1887

Abstract

In the filamentous fungus , the vast majority of the cell-wall-associated proteins are secreted proteins that are in transit in the cell wall. These proteins can be solubilized by detergents and reducing agents. Incubation of a SDS/β-mercaptoethanol-treated cell-wall extract with various recombinant enzymes that hydrolyse cell-wall polysaccharides resulted in the release of a unique protein in minute amounts only after incubation of the cell wall in the presence of 1,3-β-glucanase. Sequence analysis and biochemical studies showed that this glycoprotein, with an apparent molecular mass of 80 kDa, was an acid phosphatase (PhoAp) that was active on both phosphate monoesters and phosphate diesters. PhoAp is a glycosylphosphatidylinositol-anchored protein that was recovered in the culture filtrate and cell-wall fraction of after cleavage of its anchor. It is also a phosphate-repressible acid phosphatase. The absence of PhoAp from a phosphate-rich medium was not associated with a reduction in fungal growth, indicating that this cell-wall-associated protein does not play a role in the morphogenesis of .

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-9-2819
2002-09-01
2020-04-04
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/9/1482819a.html?itemId=/content/journal/micro/10.1099/00221287-148-9-2819&mimeType=html&fmt=ahah

References

  1. Ames B. N. 1966; Assay of inorganic phosphate and phosphatases. Methods Enzymol8:115–118
    [Google Scholar]
  2. Arnold W. N. 1972; Location of acid phosphatase and β-fructofuranosidase within yeast cell envelopes. J Bacteriol112:1346–1352
    [Google Scholar]
  3. Beauvais A., Monod M., Debeaupuis J.-P., Diaquin M., Kobayashi H., Latgé J.-P. 1997; Biochemical and antigenic characterization of a new dipeptidyl-peptidase isolated from Aspergillus fumigatus . J Biol Chem272:6238–6244[CrossRef]
    [Google Scholar]
  4. Bruneau J. M., Magnin T., Tagat E., Legrand R., Bernard M., Diaquin M., Fudali C., Latgé J.-P. 2001; Proteome analysis of Aspergillus fumigatus identifies glycosylphosphatidylinositol-anchored proteins associated to the cell wall biosynthesis. Electrophoresis22:2812–2823[CrossRef]
    [Google Scholar]
  5. Calera J. A., Paris S., Monod M., Hamilton A. J., Debeaupuis J.-P., Diaquin M., Lopez-Medrano R., Leal F., Latgé J.-P. 1997; Cloning and disruption of the antigenic catalase gene of Aspergillus fumigatus . Infect Immun65:4718–4724
    [Google Scholar]
  6. Cao L., Chan C. M., Lee C., Wong S. S. Y., Yuen K. Y. 1998; MP1 encodes an abundant and highly antigenic cell wall mannoprotein in the pathogenic fungus Penicillium marneffei . Infect Immun66:966–973
    [Google Scholar]
  7. Caro L. H. P., Tettelin H., Vossen J. H., Ram A. F. J., van den Ende H., Klis F. M. 1997; In silicio identification of glycosyl-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharomyces cerevisiae . Yeast13:1477–1489[CrossRef]
    [Google Scholar]
  8. Ehrlich K. C., Montalbano B. G., Mullaney E. J., Dishinger H. C. Jr, Ullah A. H. J. 1994; An acid phosphatase from Aspergillus ficuum has homology to Penicillium chrysogenum PhoA. Biochem Biophys Res Commun204:63–68[CrossRef]
    [Google Scholar]
  9. Ferguson M. A. 1992; Colworth medal lecture. Glycosyl-phosphatidylinositol membrane anchors: the table of a tail. Biochem Soc Trans20:243–256
    [Google Scholar]
  10. Fontaine T., Simenel C., Dubreucq G., Adam O., Delepierre M., Lemoine J., Vorgias C. E., Diaquin M., Latgé J.-P. 2000; Molecular organization of the alkali-insoluble fraction of Aspergillus fumigatus cell wall. J Biol Chem275:27594–27607
    [Google Scholar]
  11. Fuglsang C. C., Berka R. M., Wahleithner J. A., Kauppinen S., Shuster J. R., Rasmussen G., Halkier T., Dalboge H., Henrissat B. 2000; Biochemical analysis of recombinant fungal mutanases. A new family of α-1,3-glucanases with novel carbohydrate-binding domains. J Biol Chem275:2009–2018[CrossRef]
    [Google Scholar]
  12. Fujii T., Shimoi H., Iimura Y. 1999; Structure of the glucan-binding sugar chain of Tip1p, a cell wall protein of Saccharomyces cerevisiae . Biochim Biophys Acta 1427;133–144[CrossRef]
    [Google Scholar]
  13. Gerber L. D., Kodukula K., Udenfriend S. 1992; Phosphatidylinositol glycan (PI-G) anchored membrane proteins. Amino acid requirements adjacent to the site of cleavage and PI-G attachment in the COOH-terminal signal peptide. J Biol Chem267:12168–12173
    [Google Scholar]
  14. Gijsbers R., Ceulemans H., Stalmans W., Bollen M. 2001; Structural and catalytic similarities between nucleotide pyrophosphatases/phosphodiesterases and alkaline phosphatases. J Biol Chem276:1361–1368[CrossRef]
    [Google Scholar]
  15. Haas H., Redl B., Leitner E., Stöffler G. 1991; Penicillium chrysogenum extracellular acid phosphatase: purification and biochemical characterization. Biochim Biophys Acta1074:392–397[CrossRef]
    [Google Scholar]
  16. Haas H., Redl B., Friedlin E., Stöffler G. 1992; Isolation and analysis of the Penicillium chrysogenum phoA gene encoding a secreted phosphate-repressible acid phosphatase. Gene113:129–133[CrossRef]
    [Google Scholar]
  17. Hamada K., Fukuchi S., Arisawa M., Baba M., Kitada K. 1998; Screening for glycosylphosphatidylinositol (GPI)-dependent cell wall proteins in Saccharomyces cerevisiae . Mol Gen Genet258:53–59[CrossRef]
    [Google Scholar]
  18. Hoyer L. L., Clevenger J., Hecht J. E., Ehrhart E. J., Poulet F. M. 1999; Detection of Als proteins on the cell wall of Candida albicans in murine tissues. Infect Immun67:4251–4255
    [Google Scholar]
  19. Jennings D. H. 1995; Phosphorus. In The Physiology of Fungal Nutrition pp252–287 Cambridge: Cambridge University Press;
    [Google Scholar]
  20. Kandasamy R., Vediyappan G., Chaffin W. L. 2000; Evidence for the presence of pir-like proteins in Candida albicans . FEMS Microbiol Lett186:239–243[CrossRef]
    [Google Scholar]
  21. Kapteyn J. C., Montijn R. C., Dijkgraaf G. J. P., Van den Ende H., Klis F. M. 1995; Covalent association of β-1,3-glucan with β-1,6-glucosylated mannoproteins in cell walls of Candida albicans . J Bacteriol177:3788–3792
    [Google Scholar]
  22. Kapteyn J. C., Montijn R. C., Vink E., de la Cruz J., Llobell A., Douwes J. E., Shimoi H., Lipke P. N., Klis F. M. 1996; Retention of Saccharomyces cerevisiae cell wall proteins through a phosphodiester-linked β-1,3/β-1,6-glucan heteropolymer. Glycobiology6:337–345[CrossRef]
    [Google Scholar]
  23. Kapteyn J. C., Van den Ende H., Klis F. M. 1999; The contribution of cell wall proteins to the organization of the yeast cell wall. Biochim Biophys Acta1426:373–383[CrossRef]
    [Google Scholar]
  24. Kapteyn J. C., Hoyer L. L., Hecht J. E., Müller W. H., Andel A., Verkleij A. J., Makarow M., Van den Ende H., Klis F. M. 2000; The cell wall architecture of Candida albicans wild-type cells and cell wall-defective mutants. Mol Microbiol35:601–611
    [Google Scholar]
  25. Klis F. M. 1994; Review: cell wall assembly in yeast. Yeast10:851–869[CrossRef]
    [Google Scholar]
  26. Laemmli U. K. 1970; Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature227:680–685[CrossRef]
    [Google Scholar]
  27. Latgé J.-P., Moutaouakil M., Debeaupuis J.-P., Bouchara J. P., Haynes K., Prévost M. C. 1991; The 18-kilodalton antigen secreted by Aspergillus fumigatus . Infect Immun59:2586–2594
    [Google Scholar]
  28. Latgé J.-P., Kobayashi H., Debeaupuis J.-P., Diaquin M., Sarfati J., Wieruszeski J. M., Parra E., Fournet B. 1994; Chemical and immunological characterization of the extracellular galactomannan of Aspergillus fumigatus . Infect Immun62:5424–5433
    [Google Scholar]
  29. Linnemans W. A. M., Boer P., Elbers P. F. 1977; Localization of acid phosphatase in Saccharomyces cerevisiae : a clue to cell wall formation. J Bacteriol131:638–644
    [Google Scholar]
  30. Lipke P. N., Wojciechowicz D., Kurjan J. 1989; AGα1 is the structural gene for the Saccharomyces cerevisiae α-agglutinin, a cell surface glycoprotein involved in cell–cell interactions during mating. Mol Cell Biol9:3155–3165
    [Google Scholar]
  31. Lu C. F., Kurjan J., Lipke P. N. 1994; A pathway for cell wall anchorage of Saccharomyces cerevisiae α-agglutinin. Mol Cell Biol14:4825–4833
    [Google Scholar]
  32. MacRae W. D., Buxton F. P., Sibley S., Garven S., Gwynne D. I., Davies R. W., Arst H. N. Jr. 1988; A phosphate-repressible acid phosphatase gene from Aspergillus niger : its cloning, sequencing and transcriptional analysis. Gene71:339–348[CrossRef]
    [Google Scholar]
  33. Mouyna I., Fontaine T., Vai M., Monod M., Fonzi W. A., Diaquin M., Popolo L., Hartland R. P., Latgé J.-P. 2000; Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J Biol Chem275:14882–14889[CrossRef]
    [Google Scholar]
  34. Mouyna I., Sarfati J., Recco P., Fontaine T., Henrissat B., Latgé J.-P. 2002; Molecular characterization of a cell wall associated β(1-3)endoflucanase of Aspergillus fumigatus . Med Mycol in press
    [Google Scholar]
  35. Mrsa V., Seidl T., Gentzsch M., Tanner W. 1997; Specific labelling of cell wall proteins by biotinylation. Identification of four covalently linked O -mannosylated proteins of Saccharomyces cerevisiae . Yeast13:1145–1154[CrossRef]
    [Google Scholar]
  36. O’Brien P. J., Herschlag D. 2001; Functional interrelationships in the alkaline phosphatase superfamily: phosphodiesterase activity of Escherichia coli alkaline phosphatase. Biochemistry40:5691–5699[CrossRef]
    [Google Scholar]
  37. Ostanin K., Harms E. H., Stevis P. E., Kuciel R., Zhou M. M., Van Etten R. L. 1992; Overexpression, site-directed mutagenesis, and mechanism of Escherichia coli acid phosphatase. J Biol Chem267:22830–22836
    [Google Scholar]
  38. Rodriguez E., Mullaney E. J., Lei X. G. 2000; Expression of the Aspergillus fumigatus phytase gene in Pichia pastoris and characterization of the recombinant enzyme. Biochem Biophys Res Commun268:373–378[CrossRef]
    [Google Scholar]
  39. Rodriguez-Pena J. M., Cid V. J., Arroyo J., Nombela C. 2000; A novel family of cell wall-related proteins regulated differently during the yeast life cycle. Mol Cell Biol20:3245–3255[CrossRef]
    [Google Scholar]
  40. Saleh M. T., Belisle J. T. 2000; Secretion of an acid phosphatase (SapM) by Mycobacterium tuberculosis that is similar to eukaryotic acid phosphatases. J Bacteriol182:6850–6853[CrossRef]
    [Google Scholar]
  41. Schoffelmeer E. A. M., Vossen J. H., van Doorn A. A., Cornelissen B. J. C., Haring M. A. 2001; FEM1, a Fusarium oxysporum glycoprotein that is covalently linked to the cell wall matrix and is conserved in filamentous fungi. Mol Genet Genomics265:143–152[CrossRef]
    [Google Scholar]
  42. Stratford M. 1994; Another brick in the wall? Recent developments concerning the yeast cell envelope. Yeast10:1741–1752[CrossRef]
    [Google Scholar]
  43. Ullah A. H. J., Sethumadhavan K., Lei X. G., Mullaney E. J. 2000; Biochemical characterization of cloned Aspergillus fumigatus phytase (PhyA). Biochem Biophys Res Commun275:279–285[CrossRef]
    [Google Scholar]
  44. van der Vaart J. M., Caro L. H. P., Chapman J. W., Klis F. M., Verrips C. T. 1995; Identification of three mannoproteins in the cell wall of Saccharomyces cerevisiae . J Bacteriol177:3104–3110
    [Google Scholar]
  45. Van Etten R. L., Davidson R., Stevis P. E., MacArthur H., Moore D. L. 1991; Covalent structure, disulfide bonding and identification of reactive surface and active site residues of human prostatic acid phosphatase. J Biol Chem266:2313–2319
    [Google Scholar]
  46. Vogel K., Hinnen A. 1990; The yeast phosphatase system. Mol Microbiol4:2013–2017[CrossRef]
    [Google Scholar]
  47. Von Heijne G. 1986; A new method for predicting signal sequence cleavage sites. Nucleic Acids Res14:4683–4690[CrossRef]
    [Google Scholar]
  48. Vorgias C. E., Tews I., Perrrakis A., Wilson K. J., Oppenheim A. B. 1993; Purification and characterization of the recombinant chitin degrading enzymes, chitinase A and chitobiase from Serratia marcescens . In Chitin Enzymology pp417–422 Edited by Muzzarelli R. A. A.. Antona, Italy: European Chitin Society;
    [Google Scholar]
  49. Worley K. C., Wiese B. A., Smith R. F. 1995; beauty: an enhanced blast-based search tool that integrates multiple biological information resources into sequence similarity search results. Genome Res5:173–184[CrossRef]
    [Google Scholar]
  50. Wyss M., Pasamontes L., Friedlein A.. 13 other authors 1999; Biophysical characterization of fungal phytases ( myo -inositol hexakisphosphate phosphohydrolases): molecular size, glycosylation pattern, and engineering of proteolytic resistance. Appl Environ Microbiol65:359–366
    [Google Scholar]
  51. Yoda K., Ko J. H., Nagamatsu T., Lin Y., Kaibara C., Kawada T., Tomishige N., Hashimoto H., Noda Y., Yamasaki M. 2000; Molecular characterization of a novel yeast cell-wall acid phosphatase cloned from Kluyveromyces marxianus . Biosci Biotechnol Biochem64:142–148[CrossRef]
    [Google Scholar]
  52. Yoshida H., Oikawa S., Ikeda M., Reese E. T. 1989; A novel acid phosphatase excreted by Penicillium funiculosum that hydrolyzes both phosphodiesters and phosphomonoesters with aryl leaving groups. J Biochem105:794–798
    [Google Scholar]
  53. Zverlov V. V., Volkov I. Y., Velikodvorskaya T. V., Schwarz W. H. 1997; Highly thermostable endo-1,3-β-glucanase (laminarinase) LamA from Thermotoga neapolitana : nucleotide sequence of the gene and characterization of the recombinant gene product. Microbiology143:1701–1708[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-9-2819
Loading
/content/journal/micro/10.1099/00221287-148-9-2819
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error