Changes in glucosylceramide structure affect virulence and membrane biophysical properties of Cryptococcus neoformans.
Identifieur interne : 004D87 ( Ncbi/Curation ); précédent : 004D86; suivant : 004D88Changes in glucosylceramide structure affect virulence and membrane biophysical properties of Cryptococcus neoformans.
Auteurs : Shriya Raj [France] ; Saeed Nazemidashtarjandi [États-Unis] ; Jihyun Kim [États-Unis] ; Luna Joffe [Brésil] ; Xiaoxue Zhang [États-Unis] ; Ashutosh Singh [États-Unis] ; Visesato Mor [États-Unis] ; Desmarini Desmarini [Australie] ; Julianne Djordjevic [Australie] ; Daniel P. Raleigh [États-Unis] ; Marcio L. Rodrigues [Brésil] ; Erwin London [États-Unis] ; Maurizio Del Poeta [États-Unis] ; Amir M. Farnoud [États-Unis]Source :
- Biochimica et biophysica acta [ 0006-3002 ] ; 2017.
Abstract
Fungal glucosylceramide (GlcCer) is a plasma membrane sphingolipid in which the sphingosine backbone is unsaturated in carbon position 8 (C8) and methylated in carbon position 9 (C9). Studies in the fungal pathogen, Cryptococcus neoformans, have shown that loss of GlcCer synthase activity results in complete loss of virulence in the mouse model. However, whether the loss of virulence is due to the lack of the enzyme or to the loss of the sphingolipid is not known. In this study, we used genetic engineering to alter the chemical structure of fungal GlcCer and studied its effect on fungal growth and pathogenicity. Here we show that unsaturation in C8 and methylation in C9 is required for virulence in the mouse model without affecting fungal growth in vitro or common virulence factors. However, changes in GlcCer structure led to a dramatic susceptibility to membrane stressors resulting in increased cell membrane permeability and rendering the fungal mutant unable to grow within host macrophages. Biophysical studies using synthetic vesicles containing GlcCer revealed that the saturated and unmethylated sphingolipid formed vesicles with higher lipid order that were more likely to phase separate into ordered domains. Taken together, these studies show for the first time that a specific structure of GlcCer is a major regulator of membrane permeability required for fungal pathogenicity.
DOI: 10.1016/j.bbamem.2017.08.017
PubMed: 28865794
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Engineering, Ohio University, Athens, OH, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemical and Biomolecular Engineering, Ohio University, Athens, OH</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Kim, Jihyun" sort="Kim, Jihyun" uniqKey="Kim J" first="Jihyun" last="Kim">Jihyun Kim</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Joffe, Luna" sort="Joffe, Luna" uniqKey="Joffe L" first="Luna" last="Joffe">Luna Joffe</name><affiliation wicri:level="1"><nlm:affiliation>Departamento de 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Ashutosh" sort="Singh, Ashutosh" uniqKey="Singh A" first="Ashutosh" last="Singh">Ashutosh Singh</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Mor, Visesato" sort="Mor, Visesato" uniqKey="Mor V" first="Visesato" last="Mor">Visesato Mor</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Desmarini, Desmarini" sort="Desmarini, Desmarini" uniqKey="Desmarini D" first="Desmarini" last="Desmarini">Desmarini Desmarini</name><affiliation wicri:level="1"><nlm:affiliation>Fungal Pathogenesis Laboratory, Centre for Infectious Diseases and Microbiology, The Westmead Institute for Medical Research, Westmead, NSW, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Fungal Pathogenesis Laboratory, Centre for Infectious Diseases and Microbiology, The Westmead Institute for Medical Research, Westmead, NSW</wicri:regionArea><wicri:noRegion>NSW</wicri:noRegion></affiliation></author><author><name sortKey="Djordjevic, Julianne" sort="Djordjevic, Julianne" uniqKey="Djordjevic J" first="Julianne" last="Djordjevic">Julianne Djordjevic</name><affiliation wicri:level="1"><nlm:affiliation>Fungal Pathogenesis Laboratory, Centre for Infectious Diseases and Microbiology, The Westmead Institute for Medical Research, Westmead, NSW, Australia; Westmead Clinical School, University of Sydney at Westmead Hospital, Westmead, NSW, Australia; Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, NSW, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Fungal Pathogenesis Laboratory, Centre for Infectious Diseases and Microbiology, The Westmead Institute for Medical Research, Westmead, NSW, Australia; Westmead Clinical School, University of Sydney at Westmead Hospital, Westmead, NSW, Australia; Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, NSW</wicri:regionArea><wicri:noRegion>NSW</wicri:noRegion></affiliation></author><author><name sortKey="Raleigh, Daniel P" sort="Raleigh, Daniel P" uniqKey="Raleigh D" first="Daniel P" last="Raleigh">Daniel P. Raleigh</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Rodrigues, Marcio L" sort="Rodrigues, Marcio L" uniqKey="Rodrigues M" first="Marcio L" last="Rodrigues">Marcio L. Rodrigues</name><affiliation wicri:level="3"><nlm:affiliation>Departamento de Microbiologia Geral, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro (UFRJ), Brazil; Centro de Desenvolvimento Tecnológico em Saúde (CDTS) da Fundação Oswaldo Cruz (Fiocruz), Rio de Janeiro, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Departamento de Microbiologia Geral, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro (UFRJ), Brazil; Centro de Desenvolvimento Tecnológico em Saúde (CDTS) da Fundação Oswaldo Cruz (Fiocruz), Rio de Janeiro</wicri:regionArea><placeName><settlement type="city">Rio de Janeiro</settlement><region type="state">État de Rio de Janeiro</region></placeName></affiliation></author><author><name sortKey="London, Erwin" sort="London, Erwin" uniqKey="London E" first="Erwin" last="London">Erwin London</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Del Poeta, Maurizio" sort="Del Poeta, Maurizio" uniqKey="Del Poeta M" first="Maurizio" last="Del Poeta">Maurizio Del Poeta</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY, USA; Veterans Administration Medical Center, Northport, NY, USA; Division of Infectious Diseases, Stony Brook University, Stony Brook, NY, USA. Electronic address: maurizio.delpoeta@stonybrook.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY, USA; Veterans Administration Medical Center, Northport, NY, USA; Division of Infectious Diseases, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Farnoud, Amir M" sort="Farnoud, Amir M" uniqKey="Farnoud A" first="Amir M" last="Farnoud">Amir M. Farnoud</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemical and Biomolecular Engineering, Ohio University, Athens, OH, USA. Electronic address: farnoud@ohio.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemical and Biomolecular Engineering, Ohio University, Athens, OH</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PubMed</idno><date when="2017">2017</date><idno type="RBID">pubmed:28865794</idno><idno type="pmid">28865794</idno><idno type="doi">10.1016/j.bbamem.2017.08.017</idno><idno type="wicri:Area/PubMed/Corpus">000078</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Corpus" wicri:corpus="PubMed">000078</idno><idno type="wicri:Area/PubMed/Curation">000078</idno><idno type="wicri:explorRef" wicri:stream="PubMed" wicri:step="Curation">000078</idno><idno type="wicri:Area/PubMed/Checkpoint">000078</idno><idno type="wicri:explorRef" wicri:stream="Checkpoint" wicri:step="PubMed">000078</idno><idno type="wicri:Area/Ncbi/Merge">004D87</idno><idno type="wicri:Area/Ncbi/Curation">004D87</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en">Changes in glucosylceramide structure affect virulence and membrane biophysical properties of Cryptococcus neoformans.</title><author><name sortKey="Raj, Shriya" sort="Raj, Shriya" uniqKey="Raj S" first="Shriya" last="Raj">Shriya Raj</name><affiliation wicri:level="3"><nlm:affiliation>Department of Mycology, Institut Pasteur, Paris, France.</nlm:affiliation><country xml:lang="fr">France</country><wicri:regionArea>Department of Mycology, Institut Pasteur, Paris</wicri:regionArea><placeName><region type="region">Île-de-France</region><region type="old region">Île-de-France</region><settlement type="city">Paris</settlement></placeName></affiliation></author><author><name sortKey="Nazemidashtarjandi, Saeed" sort="Nazemidashtarjandi, Saeed" uniqKey="Nazemidashtarjandi S" first="Saeed" last="Nazemidashtarjandi">Saeed Nazemidashtarjandi</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemical and Biomolecular Engineering, Ohio University, Athens, OH, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemical and Biomolecular Engineering, Ohio University, Athens, OH</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author><author><name sortKey="Kim, Jihyun" sort="Kim, Jihyun" uniqKey="Kim J" first="Jihyun" last="Kim">Jihyun Kim</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Joffe, Luna" sort="Joffe, Luna" uniqKey="Joffe L" first="Luna" last="Joffe">Luna Joffe</name><affiliation wicri:level="1"><nlm:affiliation>Departamento de Microbiologia Geral, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro (UFRJ), Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Departamento de Microbiologia Geral, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro (UFRJ)</wicri:regionArea><wicri:noRegion>Universidade Federal do Rio de Janeiro (UFRJ)</wicri:noRegion></affiliation></author><author><name sortKey="Zhang, Xiaoxue" sort="Zhang, Xiaoxue" uniqKey="Zhang X" first="Xiaoxue" last="Zhang">Xiaoxue Zhang</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Singh, Ashutosh" sort="Singh, Ashutosh" uniqKey="Singh A" first="Ashutosh" last="Singh">Ashutosh Singh</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Mor, Visesato" sort="Mor, Visesato" uniqKey="Mor V" first="Visesato" last="Mor">Visesato Mor</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Desmarini, Desmarini" sort="Desmarini, Desmarini" uniqKey="Desmarini D" first="Desmarini" last="Desmarini">Desmarini Desmarini</name><affiliation wicri:level="1"><nlm:affiliation>Fungal Pathogenesis Laboratory, Centre for Infectious Diseases and Microbiology, The Westmead Institute for Medical Research, Westmead, NSW, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Fungal Pathogenesis Laboratory, Centre for Infectious Diseases and Microbiology, The Westmead Institute for Medical Research, Westmead, NSW</wicri:regionArea><wicri:noRegion>NSW</wicri:noRegion></affiliation></author><author><name sortKey="Djordjevic, Julianne" sort="Djordjevic, Julianne" uniqKey="Djordjevic J" first="Julianne" last="Djordjevic">Julianne Djordjevic</name><affiliation wicri:level="1"><nlm:affiliation>Fungal Pathogenesis Laboratory, Centre for Infectious Diseases and Microbiology, The Westmead Institute for Medical Research, Westmead, NSW, Australia; Westmead Clinical School, University of Sydney at Westmead Hospital, Westmead, NSW, Australia; Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, NSW, Australia.</nlm:affiliation><country xml:lang="fr">Australie</country><wicri:regionArea>Fungal Pathogenesis Laboratory, Centre for Infectious Diseases and Microbiology, The Westmead Institute for Medical Research, Westmead, NSW, Australia; Westmead Clinical School, University of Sydney at Westmead Hospital, Westmead, NSW, Australia; Marie Bashir Institute for Infectious Diseases and Biosecurity, University of Sydney, NSW</wicri:regionArea><wicri:noRegion>NSW</wicri:noRegion></affiliation></author><author><name sortKey="Raleigh, Daniel P" sort="Raleigh, Daniel P" uniqKey="Raleigh D" first="Daniel P" last="Raleigh">Daniel P. Raleigh</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Rodrigues, Marcio L" sort="Rodrigues, Marcio L" uniqKey="Rodrigues M" first="Marcio L" last="Rodrigues">Marcio L. Rodrigues</name><affiliation wicri:level="3"><nlm:affiliation>Departamento de Microbiologia Geral, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro (UFRJ), Brazil; Centro de Desenvolvimento Tecnológico em Saúde (CDTS) da Fundação Oswaldo Cruz (Fiocruz), Rio de Janeiro, Brazil.</nlm:affiliation><country xml:lang="fr">Brésil</country><wicri:regionArea>Departamento de Microbiologia Geral, Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro (UFRJ), Brazil; Centro de Desenvolvimento Tecnológico em Saúde (CDTS) da Fundação Oswaldo Cruz (Fiocruz), Rio de Janeiro</wicri:regionArea><placeName><settlement type="city">Rio de Janeiro</settlement><region type="state">État de Rio de Janeiro</region></placeName></affiliation></author><author><name sortKey="London, Erwin" sort="London, Erwin" uniqKey="London E" first="Erwin" last="London">Erwin London</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemistry and Biochemistry, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Del Poeta, Maurizio" sort="Del Poeta, Maurizio" uniqKey="Del Poeta M" first="Maurizio" last="Del Poeta">Maurizio Del Poeta</name><affiliation wicri:level="2"><nlm:affiliation>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY, USA; Veterans Administration Medical Center, Northport, NY, USA; Division of Infectious Diseases, Stony Brook University, Stony Brook, NY, USA. Electronic address: maurizio.delpoeta@stonybrook.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Molecular Genetics and Microbiology, Stony Brook University, Stony Brook, NY, USA; Veterans Administration Medical Center, Northport, NY, USA; Division of Infectious Diseases, Stony Brook University, Stony Brook, NY</wicri:regionArea><placeName><region type="state">État de New York</region></placeName></affiliation></author><author><name sortKey="Farnoud, Amir M" sort="Farnoud, Amir M" uniqKey="Farnoud A" first="Amir M" last="Farnoud">Amir M. Farnoud</name><affiliation wicri:level="2"><nlm:affiliation>Department of Chemical and Biomolecular Engineering, Ohio University, Athens, OH, USA. Electronic address: farnoud@ohio.edu.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Chemical and Biomolecular Engineering, Ohio University, Athens, OH</wicri:regionArea><placeName><region type="state">Ohio</region></placeName></affiliation></author></analytic><series><title level="j">Biochimica et biophysica acta</title><idno type="ISSN">0006-3002</idno><imprint><date when="2017" type="published">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Fungal glucosylceramide (GlcCer) is a plasma membrane sphingolipid in which the sphingosine backbone is unsaturated in carbon position 8 (C8) and methylated in carbon position 9 (C9). Studies in the fungal pathogen, Cryptococcus neoformans, have shown that loss of GlcCer synthase activity results in complete loss of virulence in the mouse model. However, whether the loss of virulence is due to the lack of the enzyme or to the loss of the sphingolipid is not known. In this study, we used genetic engineering to alter the chemical structure of fungal GlcCer and studied its effect on fungal growth and pathogenicity. Here we show that unsaturation in C8 and methylation in C9 is required for virulence in the mouse model without affecting fungal growth in vitro or common virulence factors. However, changes in GlcCer structure led to a dramatic susceptibility to membrane stressors resulting in increased cell membrane permeability and rendering the fungal mutant unable to grow within host macrophages. Biophysical studies using synthetic vesicles containing GlcCer revealed that the saturated and unmethylated sphingolipid formed vesicles with higher lipid order that were more likely to phase separate into ordered domains. Taken together, these studies show for the first time that a specific structure of GlcCer is a major regulator of membrane permeability required for fungal pathogenicity.</div></front></TEI></record>Pour manipuler ce document sous Unix (Dilib)
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