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Structure and biosynthesis of fungal cell walls: Methodological approaches

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Abstract

Fungal cell walls possess a characteristic chemical composition differentiating fungal cells from other cell types. For this reason, the mechanisms involved in cell-wall formation represent a potential target for selective antifungal drugs. Understanding the structure and biosynthesis of fungal cell walls opens the ways for design of effective drugs for treating fungal diseases. This article reviews the history methods employed in chemical and structural analysis of fungal cell walls and in studies concerning their formation.

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References

  • Adams A.E.M., Pringle J.R.: Relationship of actin and tubulin distribution to bud growth in wild-type and morphogenetic-mutantSaccharomyces cerevisiae.J.Cell Biol. 98, 934–945 (1984).

    Article  PubMed  CAS  Google Scholar 

  • Algranati I.D., Carminatti H., Cabib E.: The enzymic synthesis of yeast mannan.Biochem.Biophys.Res.Commun. 12, 504–509 (1963).

    Article  PubMed  CAS  Google Scholar 

  • Arnold W.N.: Physical aspects of yeast cell envelope, pp. 25–47 in W.N. Arnold (Ed.):Yeast Cell Envelopes: Biochemistry, Biophysics and Ultrastructure. CRC Press, Boca Raton (USA) 1981.

    Google Scholar 

  • Aronson J.M.: The cell wall, pp. 49–76 in G.C. Ainsworth, A.S. Sussman (Eds):The Fungi — an Advanced Treatise. Vol. 1. Academic Press, New York-London 1965.

    Google Scholar 

  • Aronson J.M., Preston R.D.: An electron microscopic and X-ray analysis of the walls of selectedPhycomycetes.Proc.Roy.Soc.London B152, 346–352 (1960).

    Google Scholar 

  • Ballou L., Cohen R.E., Ballou C.E.:Saccharomyces cerevisiae mutants that make mannoproteins with a truncated carbohydrate outer chain.J.Biol.Chem. 255, 5986–5991 (1980).

    PubMed  CAS  Google Scholar 

  • Bartnicki-Garcia S.: Cell wall chemistry, morphogenesis and taxonomy of fungi.Ann.Rev.Microbiol. 22, 87–108 (1968).

    Article  CAS  Google Scholar 

  • Bartnicki-Garcia S., Lippman E.: Fungal morphogenesis: cell wall construction inMucor rouxii.Science 165, 302–304 (1969).

    Article  PubMed  CAS  Google Scholar 

  • Bartnicki-Garcia S., Nickerson W.J.: Isolation, composition, and cell wall structure of filamentous and yeast-like forms ofMucor rouxii.Biochim.Biophys.Acta 58, 102–119 (1962).

    Article  PubMed  CAS  Google Scholar 

  • Beauvais A., Latge J.-P.: Membrane and cell wall targets inAspergillus fumigatus.Drug Resist.Updates 4, 38–49 (2001).

    Article  CAS  Google Scholar 

  • Botstein D., Amberg D., Mulholland J., Huffaker T., Adams A., Drubin D., Stearns T.: The yeast cytoskeleton, pp. 1–90 in J.R. Pringle, J.R. Broach, E.W. Jones (Eds):The Molecular and Cellular Biology of the Yeast Saccharomyces: Cell Cycle and Cell Biology, Vol. 3. Cold Spring Harbor Press, New York 1997.

    Google Scholar 

  • Cabib E., Roh D.-H., Schmidt M., Crotti L., Varma A.: The yeast cell wall and septum as paradigms of cell growth and morphogenesis.J.Biol.Chem. 276, 19679–19682 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Callewaert N., Geysens S., Molemans F., Contreras R.: Ultrasensitive profiling and sequencing of N-linked oligosaccharides using standard DNA-sequencing equipment.Glycobiology 11, 275–281 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Caro L.H.P., Tettelin H., Vossen J.H., Ram A.F.J., van den Ende H., Klis F.M.:In silicio identification of glycosyl-phosphatidyl-inositol-anchored plasma membrane and wall proteins ofSaccharomyces cerevisiae.Yeast 13, 1447–1489 (1997).

    Article  Google Scholar 

  • Catley B.J.: Isolation and analysis of cell walls, pp. 163–183 in D. Campbell, J.H. Duffus (Eds):Yeast a Practical Approach. Oxford University Press, Oxford (UK) 1989.

    Google Scholar 

  • Crotti L.B., Drgon T., Cabib E.: Yeast cell permeabilization by osmotic shock allows determination of enzymatic activitiesin situ.Anal.Biochem. 292, 8–16 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Dallies N., Francois J., Paquet V.: A new method for quantitative determination of polysaccharides in the yeast cell wall. Application to the cell wall defective mutants ofSaccharomyces cerevisiae.Yeast 14, 1297–1306 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Dische Z.: Color reactions of carbohydrates, pp. 475–514 in R.L. Whistler, M.K. Wolfrom (Eds):Methods in Carbohydrate Chemistry, Vol. 1. Academic Press, New York 1958.

    Google Scholar 

  • Douglas C.M., Foor F., Marrinan J.A., Morin N., Nielsen J.B., Dahl A.M., Mazur P., Baginsky W., Li W., El-Sherbeini M., Clemas J.A., Mandala S.M., Frommer B.R., Kurtz M.B.: TheSaccharomyces cerevisiae FKS1 (ETG1) gene encodes an integral membrane protein which is a subunit of 1,3-β-d-glucan synthase.Proc.Nat.Acad.Sci.USA 91, 12907–12911 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Drgoňová J., Drgoň T., Tanaka K., Kollár R., Chen G.-C., Ford R.A., Chan C.S.M., Takai Y., Cabib E.: Rho1p, a yeast protein at the interface between cell polarization and morphogenesis.Science 272, 277–279 (1996).

    Article  PubMed  Google Scholar 

  • Dubois M., Gilles K.A., Hamilton J.K., Rebers P.A., Smith F.: Colorimetric method for determination of sugars and related substances.Anal.Chem. 28, 350–356 (1956).

    Article  CAS  Google Scholar 

  • Duran A., Bowers B., Cabib E.: Chitin synthetase zymogen is attached to yeast plasma membrane.Proc.Nat.Acad.Sci.USA 72, 3952–3955 (1975).

    Article  PubMed  CAS  Google Scholar 

  • Farkaš V., Svoboda A., Bauer Š.: Secretion of cell wall glycoproteins by yeast protoplasts. The effect of 2-deoxy-d-glucose and cycloheximide.Biochem.J. 118, 755–758 (1970).

    PubMed  Google Scholar 

  • Farkaš V., Kovařík J., Košinová A., Bauer Š.: Autoradiographic study of mannan incorporation into the growing cell walls ofSaccharomyces cerevisiae.J.Bacteriol. 117, 265–269 (1974).

    PubMed  Google Scholar 

  • Farkaš V., Vagabov V.M., Bauer Š.: Biosynthesis of yeast mannan. Diversity of mannosyltransferases in the mannan-synthesizing enzyme system from yeast.Biochim.Biophys.Acta 428, 573–582 (1976).

    PubMed  Google Scholar 

  • Feldmesser M., Kress Y., Mednick A., Casadevall A.: The effect of the echinocandin analogue caspofungin on cell wall glucan synthesis byCryptococcus neoformans.J.Infect.Dis. 182, 1791–1795 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Fèvre M., Rougier M.: Autoradiographic study of hyphal cell wall synthesis ofSaprolegnia.Arch.Microbiol. 131, 212–215 (1982).

    Article  Google Scholar 

  • Fischer J.: Optical polarization reveals different ultrastructural arrangements of polysaccharides in the yeast cell walls.Acta Biol.Acad.Sci.Hung. 28, 49–58 (1977).

    PubMed  CAS  Google Scholar 

  • Frey-Wyssling A., Mühlethaler K.: Der mikroskopische Feinbau von Chitinzellwänden.Vierteljahresschr.Naturforsch.Ges.Zürich 95, 45–52 (1950).

    Google Scholar 

  • Galichet A., Sockalingum G.D., Belarbi A., Manfait M.: FTIR spectroscopic analysis ofSaccharomyces cerevisiae cell walls: study of an anomalous strain exhibiting a pink-colored cell phenotype.FEMS Microbiol.Lett. 197, 79–86 (2001).

    Article  Google Scholar 

  • Glaser L., Brown D.H.: The synthesis of chitin in cell free extracts ofNeurospora crassa.J.Biol.Chem. 228, 729–742 (1957).

    PubMed  CAS  Google Scholar 

  • Goldman R.C., Branstrom A.: Targeting the cell wall synthesis and assembly in microbes: similarities and contrasts between bacteria and fungi.Curr.Pharm.Design 5, 473–501 (1999).

    CAS  Google Scholar 

  • Gooday G.: Chitin metabolism: a target for antifungal and antiparasitic drugs, pp. 175–185 in E. Borowski, D. Shugar (Eds):Molecular Aspects of Chemotherapy. Pergamon Press, New York 1990.

    Google Scholar 

  • Goubet F., Jackson P., Deery M., Dufree P.: Polysaccharide analysis using carbohydrate gel electrophoresis: a method to study plant cell wall polysaccharides and polysaccharide hydrolases.Anal.Biochem. 300, 53–68 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Hardy M.R., Townsend R.R., Lee Y.C.: Monosaccharide analysis of glycoconjugates by anion exchange chromatography with pulsed amperometric detection.Anal.Biochem. 170, 54–62 (1988).

    Article  PubMed  CAS  Google Scholar 

  • Hašek J., Streiblová E.: Fluorescence microscopy methods.Meth.Mol.Biol. 53, 391–405 (1996).

    Google Scholar 

  • Horisberger M., Vonlanthen M.: Location of mannan on thin sections of budding yeasts with gold markers.Arch.Microbiol. 115, 1–7 (1977).

    Article  PubMed  CAS  Google Scholar 

  • Houwik A.L., Kreger D.R., Roelfsen P.A.: Composition and structure of yeast cell walls.Nature (London) 168, 693–699 (1951).

    Article  Google Scholar 

  • Huffaker T.C., Robbins P.W.: Temperature-sensitive yeast mutants deficient in asparagine-linked glycosylation.J.Biol.Chem. 257, 3203–3210 (1982).

    PubMed  CAS  Google Scholar 

  • Huffaker T.C., Robbins P.W.: Yeast mutants deficient in protein glycosylation.Proc.Nat.Acad.Sci.USA 80, 7466–7470 (1983).

    Article  PubMed  CAS  Google Scholar 

  • Hunsley D., Burnett J.H.: The ultrastructural architecture of the walls of some hyphal fungi.J.Gen.Microbiol. 62, 200–218 (1970).

    Google Scholar 

  • Jackson P.: High-resolution polyacrylamide gel electrophoresis of fluorophore-labeled reducing saccharides.Meth.Enzymol. 230, 250–265 (1994).

    Article  PubMed  CAS  Google Scholar 

  • Kang M.S., Elango N., Mattio E., Au-Young J., Robbins P.W., Cabib E.: Isolation of chitin synthase fromSaccharomyces cerevisiae: purification of an enzyme by entrappment in the reaction product.J.Biol.Chem. 259, 14966–14972 (1984).

    PubMed  CAS  Google Scholar 

  • Klis F.M., Mol P., Hellingwerf K., Brul S.: Dynamics of cell wall structure inSaccharomyces cerevisiae.FEMS Microbiol.Rev. 26, 239–256 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Kocourek J., Ballou C.E.: Method for fingerprinting yeast cell wall mannans.J.Bacteriol. 100, 1175–1181 (1969).

    PubMed  CAS  Google Scholar 

  • Kollar R., Petráková E., Ashwell G., Robbins P.W., Cabib E.: Architecture of the yeast cell wall. The linkage between chitin and β-(1,3)-glucan.J.Biol.Chem. 270, 1170–1178 (1995).

    Article  PubMed  CAS  Google Scholar 

  • Kopecka M., Phaff H.J., Fleet G.H.: Demonstration of a fibrillar component in the cell wall of the yeastSaccharomyces cerevisiae and its chemical nature.J.Cell.Biol. 62, 66–76 (1974).

    Article  PubMed  CAS  Google Scholar 

  • Korn E.D., Northcote D.H.: Physical and chemical properties of polysaccharides and glycoproteins of the yeast cell wall.Biochem.J. 75, 12–17 (1960).

    PubMed  CAS  Google Scholar 

  • Košinová A., Farkaš V., Machala S., Bauer Š.: Site of mannan synthesis in yeast. An autoradiographic study.Arch.Microbiol. 99, 255–263 (1974).

    Article  PubMed  Google Scholar 

  • Kreger D.R.: Observations on cell walls of yeasts and some other fungi by X-ray diffraction and solubility tests.Biochim.Biophys.Acta 13, 1–9 (1954).

    Article  PubMed  CAS  Google Scholar 

  • Kulaev I.S., Afanasieva T.P., Belikova M.P.: Localization of inorganic polyphosphates and nucleoside polyphosphates in cells of the yeastEndomyces magnusii.Biokhimiya (Moscow) 32, 539–547 (1967).

    CAS  Google Scholar 

  • Kuo S.-C., Lampen J.O.: Tunicamycin — an inhibitor of yeast glycoprotein synthesis.Biochem.Biophys.Res.Commun. 58, 287–295 (1974).

    Article  PubMed  CAS  Google Scholar 

  • Lehle L., Tanner W.: Glycosyl transfer from dolichoyl phosphate sugars to endogenous and exogenous glycoprotein acceptors in yeast.Eur.J.Biochem. 83, 563–570 (1978).

    Article  PubMed  CAS  Google Scholar 

  • Leloir L.: Two decades of research on the biosynthesis of saccharides.Science 172, 1299–1303 (1971).

    Article  PubMed  CAS  Google Scholar 

  • Lipke P.N., Ovalle R.: Cell wall architecture in yeast: new structure and new challenges.J.Bacteriol. 180, 3735–3740 (1998).

    PubMed  CAS  Google Scholar 

  • Lucero H.A., Kuranda M.J., Bulik D.A.: A nonradioactive, high throughput assay for chitin synthase activity.Anal.Biochem. 305, 97–105 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Lussier M., White A.M., Sheraton T., di Paolo T., Treadwell J., Southard S.B., Horenstein C.I., Chen-Weiner J., Ram A.F., Kapteyn J.C., Roemer T.W., Vo D.H., Bondoc D.C., Hall J., Zhong W.W., Sdicu A.M., Davies J., Klis F.M., Robbins P.W., Bussey H.: Large-scale identification of genes involved in cell surface biosynthesis and architecture inSaccharomyces cerevisiae.Genetics 147, 435–450 (1997).

    PubMed  CAS  Google Scholar 

  • Maeda H., Ishida N.: Specificity of binding of hexopyranosyl polysaccharides with fluorescent brightener.J.Biochem. 62, 276–278 (1967).

    PubMed  CAS  Google Scholar 

  • Magnelli P., Cipollo J.F., Abeijon C.: A refined method for the determination ofSaccharomyces cerevisiae cell wall composition and β-1,6-glucan fine structure.Anal.Biochem. 301, 136–150 (2002).

    Article  PubMed  CAS  Google Scholar 

  • Manners D.J., Masson A.J., Patterson J.C.: The structure of a β-(1-6)-d-glucan from yeast cell walls.Biochem.J. 135, 19–30 (1973).

    PubMed  CAS  Google Scholar 

  • Molano J., Bowers B., Cabib E.: Distribution of chitin in the yeast cell wall. An ultrastructural and chemical study.J.Cell.Biol. 85, 199–212 (1980).

    Article  PubMed  CAS  Google Scholar 

  • Montijn R.C., Vink E., Müller W.H., Verklfij A.J., Van den Ende H., Henrissat B., Klis F.M.: Localization of synthesis of β-1,6-glucan inSaccharomyces cerevisiae.J.Bacteriol. 181, 7414–7420 (1999).

    PubMed  CAS  Google Scholar 

  • Mrša V., Seidl T., Gentzsch M., Tanner W.: Specific labeling of cell wall proteins by biotinylation. Identification of four covalently linkedO-mannosylated proteins ofSaccharomyces cerevisiae.Yeast 30, 1145–1154 (1997).

    Google Scholar 

  • Nakajima T., Ballou C.E.: Characterization of the carbohydrate fragments obtained fromSaccharomyces cerevisiae mannan by alkaline degradation.J.Biol.Chem. 249, 7679–7684 (1974).

    PubMed  CAS  Google Scholar 

  • Nakajima T., Ballou C.E.: Yeast manno-protein biosynthesis: solubilization and selective assay of four mannosyltransferases.Proc.Nat.Acad.Sci.USA 72, 3912–3916 (1975).

    Article  PubMed  CAS  Google Scholar 

  • de Nobel H., van den Ende H., Klis F.M.: Cell wall maintenance in fungi.Trends Microbiol. 8, 344–345 (2000).

    Article  PubMed  Google Scholar 

  • Northcote D.H., Horne R.W.: The chemical composition and structure of the yeast cell wall.Biochem.J. 51, 232–236 (1952).

    PubMed  CAS  Google Scholar 

  • Novick P., Field C., Schekman R.: Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway.Cell 21, 205–215 (1980).

    Article  PubMed  CAS  Google Scholar 

  • Novick P., Ferro S., Schekman R.: Order of events in the yeast secretory pathway.Cell 25, 461–469 (1981).

    Article  PubMed  CAS  Google Scholar 

  • Osumi M.: The ultrastructure of yeast: cell wall structure and formation.Micron 29, 207–233 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Pardo M., Ward M., Bains S., Molina M., Blackstock W., Gil C., Nombela C.: A proteomic approach for the study ofSaccharomyces cerevisiae cell wall biogenesis.Electrophoresis 21, 339–410 (2000).

    Google Scholar 

  • Peat S., Whelan W.J., Edwards T.E.: Polysaccharides of baker’s yeast — IV. Mannan.J.Chem.Soc. 1961, 29–34 (1961).

    Article  Google Scholar 

  • Santos E., Villanueva J.R., Sentandreu R.: The plasma membrane ofSaccharomyces cerevisiae. Isolation and some properties.Biochim.Biophys.Acta 508, 39–54 (1978).

    Article  PubMed  CAS  Google Scholar 

  • Sawistowska-Schroder E.T., Kerridge D., Perry H.: Echinocandin inhibition of 1,3-β-d-glucan synthase fromCandida albicans.FEBS Lett. 173, 134–138 (1984).

    Article  PubMed  CAS  Google Scholar 

  • Schekman R.: The secretory pathway in yeast.Trends Biochem.Sci. 7, 243–246 (1982).

    Article  CAS  Google Scholar 

  • Sentandreu R., Northcote D.H.: The characterization of oligosaccharides attached to threonine and serine in mannan glycopeptide obtained from the cell wall of yeast.Carbohydr.Res. 10, 584–585 (1969).

    Article  CAS  Google Scholar 

  • Šesták S., Farkaš V.:In situ assays of fungal enzymes in cells permeabilized by osmotic shock.Anal.Biochem. 292, 34–39 (2001).

    Article  PubMed  CAS  Google Scholar 

  • Shedletzky E., Unger C., Delmer D.P.: A microtiter-based fluorescence assay for (1,3)-β-glucan synthases.Anal.Biochem. 249, 88–93 (1997).

    Article  PubMed  CAS  Google Scholar 

  • Shematek E.M., Braatz J.A., Cabib E.: Biosynthesis of the yeast cell wall — I. Preparation and properties of β-(1,3)-glucan synthetase.J.Biol.Chem. 255, 888–894 (1980).

    PubMed  CAS  Google Scholar 

  • Slaninova I., Šestak S., Svoboda A., Farkaš V.: Cell wall and cytoskeleton reorganization as the response to hyperosmotic shock inSaccharomyces cerevisiae.Arch.Microbiol. 173, 245–252 (2000).

    Article  PubMed  CAS  Google Scholar 

  • Streiblová E., Malek I., Beran K.: Structural changes in the cell wall ofSchizosaccharomyces pombe during cell division.J.Bacteriol. 91, 428–435 (1966).

    PubMed  Google Scholar 

  • Toh-E A., Yasunaga S., Nisogi H., Tanaka K., Oguchi T., Matsui Y.: Three yeast genes,PIR1, PIR2 andPIR3, containing internal tandem repeats, are related to each other, andPIR1 andPIR2 are required for tolerance to heat shock.Yeast 9, 481–494 (1993).

    Article  PubMed  CAS  Google Scholar 

  • Vaishnav V.V., Bacon B.E., O’Neill M., Cherniak R.: Structural characterization of the galactoxylomannan ofCryptococcus neoformans Cap67.Carbohydr.Res. 306, 315–330 (1998).

    Article  PubMed  CAS  Google Scholar 

  • Wang M.C., Bartnicki-Garcia S.: Biosynthesis of β-1,3- and β-1,6-linked glucan byPhytophthora cinnamomi hyphal walls.Biochem.Biophys.Res.Commun. 24, 832–837 (1966).

    Article  PubMed  CAS  Google Scholar 

  • Wessels J.G.H.: Wall growth, protein excretion and morphogenesis in fungi.New Phytol. 123, 397–413 (1993).

    Article  CAS  Google Scholar 

  • Zhang D., Miller M.J.: Polyoxins and nikkomycins: progress in synthetic and biological studies.Curr.Pharm.Design 5, 73–99 (1999).

    CAS  Google Scholar 

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Correspondence to V. Farkaš.

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The work on this review was supported by grant no. 2/7137/22 from theSlovak Grant Agency (VEGA).

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Farkaš, V. Structure and biosynthesis of fungal cell walls: Methodological approaches. Folia Microbiol 48, 469–478 (2003). https://doi.org/10.1007/BF02931327

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