SUN proteins belong to a novel family of β-(1,3)-glucanmodifying enzymes involved in fungal morphogenesis

Journal of Biological Chemistry

Volumn 288, Issue 19, 2013, Pages 13387-13396

  Gastebois, Amandine ^a,c   Aimanianda, Vishukumar ^a   Bachellier Bassi, Sophie ^a,b   Nesseir, Audrey ^a,b   Firon, Arnaud ^a   Beauvais, Anne ^a   Schmitt, Christine ^a   England, Patrick ^a   Beau, Rémi ^a   Prévost, Marie Christine ^a   D'Enfert, Christophe ^a   Latgé, Jean Paul ^a   Mouyna, Isabelle ^a  

^a INSTITUT PASTEUR   (France)

^b CEMAGREF   (France)

^c LABORATOIRE DES INTERACTIONS PLANTES MICROORGANISMES LIPM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ASPERGILLUS FUMIGATUS; BIOCHEMICAL PROPERTIES; CANDIDA ALBICANS; GLUCANASE; MODE OF ACTION;

ASPERGILLUS; MORPHOLOGY; YEAST;

RECOMBINANT PROTEINS;

1,3 BETA GLUCAN SYNTHASE; 1,3 BETA GLUCANASE; FUNGAL PROTEIN; SUN PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; ASPERGILLUS FUMIGATUS; BIOGENESIS; CANDIDA ALBICANS; CONTROLLED STUDY; DEGLYCOSYLATION; ENZYME ACTIVITY; FUNGAL GENE; FUNGAL MORPHOGENESIS; FUNGUS GROWTH; GENE IDENTIFICATION; GENE INACTIVATION; MORPHOGENESIS; NCA3 GENE; NONHUMAN; OPEN READING FRAME; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; QUANTITATIVE ANALYSIS; REVERSE GENETICS; REVERSE TRANSCRIPTION; RNA EXTRACTION; SACCHAROMYCES CEREVISIAE; SIM1 GENE; UTH1 GENE;

ASPERGILLUS; ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; CARBOHYDRATE-BINDING PROTEIN; CELL WALL; GLUCAN HYDROLASE ACTIVITY; GLYCOSIDE HYDROLASES; SUN;

AMINO ACID SEQUENCE; ASPERGILLUS FUMIGATUS; CANDIDA ALBICANS; FUNGAL PROTEINS; GENE EXPRESSION; GENE EXPRESSION REGULATION, FUNGAL; GLYCOPROTEINS; GLYCOSIDE HYDROLASES; GLYCOSYLATION; HYDROLYSIS; HYPHAE; MOLECULAR SEQUENCE DATA; MORPHOGENESIS; OLIGOSACCHARIDES; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEQUENCE HOMOLOGY, AMINO ACID; SPORES, FUNGAL;

EID: 84877721038     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.440172     Document Type: Article

References (45)

1. Camougrand, N., Kissová, I., Velours, G., and Manon, S. (2004) Uth1p: a yeast mitochondrial protein at the crossroads of stress, degradation, and cell death. FEMS Yeast Res. 5, 133-140
2. Camougrand, N. M., Mouassite, M., Velours, G. M., and Guérin, M. G. (2000) The "SUN" family: UTH1, an ageing gene, is also involved in the regulation of mitochondria biogenesis in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 375, 154-160
3. Mouassite, M., Camougrand, N., Schwob, E., Demaison, G., Laclau, M., and Guérin, M. (2000) The 'SUN' family: yeast SUN4/SCW3 is involved in cell septation. Yeast 16, 905-919
4. Finn, R. D., Mistry, J., Schuster-Böckler, B., Griffiths-Jones, S., Hollich, V., Lassmann, T., Moxon, S., Marshall, M., Khanna, A., Durbin, R., Eddy, S. R., Sonnhammer, E. L., and Bateman, A. (2006) Pfam: clans, web tools, and services. Nucleic Acids Res. 34, D247-D251
5. Bandara, P. D., Flattery-O'Brien, J. A., Grant, C. M., and Dawes, I. W. (1998) Involvement of the Saccharomyces cerevisiae UTH1 gene in the oxidative-stress response. Curr. Genet. 34, 259-268
6. Ritch, J. J., Davidson, S. M., Sheehan, J. J., and Austriaco, N. (2010) The Saccharomyces SUN gene, UTH1, is involved in cell wall biogenesis. FEMS Yeast Res. 10, 168-176
7. +, a new essential fission yeast gene involved in cell wall synthesis. Biochem. Biophys. Res. Commun. 262, 368-374
8. Firon, A., Aubert, S., Iraqui, I., Guadagnini, S., Goyard, S., Prévost, M. C., Janbon, G., and d'Enfert, C. (2007) The SUN41 and SUN42 genes are essential for cell separation in Candida albicans. Mol. Microbiol. 66, 1256-1275
9. Hiller, E., Heine, S., Brunner, H., and Rupp, S. (2007) Candida albicans Sun41p, a putative glycosidase, is involved in morphogenesis, cell wall biogenesis, and biofilm formation. Eukaryot. Cell 6, 2056-2065
10. Norice, C. T., Smith, F. J., Jr., Solis, N., Filler, S. G., and Mitchell, A. P. (2007) Requirement for Candida albicans Sun41 in biofilm formation and virulence. Eukaryot. Cell 6, 2046-2055
11. Sorgo, A. G., Heilmann, C. J., Dekker, H. L., Brul, S., de Koster, C. G., and Klis, F. M. (2010) Mass spectrometric analysis of the secretome of Candida albicans. Yeast 27, 661-672
12. Sosinska, G. J., de Groot, P. W., Teixeira de Mattos, M. J., Dekker, H. L., de Koster, C. G., Hellingwerf, K. J., and Klis, F. M. (2008) Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. Microbiology 154, 510-520
13. da Silva Ferreira, M. E., Kress, M. R., Savoldi, M., Goldman, M. H., Härtl, A., Heinekamp, T., Brakhage, A. A., and Goldman, G. H. (2006) The akuBKU80 mutant deficient for nonhomologous end joining is a powerful tool for analyzing pathogenicity in Aspergillus fumigatus. Eukaryot. Cell 5, 207-211
14. Cove, D. J. (1966) The induction and repression of nitrate reductase in the fungus Aspergillus fumigatus. Biochim. Biophys. Acta 113, 51-56
15. Wilson, R. B., Davis, D., and Mitchell, A. P. (1999) Rapid hypothesis testing with Candida albicans through gene disruption with short homology regions. J. Bacteriol. 181, 1868-1874
16. Lambou, K., Lamarre, C., Beau, R., Dufour, N., and Latge, J. P. (2010) Functional analysis of the superoxide dismutase family in Aspergillus fumigatus. Mol. Microbiol. 75, 910-923
17. Mouyna, I., Kniemeyer, O., Jank, T., Loussert, C., Mellado, E., Aimanianda, V., Beauvais, A., Wartenberg, D., Sarfati, J., Bayry, J., Prévost, M. C., Brakhage, A. A., Strahl, S., Huerre, M., and Latgé, J. P. (2010) Members of protein O-mannosyltransferase family in Aspergillus fumigatus differentially affect growth, morphogenesis and viability. Mol. Microbiol. 76, 1205-1221
18. Lamarre, C., Ibrahim-Granet, O., Du, C., Calderone, R., and Latgé, J. P. (2007) Characterization of the SKN7 ortholog of Aspergillus fumigatus. Fungal. Genet. Biol. 44, 682-690
19. Punt, P. J., Oliver, R. P., Dingemanse, M. A., Pouwels, P. H., and van den Hondel, C. A. (1987) Transformation of Aspergillus based on the hygromycin B resistance marker from Escherichia coli. Gene 56, 117-124
20. Girardin, H., Latgé, J. P., Srikantha, T., Morrow, B., and Soll, D. R. (1993) Development of DNA probes for fingerprinting Aspergillus fumigatus. J. Clin. Microbiol. 31, 1547-1554
21. Sánchez, M., Iglesias, F. J., Santamaría, C., and Domínguez, A. (1993) Transformation of Kluyveromyces lactis by electroporation. Appl. Environ. Microbiol. 59, 2087-2092
22. Weidner, G., d'Enfert, C., Koch, A., Mol, P. C., and 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
23. Diaz-Guerra, T. M., Mellado, E., Cuenca-Estrella, M., and Rodriguez-Tudela, J. L. (2003) A point mutation in the 14α-sterol demethylase gene cyp51A contributes to itraconazole resistance in Aspergillus fumigatus. Antimicrob. Agents Chemother. 47, 1120-1124
24. Desai, N. N., Allen, A. K., and Neuberger, A. (1983) The properties of potato (Solanum tuberosum) lectin after deglycosylation by trifluoro- methanesulphonic acid. Biochem. J. 211, 273-276
25. Richie, D. L., Hartl, L., Aimanianda, V., Winters, M. S., Fuller, K. K., Miley, M. D., White, S., McCarthy, J. W., Latgé, J. P., Feldmesser, M., Rhodes, J. C., and Askew, D. S. (2009) A role for the unfolded protein response (UPR) in virulence and antifungal susceptibility in Aspergillus fumigatus. PLoS Pathog. 5, e1000258
26. Wang, H. X., Douglas, L. M., Aimanianda, V., Latgé, J. P., and Konopka, J. B. (2011) The Candida albicans Sur7 protein is needed for proper synthesis of the fibrillar component of the cell wall that confers strength. Eukaryot. Cell 10, 72-80
27. Wei, Y., Zhao, W., Zhang, Q., Zhao, Y., and Zhang, Y. (2011) Purification and characterization of a novel and unique ginsenoside Rg1-hydrolyzing β-D-glucosidase from Penicillium sclerotiorum. Acta Biochim. Biophys. Sin. (Shanghai) 43, 226-231
28. Martín-Cuadrado, A. B., Encinar del Dedo, J., de Medina-Redondo, M., Fontaine, T., del Rey, F., Latgé, J. P., and Vázquez de Aldana, C. R. (2008) The Schizosaccharomyces pombe endo-1,3-β-glucanase Eng1 contains a novel carbohydrate binding module required for septum localization. Mol. Microbiol. 69, 188-200
29. Emanuelsson, O., Brunak, S., von Heijne, G., and Nielsen, H. (2007) Locating proteins in the cell using TargetP, SignalP, and related tools. Nat. Protoc. 2, 953-971
30. Eisenhaber, B., Schneider, G., Wildpaner, M., and Eisenhaber, F. (2004) 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
31. Rau, U., Gura, E., Olszewski, E., and Wagner, F. (1992) Enhanced glucan formation of filamentous fungi by effective mixing, oxygen limitation, and fed-batch processing. J. Ind. Microbiol. 9, 19-26
32. Xu, Z., Shih, M. C., and Poulton, J. E. (2006) An extracellular exo-β-(1,3)-glucanase from Pichia pastoris: purification, characterization, molecular cloning, and functional expression. Protein Expr. Purif. 47, 118-127
33. Trinci, A. P., and Collinge, A. J. (1974) Occlusion of the septal pores of damaged hyphae of Neurospora crassa by hexagonal crystals. Protoplasma 80, 57-67
34. Takeshita, N., Yamashita, S., Ohta, A., and Horiuchi, H. (2006) s 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
35. Jiménez-Ortigosa, C., Aimanianda, V., Muszkieta, L., Mouyna, I., Alsteens, D., Pire, S., Beau, R., Krappmann, S., Beauvais, A., Dufrêne, Y. F., Roncero, C., and Latgé, J. P. (2012) Chitin synthases with a myosin motorlike domain control the resistance of Aspergillus fumigatus to echinocandins. Antimicrob. Agents Chemother. 56, 6121-6131
36. Guyard, C., Cailliez, J. C., Tissier, J. P., Dei-Cas, E., Mercenier, A., and Menozzi, F. D. (2002) Cloning and characterization of WMSU1, a Williopsis saturnus var. mrakii gene encoding a new yeast SUN protein involved in the cell wall structure. Yeast 19, 1127-1138
37. Guyard, C., Séguy, N., Cailliez, J. C., Drobecq, H., Polonelli, L., Dei-Cas, E., Mercenier, A., and Menozzi, F. D. (2002) Characterization of a Williopsis saturnus var. mrakii high molecular weight secreted killer toxin with broad-spectrum antimicrobial activity. J. Antimicrob. Chemother. 49, 961-971
38. Alonso-Nuñez, M. L., An, H., Martín-Cuadrado, A. B., Mehta, S., Petit, C., Sipiczki, M., del Rey, F., Gould, K. L., and de Aldana, C. R. (2005) Ace2p controls the expression of genes required for cell separation in Schizosaccharomyces pombe. Mol. Biol. Cell 16, 2003-2017
39. Skory, C. D., and Freer, S. N. (1995) Cloning and characterization of a gene encoding a cell-bound, extracellular β-glucosidase in the yeast Candida wickerhamii. Appl. Environ. Microbiol. 61, 518-525
40. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for glycogenomics. Nucleic Acids Res. 37, D233-D238
41. Zverlov, V. V., Volkov, I. Y., Velikodvorskaya, T. V., and Schwarz, W. H. (1997) Thermotoga neapolitana bglB gene, upstream of lamA, encodes a highly thermostable β-glucosidase that is a laminaribiase. Microbiology 143, 3537-3542
42. Fontaine, T., Hartland, R. P., Diaquin, M., Simenel, C., and Latgé, J. P. (1997) Differential patterns of activity displayed by two exo-β-1,3-glucanases associated with the Aspergillus fumigatus cell wall. J. Bacteriol. 179, 3154-3163
43. Mishima, Y., Quintin, J., Aimanianda, V., Kellenberger, C., Coste, F., Clavaud, C., Hetru, C., Hoffmann, J. A., Latgé, J. P., Ferrandon, D., and Roussel, A. (2009) The N-terminal domain of Drosophila Gram-negative binding protein 3 (GNBP3) defines a novel family of fungal pattern recognition receptors. J. Biol. Chem. 284, 28687-28697
44. Roncero, C., and Sánchez, Y. (2010) Cell separation and the maintenance of cell integrity during cytokinesis in yeast: the assembly of a septum. Yeast 27, 521-530
45. Sipiczki, M. (2007) Splitting of the fission yeast septum. FEMS Yeast Res. 7, 761-770