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Abstract

-Mannosidases play an important role in the processing of mannose-containing glycans in eukaryotes. A deficiency in -mannosidase is lethal in humans and cattle. In contrast to mammals, does not require the endoplasmic reticulum -mannosidase gene for growth. However, little is known of the consequence of loss of function of class I -mannosidases in filamentous fungi. In this study, the /Af gene was identified to encode 1,2--mannosidase MsdS in . Soluble MsdS expressed in was characterized as a typical class I -mannosidase. The gene was deleted by replacement of the gene with a gene. Although the mutant showed a defect in -glycan processing, as well as a reduction of cell wall components and a reduced ability of conidiation, it appeared that the rate of hyphal growth was not affected. Morphology analysis revealed abnormal polarity and septation at the stages of germination, hyphal growth and conidiation. Although the mechanism by which the -glycan processing affects polarity and septation is unclear, our results show that is involved in polarity and septation in .

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2008-07-01
2019-10-13
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References

  1. Akao, T., Yamaguchi, M., Yahara, A., Yoshiuchi, K., Fujita, H., Yamada, O., Akita, O., Ohmachi, T., Asada, Y. & Yoshida, T. ( 2006; ). Cloning and expression of 1,2-alpha-mannosidase gene (fmanIB) from filamentous fungus Aspergillus oryzae: in vivo visualization of the FmanIBp-GFP fusion protein. Biosci Biotechnol Biochem 70, 471–479.[CrossRef]
    [Google Scholar]
  2. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D. J. ( 1997; ). Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25, 3389–3402.[CrossRef]
    [Google Scholar]
  3. Burditt, L. J., Phillips, N. C., Robinson, D., Winchester, B. G., Van-de-Water, N. S. & Jolly, R. D. ( 1978; ). Characterization of the mutant α-mannosidase in bovine mannosidosis. Biochem J 175, 1013–1022.
    [Google Scholar]
  4. Chiba, Y., Yamagata, Y., Iijima, S., Nakajima, T. & Ichishima, E. ( 1993; ). The carbohydrate moiety of the acid carboxypeptidase from Aspergillus saitoi. Curr Microbiol 27, 281–288.[CrossRef]
    [Google Scholar]
  5. Cove, D. J. ( 1966; ). The induction and repression of nitrate reductase in the fungus Aspergillus nidulans. Biochim Biophys Acta 113, 51–56.[CrossRef]
    [Google Scholar]
  6. d'Enfert, C. ( 1996; ). Selection of multiple disruption events in Aspergillus fumigatus using the orotidine-5′-decarboxylase gene, pyrG, as a unique transformation marker. Curr Genet 30, 76–82.[CrossRef]
    [Google Scholar]
  7. Daniel, P. F., Winchester, B. & Warren, C. D. ( 1994; ). Mammalian α-mannosidases – multiple forms but a common purpose? Glycobiology 4, 551–566.[CrossRef]
    [Google Scholar]
  8. Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A. & Smith, F. ( 1956; ). Colorimetric method for determination of sugars and related substances. Anal Chem 28, 350–356.[CrossRef]
    [Google Scholar]
  9. Eades, C. J. & Hintz, W. E. ( 2000; ). Characterization of the class I alpha-mannosidase gene family in the filamentous fungus Aspergillus nidulans. Gene 255, 25–34.[CrossRef]
    [Google Scholar]
  10. Eades, C. J., Gilbert, A. M., Goodman, C. D. & Hintz, W. E. ( 1998; ). Identification and analysis of a class 2 α-mannosidase from Aspergillus nidulans. Glycobiology 8, 17–33.[CrossRef]
    [Google Scholar]
  11. Elorza, M. V., Murgui, A. & Sentandreu, R. ( 1985; ). Dimorphism in Candida albicans: contribution of mannoproteins to the architecture of yeast and mycelial cell walls. J Gen Microbiol 131, 2209–2216.
    [Google Scholar]
  12. Galagan, J. E., Calvo, S. E., Cuomo, C., Ma, L. J., Wortman, J. R., Batzoglou, S., Lee, S. I., Baştürkmen, M., Spevak, C. C. & other authors ( 2005; ). Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438, 1105–1115.[CrossRef]
    [Google Scholar]
  13. Hearn, V. M. & Sietsma, J. H. ( 1994; ). Chemical and immunological analysis of the Aspergillus fumigatus cell wall. Microbiology 140, 789–795.[CrossRef]
    [Google Scholar]
  14. Ichishima, E., Taya, N., Ikeguchi, M., Chiba, Y., Nakamura, M., Kawabata, C., Inoue, T., Takahashi, K., Minetoki, T. & other authors ( 1999; ). Molecular and enzymic properties of recombinant 1,2-α-mannosidase from Aspergillus saitoi overexpressed in Aspergillus oryzae cells. Biochem J 339, 589–597.[CrossRef]
    [Google Scholar]
  15. Kornfeld, R. & Kornfeld, S. ( 1985; ). Assembly of asparagine-linked oligosaccharides. Annu Rev Biochem 54, 631–664.[CrossRef]
    [Google Scholar]
  16. Kukuruzinska, M. A., Bergh, M. L. & Jackson, B. J. ( 1987; ). Protein glycosylation in yeast. Annu Rev Biochem 56, 915–944.[CrossRef]
    [Google Scholar]
  17. Latgé, J. P. ( 1999; ). Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 12, 310–350.
    [Google Scholar]
  18. Lee, J. I., Yu, Y. M., Rho, Y. M., Park, B. C., Choi, J. H., Park, H. M. & Maeng, P. J. ( 2005; ). Differential expression of the chsE gene encoding a chitin synthase of Aspergillus nidulans in response to developmental status and growth conditions. FEMS Microbiol Lett 249, 121–129.[CrossRef]
    [Google Scholar]
  19. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. ( 1951; ). Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265–275.
    [Google Scholar]
  20. Maras, M., De Bruyn, A., Schraml, J., Herdewijn, P., Claeyssens, M., Fiers, W. & Contreras, R. ( 1997; ). Structural characterization of N-linked oligosaccharides from cellobiohydrolase I secreted by the filamentous fungus Trichoderma reesei RUTC 30. Eur J Biochem 245, 617–625.[CrossRef]
    [Google Scholar]
  21. Maras, M., Callewaert, N., Piens, K., Claeyssens, M., Martinet, W., Dewaele, S., Contreras, H., Dewerte, I., Penttila, M. & Contreras, R. ( 2000; ). Molecular cloning and enzymatic characterization of a Trichoderma reesei 1,2-α-d-mannosidase. J Biotechnol 77, 255–263.[CrossRef]
    [Google Scholar]
  22. Matta, K. L. & Bahl, O. P. ( 1972; ). Glycosidases of Aspergillus niger. IV. Purification and characterization of α-mannosidase. J Biol Chem 247, 1780–1787.
    [Google Scholar]
  23. Momany, M. & Taylor, I. ( 2000; ). Landmarks in the early duplication cycles of Aspergillus fumigatus and Aspergillus nidulans: polarity, germ tube emergence and septation. Microbiology 146, 3279–3284.
    [Google Scholar]
  24. Momany, M., Westfall, P. J. & Abramowsky, G. ( 1999; ). Aspergillus nidulans swo mutants show defects in polarity establishment, polarity maintenance and hyphal morphogenesis. Genetics 151, 557–567.
    [Google Scholar]
  25. Moremen, K. W., Trimble, R. B. & Herscovics, A. ( 1994; ). Glycosidases of the asparagine-linked oligosaccharide processing pathway. Glycobiology 4, 113–125.[CrossRef]
    [Google Scholar]
  26. Norden, N. E., Lundblad, A., Ockerman, P. A. & Jolly, R. D. ( 1973; ). Mannosidosis in Angus cattle: partial characterization of two mannose containing oligosaccharides. FEBS Lett 35, 209–212.[CrossRef]
    [Google Scholar]
  27. Oka, T., Hamaguchi, T., Sameshima, Y., Goto, M. & Furukawa, K. ( 2004; ). Molecular characterization of protein O-mannosyltransferase and its involvement in cell-wall synthesis in Aspergillus nidulans. Microbiology 150, 1973–1982.[CrossRef]
    [Google Scholar]
  28. Oka, T., Sameshima, Y., Koga, T., Kim, H., Goto, M. & Furukawa, K. ( 2005; ). Protein O-mannosyltransferase A of Aspergillus awamori is involved in O-mannosylation of glucoamylase I. Microbiology 151, 3657–3667.[CrossRef]
    [Google Scholar]
  29. Phillips, N. C., Robinson, D., Winchester, B. G. & Jolly, R. D. ( 1974; ). Mannosidosis in Angus cattle. The enzymic defect. Biochem J 137, 363–371.
    [Google Scholar]
  30. Puccia, R., Grondin, B. & Herscovics, A. ( 1993; ). Disruption of the processing α-mannosidase gene does not prevent outer chain synthesis in Saccharomyces cerevisiae. Biochem J 290, 21–26.
    [Google Scholar]
  31. Roberts, D. B., Mulvany, W. J., Dwek, R. A. & Rudd, P. M. ( 1998; ). Mutant analysis reveals an alternative pathway for N-linked glycosylation in Drosophila melanogaster. Eur J Biochem 253, 494–498.[CrossRef]
    [Google Scholar]
  32. Rose, D. P. ( 1967; ). Tryptophan metabolism in carcinoma of the breast. Lancet 1, 239–241.
    [Google Scholar]
  33. Schoffelmeer, E. A., Klis, F. M., Sietsma, J. H. & Cornelissen, B. J. ( 1999; ). The cell wall of Fusarium oxysporum. Fungal Genet Biol 27, 275–282.[CrossRef]
    [Google Scholar]
  34. Seiler, S. & Plamann, M. ( 2003; ). The genetic basis of cellular morphogenesis in the filamentous fungus Neurospora crassa. Mol Biol Cell 14, 4352–4364.[CrossRef]
    [Google Scholar]
  35. Shaw, B. D. & Momany, M. ( 2002; ). Aspergillus nidulans polarity mutant swoA is complemented by protein O-mannosyltransferase pmtA. Fungal Genet Biol 37, 263–270.[CrossRef]
    [Google Scholar]
  36. Steinbach, W. J., Stevens, D. A. & Denning, D. W. ( 2003; ). Combination and sequential antifungal therapy for invasive aspergillosis: review of published in vitro and in vivo interactions and 6281 clinical cases from 1966 to 2001. Clin Infect Dis 37, S188–S224.[CrossRef]
    [Google Scholar]
  37. Tanner, W. & Lehle, L. ( 1987; ). Protein glycosylation in yeast. Biochim Biophys Acta 906, 81–99.[CrossRef]
    [Google Scholar]
  38. Weidner, G., D'Enfert, C., Koch, A., Mol, P. C. & Brakhage, A. A. ( 1998; ). Development of a homologous transformation system for the human pathogenic fungus Aspergillus fumigatus based on the pyrG gene encoding orotidine 5′-monophosphate decarboxylase. Curr Genet 33, 378–385.[CrossRef]
    [Google Scholar]
  39. Weng, S. & Spiro, R. G. ( 1993; ). Demonstration that a kifunensine-resistant α-mannosidase with a unique processing action on N-linked oligosaccharides occurs in rat liver endoplasmic reticulum and various cultured cells. J Biol Chem 268, 25656–25663.
    [Google Scholar]
  40. Weng, S. & Spiro, R. G. ( 1996; ). Endoplasmic reticulum kifunensine-resistant α-mannosidase is enzymatically and immunologically related to the cytosolic α-mannosidase. Arch Biochem Biophys 325, 113–123.[CrossRef]
    [Google Scholar]
  41. Xia, G., Jin, C., Zhou, J., Yang, S. & Zhang, S. ( 2001; ). A novel chitinase having a unique mode of action from Aspergillus fumigatus YJ-407. Eur J Biochem 268, 4079–4085.[CrossRef]
    [Google Scholar]
  42. Yelton, M. M., Hamer, J. E. & Timberlake, W. E. ( 1984; ). Transformation of Aspergillus nidulans by using a trpC plasmid. Proc Natl Acad Sci U S A 81, 1470–1474.[CrossRef]
    [Google Scholar]
  43. Yoshida, T. & Ichishima, E. ( 1995; ). Molecular cloning and nucleotide sequence of the genomic DNA for 1,2-α-d-mannosidase gene, msdC from Penicillium citrinum. Biochim Biophys Acta 1263, 159–162.[CrossRef]
    [Google Scholar]
  44. Yoshida, T., Inoue, T. & Ichishima, E. ( 1993; ). 1,2-α-d-mannosidase from Penicillium citrinum: molecular and enzymic properties of two isoenzymes. Biochem J 290, 349–354.
    [Google Scholar]
  45. Yoshihisa, T. & Anraku, Y. ( 1989; ). Nucleotide sequence of AMS1, the structure gene of vacuolar α-mannosidase of Saccharomyces cerevisiae. Biochem Biophys Res Commun 163, 908–915.[CrossRef]
    [Google Scholar]
  46. Yoshihisa, T. & Anraku, Y. ( 1990; ). A novel pathway of import of α-mannosidase, a marker enzyme of vacuolar membrane, in Saccharomyces cerevisiae. J Biol Chem 265, 22418–22425.
    [Google Scholar]
  47. Zhou, H., Hu, H., Zhang, L., Li, R., Ouyang, H., Ming, J. & Jin, C. ( 2007; ). Protein O-mannosyltransferase 1 (AfPmt1p) in Aspergillus fumigatus is crucial for cell wall integrity and conidia morphology especially at an elevated temperature. Eukaryot Cell 6, 2260–2268.[CrossRef]
    [Google Scholar]
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vol. , part 7, pp. 1960-1972

LC-MS/MS analysis of proteins secreted by the wild-type and the Δ strain.



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