C, Delepierre M, Latgé JP (1996) A novel beta-(1-3)-glucanosyltransferase from the cell wall of Aspergillus fumigatus. J Biol Chem 271:26843–26849
Hiller E, Heine S, Brunner H, Rupp S (2007) Candida albicans Sun41p, a putative glycosidase, is involved in morphogenesis, cell wall biogenesis, and biofilm formation. Eukaryot Cell 6:2056–2065
Kapteyn JC, Hoyer LL, Hecht JE, Müller WH, Andel A, Verkleij AJ et al (2000) The cell wall architecture of Candida albicans wild-type cells and cell wall-defective mutants. Mol Microbiol 35:601–611
Kitagaki H, Wu H, Shimoi H, Ito K (2002) Two homologous genes, DCW1 (YKL046c) and DFG5, are essential for cell growth and encode glycosylphosphatidylinositol (GPI)-anchored membrane proteins required for cell wall biogenesis in Saccharomyces cerevisiae. Mol Microbiol 46:1011–1022
Korman DR, Bayliss FT, Barnett CC, Carmona CL, Kodama KH, Royer TJ et al (1990) Cloning, characterization, and expression of two alpha-amylase genes from Aspergillus niger var. awamori. Curr Genet 17:203–212
Kulkarni RD, Kelkar HS, Dean RA (2003) An eight-cysteine-containing CFEM domain unique to a group of fungal membrane proteins. Trends Biochem Sci 28:118–121
Latgé J-P, Beauvais A, Chamilos G (2017) The cell wall of the human fungal pathogen Aspergillus fumigatus: biosynthesis, organization, immune response, and virulence. Annu Rev Microbiol 71:99–116
Leidich SD, Ibrahim AS, Fu Y, Koul A, Jessup C, Vitullo J et al (1998) Cloning and disruption of caPLB1, a phospholipase B gene involved in the pathogenicity of Candida albicans. J Biol Chem 273:26078–26086
Levdansky E, Kashi O, Sharon H, Shadkchan Y, Osherov N (2010) The Aspergillus fumigatus cspA gene encoding a repeat-rich cell wall protein is important for normal conidial cell wall architecture and interaction with host cells. Eukaryot Cell 9:1403–1415
Lu CF, Kurjan J, Lipke PN (1994) A pathway for cell wall anchorage of Saccharomyces cerevisiae alpha-agglutinin. Mol Cell Biol 14:4825–4833
Millet N, Latgé J-P, Mouyna I (2018) Members of glycosyl-hydrolase family 17 of A. fumigatus differentially affect morphogenesis. J Fungi 4(1)
Monod M, Capoccia S, Léchenne B, Zaugg C, Holdom M, Jousson O (2002) Secreted proteases from pathogenic fungi. Int J Med Microbiol 292:405–419
Morita T, Tanaka N, Hosomi A, Giga-Hama Y, Takegawa K (2006) An alpha-amylase homologue, aah3, encodes a GPI-anchored membrane protein required for cell wall integrity and morphogenesis in Schizosaccharomyces pombe. Biosci Biotechnol Biochem 70:1454–1463
Mouyna I, Morelle W, Vai M, Monod M, Léchenne B, Fontaine T, Beauvais A, Sarfati J, Prévost MC, Henry C, Latgé JP (2005) Deletion of GEL2 encoding for a beta(1–3)glucanosyltransferase affects morphogenesis and virulence in Aspergillus fumigatus. Mol Microbiol 56:1675–1688
Mouyna I, Hartland RP, Fontaine T, Diaquin M, Simenel C, Delepierre M et al (1998) A 1,3- glucanosyltransferase isolated from the cell wall of Aspergillus fumigatus is a homologue of the yeast Bgl2p. Microbiology 144:3171–3180
Mouyna I, Fontaine T, Vai M, Monod M, Fonzi WA, Diaquin M et al (2000a) Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J Biol Chem 275:14882–14889
Mouyna I, Monod M, Fontaine T, Henrissat B, Léchenne B, Latgé JP (2000b) Identification of the catalytic residues of the first family of beta(1-3)glucanosyltransferases identified in fungi. Biochem J 347(Pt 3):741–747
Mouyna I, Aimanianda V, Hartl L, Prevost M-C, Sismeiro O, Dillies M-A et al (2016) GH16 and GH81 family β-(1,3)-glucanases in Aspergillus fumigatus are essential for conidial cell wall morphogenesis. Cell Microbiol 18:1285–1293
Mouyna I, Delliere S, Beauvais A, Gravelat F, Snarr B, Lehoux M et al (2020) What are the functions of chitin deacetylases in Aspergillus fumigatus? Front Cell Infect Microbiol 10:28
Muszkieta L, Fontaine T, Beau R, Mouyna I, Vogt MS, Trow J et al (2019) The glycosylphosphatidylinositol-anchored DFG family is essential for the insertion of galactomannan into the β-(1,3)-glucan-chitin core of the cell wall of Aspergillus fumigatus. mSphere 4:e00397–19
Norice CT, Smith FJ, Solis N, Filler SG, Mitchell AP (2007) Requirement for Candida albicans Sun41 in biofilm formation and virulence. Eukaryot Cell 6:2046–2055
Pérez A, Pedrós B, Murgui A, Casanova M, López-Ribot JL, Martínez JP (2006) Biofilm formation by Candida albicans mutants for genes coding fungal proteins exhibiting the eight-cysteine-containing CFEM domain. FEMS Yeast Res 6:1074–1084
Pérez A, Ramage G, Blanes R, Murgui A, Casanova M, Martínez JP (2011) Some biological features of Candida albicans mutants for genes coding fungal proteins containing the CFEM domain. FEMS Yeast Res 11:273–284
Pille A, Kwan AH, Cheung I, Hampsey M, Aimanianda V, Delepierre M et al (2015) (1)H, (13)C and (15)N resonance assignments of the RodA hydrophobin from the opportunistic pathogen Aspergillus fumigatus. Biomol NMR Assign 9:113–118
Plaine A, Walker L, Da Costa G, Mora-Montes HM, McKinnon A, Gow NAR et al (2008) Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet Biol 45:1404–1414
Popolo L, Vai M (1999) The Gas1 glycoprotein, a putative wall polymer cross-linker. Biochim Biophys Acta 1426:385–400
Popolo L, Degani G, Camilloni C, Fonzi WA (2017) The PHR family: the role of extracellular transglycosylases in shaping Candida albicans cells. J Fungi 3(4)
Rodríguez-Peña JM, Cid VJ, Arroyo J, Nombela C (2000) A novel family of cell wall-related proteins regulated differently during the yeast life cycle. Mol Cell Biol 20:3245–3255
Rolli E, Ragni E, de Medina-Redondo M, Arroyo J, de Aldana CRV, Popolo L (2011) Expression, stability, and replacement of glucan-remodeling enzymes during developmental transitions in Saccharomyces cerevisiae. Mol Biol Cell 22:1585–1598
Sestak S, Hagen I, Tanner W, Strahl S (2004) Scw10p, a cell-wall glucanase/transglucosidase important for cell-wall stability in Saccharomyces cerevisiae. Microbiology 150:3197–3208
Shen D-K, Noodeh AD, Kazemi A, Grillot R, Robson G, Brugère J-F (2004) Characterisation and expression of phospholipases B from the opportunistic fungus Aspergillus fumigatus. FEMS Microbiol Lett 239:87–93
Spreghini E, Davis DA, Subaran R, Kim M, Mitchell AP (2003) Roles of Candida albicans Dfg5p and Dcw1p cell surface proteins in growth and hypha formation. Eukaryot Cell 2:746–755
Vaknin Y, Shadkchan Y, Levdansky E, Morozov M, Romano J, Osherov N (2014) The three Aspergillus fumigatus CFEM-domain GPI-anchored proteins (CfmA-C) affect cell-wall stability but do not play a role in fungal virulence. Fungal Genet Biol 63:55–64
Valsecchi I, Dupres V, Stephen-Victor E, Guijarro JI, Gibbons J, Beau R et al (2017a) Role of hydrophobins in Aspergillus fumigatus. J Fungi 4(1):2
Valsecchi I, Sarikaya-Bayram Ö, Wong Sak Hoi J, Muszkieta L, Gibbons J, Prevost MC, Mallet A, Krijnse-Locker J, Ibrahim-Granet O, Mouyna I, Carr P, Bromley M, Aimanianda V, Yu JH, Rokas A, Braus GH, Saveanu C, Bayram Ö, Latgé JP (2017b) MybA, a transcription factor involved in conidiation and conidial viability of the human pathogen Aspergillus fumigatus. Mol Microbiol 105:880–900
van der Kaaij RM, Janeček Š, van der Maarel MJEC, Dijkhuizen L (2007a) Phylogenetic and biochemical characterization of a novel cluster of intracellular fungal alpha-amylase enzymes. Microbiol 153:4003–4015
van der Kaaij RM, Yuan X-L, Franken A, Ram AFJ, Punt PJ, van der Maarel MJEC, Dijkhuizen L (2007b) Two novel, putatively cell wall-associated and glycosylphosphatidylinositol-anchored alpha-glucanotransferase enzymes of Aspergillus niger. Eukaryot Cell 6:1178–1188
Van der Vaart JM, te Biesebeke R, Chapman JW, Toschka HY, Klis FM, Verrips CT (1997) Comparison of cell wall proteins of Saccharomyces cerevisiae as anchors for cell surface expression of heterologous proteins. Appl Environ Microbiol 63:615–620
Vickers I, Reeves EP, Kavanagh KA, Doyle S (2007) Isolation, activity and immunological characterisation of a secreted aspartic protease, CtsD, from Aspergillus fumigatus. Protein Expr Purif 53:216–224
Voltersen V, Blango MG, Herrmann S, Schmidt F, Heinekamp T, Strassburger M et al (2018) Proteome analysis reveals the conidial surface protein CcpA essential for virulence of the pathogenic fungus Aspergillus fumigatus. mBio 9(5)
Woo PCY, Chan C-M, Leung ASP, Lau SKP, Che X-Y, Wong SSY et al (2002) Detection of cell wall galactomannoprotein Afmp1p in culture supernatants of Aspergillus fumigatus and in sera of aspergillosis patients. J Clin Microbiol 40:4382–4387
Woo PCY, Lau SKP, Lau CCY, Tung ETK, Au-Yeung RKH, Cai J-P et al (2018) Mp1p homologues as virulence factors in Aspergillus fumigatus. Med Mycol 56:350–360
Woo PCY, Lau SKP, Lau CCY, Tung ETK, Chong KTK, Yang F et al (2016) Mp1p is a virulence factor in Talaromyces (Penicillium) marneffei. PLoS Negl Trop Dis 10:e0004907
Yuan X-L, van der Kaaij RM, van den Hondel CAMJJ, Punt PJ, van der Maarel MJEC, Dijkhuizen L, Ram AFJ (2008) Aspergillus niger genome-wide analysis reveals a large number of novel alpha-glucan acting enzymes with unexpected expression profiles. Mol Genet Genomics MGG 279:545–561
Yuen KY, Chan CM, Chan KM, Woo PC, Che XY, Leung AS, Cao L (2001) Characterization of AFMP1: a novel target for serodiagnosis of aspergillosis. J Clin Microbiol 39:3830–3837
Zhao C, Fraczek MG, Dineen L, Lebedinec R, Macheleidt J, Heinekamp T et al (2019) High-throughput gene replacement in Aspergillus fumigatus. Curr Protoc Microbiol 54:e88
Acknowledgements
This research was funded by l’Agence Nationale pour la Recherche (AfuInf ANR-16-CE92-0039), la Fondation pour la Recherche Médicale (DEQ 20150331722 LATGE Equipe FRM 2015) and the AIC (Action Incitative Ciblée) grant of Pasteur Institute. This work was also supported by the Wellcome trust grant 208396/Z/17/Z to MB.
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Samalova, M. et al. (2020). GPI Anchored Proteins in Aspergillus fumigatus and Cell Wall Morphogenesis. In: Latgé, JP. (eds) The Fungal Cell Wall . Current Topics in Microbiology and Immunology, vol 425. Springer, Cham. https://doi.org/10.1007/82_2020_207
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