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

Authors :
Christine Schmitt
Christophe d'Enfert
Audrey Nesseir
Anne Beauvais
Patrick England
Vishukumar Aimanianda
Rémi Beau
Arnaud Firon
Marie-Christine Prévost
Amandine Gastebois
Sophie Bachellier-Bassi
Jean-Paul Latgé
Isabelle Mouyna
Aspergillus
Institut Pasteur [Paris]
Biologie et Pathogénicité fongiques
Institut Pasteur [Paris]-Institut National de la Recherche Agronomique (INRA)
Microscopie ultrastructurale (plate-forme)
Biochimie et Biophysique des Macromolécules (Plate-forme)
Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS)
This work was supported by grants from the European Commission (Galar Fungail 2, MRTN-CT-2003-504148
FINSysB, PITN-GA-2008-214004) (to C. d. E.) and the European Science Foundation (ESF) Fuminomics, Partenariat Sanofi-aventis-Aviesan (ITMO Maladies Infectieuses, Sanofi Aventis Research & Development TSU ID (SAR&D) TSU ID/Sanofi-Pasteur), and Agence Nationale de Recherches (ANR) (Grant 09-BLAN-0287) (to J. P. L.)
ANR-09-BLAN-0287,REMODELE,Nouvelles voies métaboliques essentielles pour la biosynthèse de la paroi des champignons(2009)
European Project: 214004,PEOPLE,FP7-PEOPLE-2007-1-1-ITN,FINSYSB(2008)
Institut Pasteur [Paris] (IP)
Biologie et Pathogénicité fongiques (BPF)
Institut National de la Recherche Agronomique (INRA)-Institut Pasteur [Paris] (IP)
Institut Pasteur [Paris] (IP)-Centre National de la Recherche Scientifique (CNRS)
Institut National de la Recherche Agronomique (INRA)-Institut Pasteur [Paris]
Biophysique des macromolécules et de leurs interactions
ANR Grant 09-BLAN-0287,ANR Grant 09-BLAN-0287,Grant 09-BLAN-0287
Institut National de la Recherche Agronomique (INRA) - Institut Pasteur [Paris]
Microscopie ultrastructurale - Ultrapole (CITECH)
Biophysique des macromolécules et leurs interactions
Institut Pasteur [Paris] - Centre National de la Recherche Scientifique (CNRS)
Source :
Journal of Biological Chemistry, Journal of Biological Chemistry, American Society for Biochemistry and Molecular Biology, 2013, 288 (19), pp.13387-96. ⟨10.1074/jbc.M112.440172⟩, Journal of Biological Chemistry, 2013, 288 (19), pp.13387-96. ⟨10.1074/jbc.M112.440172⟩, Journal of Biological Chemistry 19 (288), 13387-13396. (2013), Journal of Biological Chemistry, American Society for Biochemistry and Molecular Biology, 2013, 288 (19), pp.13387-13396. 〈10.1074/jbc.M112.440172〉
Publication Year :
2013
Publisher :
HAL CCSD, 2013.

Abstract

International audience; BACKGROUND:SUN proteins are involved in yeast morphogenesis, but their function is unknown.RESULTS:SUN protein plays a role in the Aspergillus fumigatus morphogenesis. Biochemical properties of recombinant SUN proteins were elucidated.CONCLUSION:Both Candida albicans and Aspergillus fumigatus sun proteins show a β-(1,3)-glucanase activity.SIGNIFICANCE:The mode of action of SUN proteins on β-(1,3)-glucan is unique, new, and original. In yeasts, the family of SUN proteins has been involved in cell wall biogenesis. Here, we report the characterization of SUN proteins in a filamentous fungus, Aspergillus fumigatus. The function of the two A. fumigatus SUN genes was investigated by combining reverse genetics and biochemistry. During conidial swelling and mycelial growth, the expression of AfSUN1 was strongly induced, whereas the expression of AfSUN2 was not detectable. Deletion of AfSUN1 negatively affected hyphal growth and conidiation. A closer examination of the morphological defects revealed swollen hyphae, leaky tips, intrahyphal growth, and double cell wall, suggesting that, like in yeast, AfSun1p is associated with cell wall biogenesis. In contrast to AfSUN1, deletion of AfSUN2 either in the parental strain or in the AfSUN1 single mutant strain did not affect colony and hyphal morphology. Biochemical characterization of the recombinant AfSun1p and Candida albicans Sun41p showed that both proteins had a unique hydrolysis pattern: acting on β-(1,3)-oligomers from dimer up to insoluble β-(1,3)-glucan. Referring to the CAZy database, it is clear that fungal SUN proteins represent a new family of glucan hydrolases (GH132) and play an important morphogenetic role in fungal cell wall biogenesis and septation.

Subjects

Subjects :
Hyphal growth
MESH : Spores, Fungal
MESH : Molecular Sequence Data
Glycosylation
MESH: Sequence Homology, Amino Acid
Conidiation
Gene Expression
Oligosaccharides
Glycobiology and Extracellular Matrices
MESH: Amino Acid Sequence
Biochemistry
Aspergillus fumigatus
Cell Wall
Gene Expression Regulation, Fungal
Candida albicans
Morphogenesis
MESH : Fungal Proteins
skin and connective tissue diseases
[SDV.MP.MYC]Life Sciences [q-bio]/Microbiology and Parasitology/Mycology
0303 health sciences
integumentary system
MESH : Amino Acid Sequence
Hydrolysis
MESH : Glycosylation
Glucan Hydrolase Activity
SUN
MESH : Protein Binding
MESH : Glycoside Hydrolases
Spores, Fungal
MESH: Glycosylation
MESH : Sequence Homology, Amino Acid
Cell biology
[SDV] Life Sciences [q-bio]
Aspergillus
CELL-WALL BIOGENESIS
MOTOR-LIKE DOMAIN
ASPERGILLUS-FUMIGATUS
CANDIDA-ALBICANS
SCHIZOSACCHAROMYCES-POMBE
SACCHAROMYCES-CEREVISIAE
BIOFILM FORMATION
BETA-GLUCOSIDASE
CHITIN SYNTHASES
GENE
MESH: Fungal Proteins
MESH: Aspergillus fumigatus
MESH: Gene Expression Regulation, Fungal
MESH: Hydrolysis
Protein Binding
CAZy
MESH: Gene Expression
Hypha
MESH : Candida albicans
Glycoside Hydrolases
Molecular Sequence Data
Hyphae
MESH: Glycoproteins
Biology
Microbiology
Cell wall
Fungal Proteins
03 medical and health sciences
MESH : Hydrolysis
MESH: Hyphae
MESH: Spores, Fungal
MESH : Gene Expression Regulation, Fungal
MESH: Glycoside Hydrolases
MESH: Protein Binding
Amino Acid Sequence
Molecular Biology
030304 developmental biology
MESH : Protein Processing, Post-Translational
Glycoproteins
MESH: Molecular Sequence Data
Sequence Homology, Amino Acid
030306 microbiology
MESH: Candida albicans
MESH : Oligosaccharides
Cell Biology
biology.organism_classification
MESH : Glycoproteins
[SDV.MP.MYC] Life Sciences [q-bio]/Microbiology and Parasitology/Mycology
Yeast
MESH: Morphogenesis
MESH : Gene Expression
MESH : Morphogenesis
MESH : Aspergillus fumigatus
MESH: Protein Processing, Post-Translational
MESH : Hyphae
Carbohydrate-binding Protein
Protein Processing, Post-Translational
MESH: Oligosaccharides
Biogenesis

Details

Language :
English
ISSN :
00219258 and 1083351X
Database :
OpenAIRE
Journal :
Journal of Biological Chemistry, Journal of Biological Chemistry, American Society for Biochemistry and Molecular Biology, 2013, 288 (19), pp.13387-96. ⟨10.1074/jbc.M112.440172⟩, Journal of Biological Chemistry, 2013, 288 (19), pp.13387-96. ⟨10.1074/jbc.M112.440172⟩, Journal of Biological Chemistry 19 (288), 13387-13396. (2013), Journal of Biological Chemistry, American Society for Biochemistry and Molecular Biology, 2013, 288 (19), pp.13387-13396. 〈10.1074/jbc.M112.440172〉
Accession number :
edsair.doi.dedup.....9a6f9df74669906a54aa3de73b481161