Abstract
The cell wall provides physical strength to cells and defines the morphology of fungi. During hyphal development of filamentous fungi, the apical region and the branching sites of the cell are remodeled to support hyphal extension and formation of a new hypha. The cell wall has contact with the environment and thus is the place of first contact with external stresses originating outside of the cells. The cell wall also acts as a matrix for various extracellular proteins such as enzymes and sensor proteins. Budding yeast (Saccharomyces cerevisiae) and filamentous fungi (Aspergillus species) are industrially and medically important fungi belonging to the Ascomycota. These fungi share similar composition in the cell wall although they are morphologically different. Fungal cell walls are usually composed of glucose, mannose, N-acetyl-d-glucosamine, proteins, and lipids. Some glycans composed of galactofuranose or N-acetyl-d-galactosamine are found characteristically in the cell wall of Aspergillus species. In this chapter, we present an overview of current knowledge on cell wall biogenesis and wall-stress sensing in fungi, particularly focusing on recent findings in filamentous fungi.
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References
Afroz S, El-Ganiny AM, Sanders DA, Kaminskyj SG (2011) Roles of the Aspergillus nidulans UDP-galactofuranose transporter, UgtA in hyphal morphogenesis, cell wall architecture, conidiation, and drug sensitivity. Fungal Genet Biol 48:896–903
Akiyama H (2010) Sake: the essence of 2000 years of Japanese wisdom gained from brewing alcoholic beverages from rice. Brewing Society of Japan, Tokyo
Alberts AS, Bouquin N, Johnston LH, Treisman R (1998) Analysis of RhoA-binding proteins reveals an interaction domain conserved in heterotrimeric G protein β subunits and the yeast response regulator protein Skn7. J Biol Chem 273:8616–8622
Bakker H, Kleczka B, Gerardy-Schahn R, Routier FH (2005) Identification and partial characterization of two eukaryotic UDP-galactopyranose mutases. Biol Chem 386:657–661
Beauvais A, Bozza S, Kniemeyer O et al (2013) Deletion of the α-(1,3)-glucan synthase genes induces a restructuring of the conidial cell wall responsible for the avirulence of Aspergillus fumigatus. PLoS Pathog 9(11):e1003716. doi:10.1371/journal.ppat.1003716
Cabib E (2009) Two novel techniques for determination of polysaccharide cross-links show that Crh1p and Crh2p attach chitin to both β(1-6)- and β(1-3) glucan in the Saccharomyces cerevisiae cell wall. Eukaryot Cell 8:1626–1636
Costachel C, Coddeville B, Latgé JP, Fontaine T (2005) Glycosylphosphatidylinositol-anchored fungal polysaccharide in Aspergillus fumigatus. J Biol Chem 280:39835–39842
Cruz S, Muñoz S, Manjón E et al (2013) The fission yeast cell wall stress sensor-like proteins Mtl2 and Wsc1 act by turning on the GTPase Rho1p but act independently of the cell wall integrity pathway. Microbiol Open 2:778–794
Dähn U, Hagenmaier H, Höhne H et al. (1976) Stoffwechselprodukte von mikroorganismen. 154. Mitteilung. Nikkomycin, ein neuer hemmstoff der chitinsynthese bei pilzen. Arch Microbiol 107:143–160
Damveld RA, Franken A, Arentshorst M et al (2008) A novel screening method for cell wall mutants in Aspergillus niger identifies UDP-galactopyranose mutase as an important protein in fungal cell wall biosynthesis. Genetics 178:873–881
De Groot PWJ, Ram AF, Klis FM (2005) Features and functions of covalently linked proteins in fungal cell walls. Fungal Genet Biol 42:657–675
Deshpande N, Wilkins MR, Packer N et al (2008) Protein glycosylation pathways in filamentous fungi. Glycobiology 8:626–637
Dichtl K, Helmschrott C, Dirr F, Wagener J (2012) Deciphering cell wall integrity signaling in Aspergillus fumigatus: identification and functional characterization of cell wall stress sensors and relevant Rho GTPases. Mol Microbiol 83:506–519
Dupres V, Alsteens D, Wilk S et al (2009) The yeast Wsc1 cell surface sensor behaves like a nanospring in vivo. Nat Chem Biol 5:857–862
El-Ganiny AM, Sanders DA, Kaminskyj SG et al (2008) Aspergillus nidulans UDP-galactopyranose mutase, encoded by ugmA plays key roles in colony growth, hyphal morphogenesis, and conidiation. Fungal Genet Biol 45:1533–1542
El-Ganiny AM, Sheoran I, Sanders DA, Kaminskyj SG (2010) Aspergillus nidulans UDP-glucose-4-epimerase UgeA has multiple roles in wall architecture, hyphal morphogenesis, and asexual development. Fungal Genet Biol 47:629–635
Endo A, Misato T (1969) Polyoxin D, a competitive inhibitor of UDP-N-acetylglucosamine: Chitin N-acetylglucosaminyltransferase in Neurospora crassa. Biochem Biophys Res Commun 37:718–722
Engel J, Schmalhorst PS, Dörk-Bousset T et al (2009) A single UDP-galactofuranose transporter is required for galactofuranosylation in Aspergillus fumigatus. J Biol Chem 284:33859–33868
Farkaš V (1985) The fungal cell wall. In: Peberdy JF, Ferenczy L (eds) Fungal protoplasts. Dekker, New York, pp 3–29
Fontaine T, Simenel C, Dubreucq G et al (2000) Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem 275:27594–27607
Fontaine T, Delangle A, Simenel C et al (2011) Galactosaminogalactan, a new immunosuppressive polysaccharide of Aspergillus fumigatus. PLoS Pathog 7:e1002372
Fujioka T, Mizutani O, Furukawa K et al (2007) MpkA-dependent and -independent cell wall integrity signaling in Aspergillus nidulans. Eukaryot Cell 6:1497–1510
Furukawa K, Yoshimi A, Furukawa T et al (2007) Novel reporter gene expression systems for monitoring activation of the Aspergillus nidulans HOG pathway. Biosci Biotechnol Biochem 71:1724–1730
Futagami T, Goto M (2012) Putative cell wall integrity sensor proteins in Aspergillus nidulans. Commun Integr Biol 5:206–208
Futagami T, Nakao S, Kido Y et al (2011) Putative stress sensors WscA and WscB are involved in hypo-osmotic and acidic pH stress tolerance in Aspergillus nidulans. Eukaryot Cell 10:1504–1515
Futagami T, Seto K, Kajiwara Y et al (2014) The putative stress sensor protein MtlA is required for conidia formation, cell wall stress tolerance, and cell wall integrity in Aspergillus nidulans. Biosci Biotechnol Biochem. doi:10.1080/09168451.2014.878218
Goto M (2007) Protein O-glycosylation in fungi: diverse structures and multiple functions. Biosci Biotechnol Biochem 6:1415–1427
Goto M, Harada Y, Oka T et al (2009) Protein O-mannosyltransferases B and C support hyphal development and differentiation in Aspergillus nidulans. Eukaryot Cell 10:1465–1474
Gravelat FN, Beauvais A, Liu H et al (2013) Aspergillus galactosaminogalactan mediates adherence to host constituents and conceals hyphal β-glucan from the immune system. PLoS Pathog 9:e1003575
Heinisch JJ, Dupres V, Wilk S et al (2010) Single-molecule atomic force microscopy reveals clustering of the yeast plasma-membrane sensor Wsc1. PLoS One 5:e11104
Horiuchi H (2009) Functional diversity of chitin synthases of Aspergillus nidulans in hyphal growth, conidiophore development and septum formation. Med Mycol. doi:10.1080/13693780802213332
Hutzler F, Gerstl R, Lommel M, Strahl S (2008) Protein N-glycosylation determines functionality of the Saccharomyces cerevisiae cell wall integrity sensor Mid2p. Mol Microbiol 68:1438–1449
Jigami Y (2008) Yeast glycobiology and its application. Biosci Biotechnol Biochem 3:637–648
Klis FM, De Groot P, Hellingwerf K (2001) Molecular organization of the cell wall of Candida albicans. Med Mycol 39:1–8
Komachi Y, Hatakeyama S, Motomatsu H et al (2013) GfsA encodes a novel galactofuranosyltransferase involved in biosynthesis of galactofuranose antigen of O-glycan in Aspergillus nidulans and Aspergillus fumigatus. Mol Microbiol 90:1054–1073
Kovács Z, Szarka M, Kovács S et al (2013) Effect of cell wall integrity stress and RlmA transcription factor on asexual development and autolysis in Aspergillus nidulans. Fungal Genet Biol 54:1–14
Kriangkripipat T, Momany M (2009) Aspergillus nidulans protein O-mannosyltransferases play roles in cell wall integrity and developmental patterning. Eukaryot Cell 8:1475–1485
Kurita T, Noda Y, Takagi T et al (2011) Kre6 protein essential for yeast cell wall β-1,6-glucan synthesis accumulates at sites of polarized growth. J Biol Chem 286:7429–7438
Lamarre C, Ibrahim-Granet O, Du C et al (2007) Characterization of the SKN7 ortholog of Aspergillus fumigatus. Fungal Genet Biol 44:682–690
Lambou K, Perkhofer S, Fontaine T et al (2010) Comparative functional analysis of the OCH1 mannosyltransferase families in Aspergillus fumigatus and Saccharomyces cerevisiae. Yeast 8:625–636
Latgé JP, Kobayashi H, Debeaupuis JP et al (1994) Chemical and immunological characterization of the extracellular galactomannan of Aspergillus fumigatus. Infect Immun 62:5424–5433
Latgé JP, Mouyna I, Tekaia F et al (2005) Specific molecular features in the organization and biosynthesis of the cell wall of Aspergillus fumigatus. Med Mycol 43:15–22
Lee MJ, Gravelat FN, Cerone RP et al (2014) Overlapping and distinct roles of Aspergillus fumigatus UDP-glucose 4-epimerases in galactose metabolism and the synthesis of galactose-containing cell wall polysaccharides. J Biol Chem 289:1243–1256
Leitao EA, Bittencourt VC, Haido RM et al (2003) β-Galactofuranose-containing O-linked oligosaccharides present in the cell wall peptidogalactomannan of Aspergillus fumigatus contain immunodominant epitopes. Glycobiology 13:681–692
Levin DE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189:1145–1175
Levin DE, Bartlett-Heubusch E (1992) Mutants in the S. cerevisiae PKC1 gene display a cell cycle-specific osmotic stability defect. J Cell Biol 116:1221–1229
Lommel M, Bagnat M, Strahl S (2004) Aberrant processing of the WSC family and Mid2p cell surface sensors results in cell death of Saccharomyces cerevisiae O-mannosylation mutants. Mol Cell Biol 24:46–57
Maras M, van Die I, Contreras R et al (1990) Filamentous fungi as production organisms for glycoproteins of bio-medical interest. Glycoconj J 16:99–107
Mouyna I, Kniemeyer O, Jank T et al (2010) Members of protein O-mannosyltransferase family in Aspergillus fumigatus differentially affect growth, morphogenesis and viability. Mol Microbiol 76:1205–1221
Mouyna I, Hartl L, Latgé JP (2013) β-1,3-Glucan modifying enzymes in Aspergillus fumigatus. Front Microbiol 4:81. doi:10.3389/fmicb.2013.00081
Nikolaou E, Agrafioti I, Stumpf M et al (2009) Phylogenetic diversity of stress signalling pathways in fungi. BMC Evol Biol 9:44
Oka T, Hamaguchi T, Sameshima Y et al (2004) Molecular characterization of protein O-mannosyltransferase and its involvement in cell-wall synthesis in Aspergillus nidulans. Microbiology 6:1973–1982
Orchard MG, Neuss JC, Galley CM, et al. (2004) Rhodanine-3-acetic acid derivatives as inhibitors of fungal protein mannosyl transferase 1 (PMT1). Bioorg Med Chem Lett 14:3975–3978
Osherov N, Yarden O (2010) The cell wall of filamentous fungi. In: Borkovich KA, Ebbole DJ (eds) Cellular and molecular biology of filamentous fungi. ASM, Washington, pp 224–237
Rajavel M, Philip B, Buehrer BM et al (1999) Mid2 is a putative sensor for cell integrity signaling in Saccharomyces cerevisiae. Mol Cell Biol 19:3969–3976
Reinoso-MartÃn C, Schuller C, Schuetzer-Muehlbauer M, Kuchler K (2003) The yeast protein kinase C cell integrity pathway mediates tolerance to the antifungal drug caspofungin through activation of Slt2p mitogen-activated protein kinase signaling. Eukaryot Cell 2:1200–1210. doi:10.1128/EC.2.6.1200-1210.2003
Rispail N, Soanes DM, Ant C et al (2009) Comparative genomics of MAP kinase and calcium-calcineurin signalling components in plant and human pathogenic fungi. Fungal Genet Biol 46:287–298
Rodicio R, Buchwald U, Schmitz HP, Heinisch JJ (2008) Dissecting sensor functions in cell wall integrity signaling in Kluyveromyces lactis. Fungal Genet Biol 45:422–435
Ruiz-Herrera J (2012) Fungal cell wall, structure, synthesis, and assembly. CRC, Boca Raton
Saito H, Posas F (2012) Response to hyperosmotic stress. Genetics 192:289–318
Samantaray S, Neubauer M, Helmschrott C, Wagener J (2013) Role of the guanine nucleotide exchange factor Rom2 in cell wall integrity maintenance of Aspergillus fumigatus. Eukaryot Cell 12:288–298
Schmalhorst PS, Krappmann S, Vervecken W et al (2008) Contribution of galactofuranose to the virulence of the opportunistic pathogen Aspergillus fumigatus. Eukaryot Cell 7:1268–1277
Serrano R, Martin H, Casamayor A, Arino J (2006) Signaling alkaline pH stress in the yeast Saccharomyces cerevisiae through the Wsc1 cell surface sensor and the Slt2 MAPK pathway. J Biol Chem 281:39785–39795
Straede A, Heinisch JJ (2007) Functional analyses of the extra- and intracellular domains of the yeast cell wall integrity sensors Mid2 and Wsc1. FEBS Lett 581:4495–4500
Takeshita N, Yamashita S, Ohta A et al (2006) Aspergillus nidulans class V and VI chitin synthases CsmA and CsmB, each with a myosin motor-like domain, perform compensatory functions that are essential for hyphal tip growth. Mol Microbiol 59:1380–1394
Tsuizaki M, Ohta A, Horiuchi H (2013) Myosin motor-like domain of class VI chitin synthase CsmB of Aspergillus nidulans is not functionally equivalent to that of class V chitin synthase CsmA. Biosci Biotechnol Biochem 77:369–374
Wallis GL, Easton RL, Jolly K et al (2001) Galactofuranoic-oligomannose N-linked glycans of alpha-galactosidase A from Aspergillus niger. Eur J Biochem 268:4134–4143
Walsh TJ, Giri N (1997) Pradimicins: a novel class of broad-spectrum antifungal compounds. Eur J Clin Microbiol Infect Dis 16:93–97
Willer T, Valero MC, Tanner W et al (2003) O-Mannosyl glycans: from yeast to novel associations with human disease. Curr Opin Struct Biol 13:621–630
Yoshimi A, Sano M, Inaba A et al (2013) Functional analysis of the α-1,3-glucan synthase genes agsA and agsB in Aspergillus nidulans: agsB is the major α-1,3-glucan synthase in this fungus. PLoS One 8(1):e54893. doi:10.1371/journal.pone.0054893
Zhou H, Hu H, Zhang L et al (2007) O-Mannosyltransferase 1 in Aspergillus fumigatus (AfPmt1p) is crucial for cell wall integrity and conidium morphology, especially at an elevated temperature. Eukaryot Cell 6:2260–2268
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Oka, T., Futagami, T., Goto, M. (2015). Cell Wall Biosynthesis in Filamentous Fungi. In: Takagi, H., Kitagaki, H. (eds) Stress Biology of Yeasts and Fungi. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55248-2_10
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DOI: https://doi.org/10.1007/978-4-431-55248-2_10
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