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Original Articles

An α-Amylase Homologue, aah3, Encodes a GPI-Anchored Membrane Protein Required for Cell Wall Integrity and Morphogenesis in Schizosaccharomyces pombe

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Pages 1454-1463 | Received 26 Dec 2005, Accepted 19 Jan 2006, Published online: 22 May 2014

  • 1) Kapteyn, J. C., Van Den Ende, H., and Klis, F. M., The contribution of cell-wall proteins to the organization of the yeast cell wall. Biochim. Biophys. Acta, 1426, 373–383 (1999).
  • 2) Verstrepen, K. J., Derdelinckx, G., Verachtert, H., and Delvaux, F. R., Yeast flocculation: what brewers should know. Appl. Microbiol. Biotechnol., 61, 197–205 (2003).
  • 3) Colussi, P. A., and Orlean, P., The essential Schizosaccharomyces pombe gpi1 + gene complements a bakers’ yeast GPI anchoring mutant and is required for efficient cell separation. Yeast, 13, 139–150 (1997).
  • 4) Tiede, A., Schubert, J., Nischan, C., Jensen, I., Westfall, B., Taron, C. H., Orlean, P., and Schmidt, R. E., Human and mouse Gpi1p homologues restore glycosylphosphatidylinositol membrane anchor biosynthesis in yeast mutants. Biochem. J., 334, 609–616 (1998).
  • 5) Wood, V., Gwilliam, R., Rajandream, M. A., Lyne, M., Lyne, R., Stewart, A., Sgouros, J., Peat, N., Hayles, J., Baker, S., Basham, D., Bowman, S., Brooks, K., Brown, D., Brown, S., Chillingworth, T., Churcher, C., Collins, M., Connor, R., Cronin, A., Davis, P., Feltwell, T., Fraser, A., Gentles, S., Goble, A., Hamlin, N., Harris, D., Hidalgo, J., Hodgson, G., Holroyd, S., Hornsby, T., Howarth, S., Huckle, E. J., Hunt, S., Jagels, K., James, K., Jones, L., Jones, M., Leather, S., McDonald, S., McLean, J., Mooney, P., Moule, S., Mungall, K., Murphy, L., Niblett, D., Odell, C., Oliver, K., O’Neil, S., Pearson, D., Quail, M. A., Rabbinowitsch, E., Rutherford, K., Rutter, S., Saunders, D., Seeger, K., Sharp, S., Skelton, J., Simmonds, M., Squares, R., Squares, S., Stevens, K., Taylor, K., Taylor, R. G., Tivey, A., Walsh, S., Warren, T., Whitehead, S., Woodward, J., Volckaert, G., Aert, R., Robben, J., Grymonprez, B., Weltjens, I., Vanstreels, E., Rieger, M., Schafer, M., Muller-Auer, S., Gabel, C., Fuchs, M., Dusterhoft, A., Fritzc, C., Holzer, E., Moestl, D., Hilbert, H., Borzym, K., Langer, I., Beck, A., Lehrach, H., Reinhardt, R., Pohl, T. M., Eger, P., Zimmermann, W., Wedler, H., Wambutt, R., Purnelle, B., Goffeau, A., Cadieu, E., Dreano, S., Gloux, S., Lelaure, V., Mottier, S., Galibert, F., Aves, S. J., Xiang, Z., Hunt, C., Moore, K., Hurst, S. M., Lucas, M., Rochet, M., Gaillardin, C., Tallada, V. A., Garzon, A., Thode, G., Daga, R. R., Cruzado, L., Jimenez, J., Sanchez, M., del Rey, F., Benito, J., Dominguez, A., Revuelta, J. L., Moreno, S., Armstrong, J., Forsburg, S. L., Cerutti, L., Lowe, T., McCombie, W. R., Paulsen, I., Potashkin, J., Shpakovski, G. V., Ussery, D., Barrell, B. G., and Nurse, P., The genome sequence of Schizosaccharomyces pombe. Nature, 415, 871–880 (2002).
  • 6) De Groot, P. W. J., Hellingwerf, K. J., and Klis, F. M., Genome-wide identification of fungal GPI proteins. Yeast, 20, 781–796 (2003).
  • 7) Eisenhaber, B., Schneider, G., Wildpaner, M., and Eisenhaber, F., 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 (2004).
  • 8) Henrissat, B., A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem. J., 280, 309–316 (1991).
  • 9) Prieto, J. A., Bort, B. R., Martinez, J., Randez-Gil, F., Buesa, C., and Sanz, P., Purification and characterization of new alpha-amylase of intermediate thermal stability from the yeast Lipomyces konoenkoae. Biochem. Cell Biol., 73, 41–49 (1995).
  • 10) Moranelli, F., Yaguchi, M., Calleja, B., and Nasim, A., Purification and characterization of the extracellular alpha-amylase activity of the yeast Schwanniomyces alluvius. Biochem. Cell Biol., 65, 899–908 (1987).
  • 11) Wilson, J. J., and Ingledew, W. M., Isolation and characterization of Schwanniomyces alluvius amylolytic enzymes. Appl. Environ. Microbiol., 44, 301–307 (1982).
  • 12) De Mot, R., and Verachtert, H., Secretion of α-amylase and multiple forms of glucoamylase by the yeast Trichosporon pullulans. Can. J. Microbiol., 32, 47–51 (1986).
  • 13) De Mot, R., and Verachtert, H., Purification and characterization of extracellular α-amylase and glucoamilase from yeast Candida Antarctica CBS6678. Eur. J. Biochem., 164, 643–654 (1987).
  • 14) Wanderley, K. J., Torres, F. A. G., Moraes, L. M. P., and Ulhoa, C. J., Biochemical characterization of α-amylase from the yeast Cryptococcus flavus. FEMS Microbiol. Lett., 231, 165–169 (2004).
  • 15) Tokunaga, S., Kawamura, A., Yonekyu, S., Kishida, M., and Hishinuma, F., Secretion of mouse alpha-amylase from fission yeast Schizosaccharomyces pombe: presence of Chymostatin-sensitive protease activity in the culture medium. Yeast, 9, 379–387 (1993).
  • 16) Iwaki, T., Tanaka, N., Takagi, H., Hama, Y. G., and Takagawa, K., Characterization of end4 +, a gene required for endocytosis in Schizosaccharomyces pombe. Yeast, 21, 867–881 (2004).
  • 17) Moreno, S., Klar, A., and Nurse, P., Molecular genetic analysis of the fission yeast Schizosaccharomyces pombe. Methods Enzymol., 194, 795–823 (1991).
  • 18) Morita, T., and Takegawa, K., A simple and efficient procedure for transformation of Schizosaccharomyces pombe. Yeast, 21, 613–617 (2004).
  • 19) Janecek, S., α-Amylase family: molecular biology and evolution. Prog. Biophys. Molec. Biol., 67, 67–97 (1997).
  • 20) MacGregor, E. A., Janecek, S., and Svensson, B., Relationship of sequence and structure to specificity in the α-amylase family of enzymes. Biochem. Biophys. Acta, 1546, 1–20 (2001).
  • 21) Hochstenbach, F., Klis, F. M., Van Den Ende, H., Van Donselaar, E., Peters, P. J., and Klausner, R. D., Identification of a putative alpha-glucan synthase essential for cell wall construction and morphogenesis in fission yeast. Proc. Natl. Acad. Sci. USA, 95, 9161–9166 (1998).
  • 22) Katayama, S., Hirata, D., Arellano, M., Pérez, P., and Toda, T., Fission yeast α-glucan synthase Mok1 requires the actin cytoskeleton to localize the site of growth and plays an essential role in cell morphogenesis downstream of protein kinase C function. J. Cell. Biol., 144, 1173–1186 (1999).
  • 23) Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., and Smith, F., Colorimetric method for determination of sugars and related substances. Anal. Chem., 28, 350–356 (1956).
  • 24) Perez, P., and Ribas, J. C., Cell wall analysis. Methods, 33, 245–251 (2004).
  • 25) Laemmli, U. K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 27, 680–685 (1970).
  • 26) Yoko-o, T., Roy, S. K., and Jigami, Y., Difference in in vivo acceptor specificity of two galactosyltransferases, the gmh3 + and gma12 + gene products from Schizosaccharomyces pombe. Eur. J. Biochem., 257, 630–637 (1998).
  • 27) Schweingruber, A. M., Schoenholzer, F., Keller, L., Schwaninger, R., Trachsel, H., and Schweingruber, M. E., Glycosylation and secretion of acid phosphatase in Schizosaccharomyces pombe. Eur. J. Biochem., 158, 133–140 (1986).
  • 28) Martin-Cuadrado, A. B., Dueñas, E., Sipiczki, M., De Aldana, C. R. V., and Del Rey, F., The endo-β-1,3-glucanase eng1p is required for dissolution of the primary septum during cell separation in Schizosaccharomyces pombe. J. Cell Sci., 116, 1689–1698 (2003).
  • 29) Matsuura, Y., Kusunoki, M., Harada, W., and Kakudo, M., Structure and possible catalytic residues of Taka amylase A. J. Biochem., 95, 697–702 (1984).
  • 30) Svensson, B., Protein engineering in the alpha-amylase family: catalytic mechanism, substrate specificity, and stability. Plant Mol. Biol., 25, 141–157 (1994).
  • 31) Braspenning, J., Meschede, W., Marchini, A., Muller, M., Gissmann, L., and Tommasino, M., Secretion of heterologous proteins from Schizosaccharomyces pombe using the homologous leader sequence of pho1 + acid phosphatase. Biochem. Biophys. Res. Commun., 245, 166–171 (1998).
  • 32) Caro, L. H., Tettelin, H., Vossen, J. H., Ram, A. F., van den Ende, H., and Klis, F. M., In silico identification of glycosyla-phosphatidylinositol-anchored plasma-membrane and cell wall proteins of Saccharmyces cerevisiae. Yeast, 13, 1477–1489 (1997).
  • 33) De Sampaio, G., Boudineaud, J. P., and Lauquin, G. J., A constitutive role for GPI anchors in Saccharomyces cerevisiae: cell wall targeting. Mol. Microbiol., 34, 247–256 (1999).
  • 34) Kopecká, M., Fleet, G. H., and Phaff, H. F., Ultrastructure of the cell wall of Schizosaccharomyces pombe following treatment with various glucanases. J. Struct. Biol., 114, 140–152 (1995).
  • 35) Manners, D. J., and Meyer, M. T., The molecular structure of some glucans from the cell wall of Schizosaccharomyces pombe. Carbohydr. Res., 57, 189–203 (1977).
  • 36) Arellano, M., Coll, P. M., and Pérez, P., RHO GTPases in the control of cell morphology, cell polarity, and actin localization in fission yeast. Microsc. Res. Tech., 47, 51–60 (1999).
  • 37) Verde, F., On growth and form: control of cell morphogenesis in fission yeast. Curr. Opin. Microbiol., 1, 712–718 (1998).
  • 38) Konomi, M., Fujimoto, K., Toda, T., and Osumi, M., Characterization and behavior of α-glucan synthase in Schizosaccharomyces pombe as revealed by electron microscopy. Yeast, 20, 427–438 (2003).
  • 39) Mouyna, I., Fontaine, T., Vai, M., Monod, M., Fonzi, W. A., Diaquin, M., Popolo, L., Hartland, R. P., and Latge, J. P., Glycosylphosphatidylinositol-anchored glucanosyltransferases play an active role in the biosynthesis of the fungal cell wall. J. Biol. Chem., 275, 14882–14889 (2000).
  • 40) Dekker, N., Speijer, D., Grün, C. H., Van Den Berg, M., De Haan, A., and Hochstenbach, F., Role of the alpha-glucanase Agn1p in fission-yeast cell separation. Mol. Biol. Cell, 15, 3903–3914 (2004).
  • 41) Popolo, L., and Vai, M., The Gas1 glycoprotein, a putative wall polymer cross-linker. Biochim. Biophys. Acta, 1426, 385–400 (1999).
  • 42) Sarthy, A. V., McGonigal, T., Coen, M., Frost, D. J., Meulbroek, J. A., and Goldman, R. C., Phenotype in Candida albicans of a disruption of the BGL2 gene encoding a 1,3-β-glucosyltransferase. Microbiology, 143, 367–376 (1997).
  • 43) Kalebina, T. S., Farkas, V., Laurinavichiute, D. K., Gorlovoy, P. M., Fominov, G. V., Bartek, P., and Kulaev, I. S., Deletion of BGL2 results in an increased chitin level in the cell wall of Saccharomyces cerevisiae. Antonie van Leeuwenhoek, 84, 179–184 (2003).
  • 44) Watanabe, T., Miyashita, K., Sato, T. T., Yoneki, T., Kakihara, Y., Nabeshima, K., Kishi, Y. A., Shimoda, C., and Nojima, H., Comprehensive isolation of meiosis-specific genes identities novel proteins and usual non-coding transcripts in Schizosaccharomyces pombe. Nucl. Acids Res., 29, 2327–2337 (2001).

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