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Visualization of the heterogeneous membrane distribution of sphingomyelin associated with cytokinesis, cell polarity, and sphingolipidosis.

Identifieur interne : 003029 ( PubMed/Corpus ); précédent : 003028; suivant : 003030

Visualization of the heterogeneous membrane distribution of sphingomyelin associated with cytokinesis, cell polarity, and sphingolipidosis.

Auteurs : Asami Makino ; Mitsuhiro Abe ; Motohide Murate ; Takehiko Inaba ; Neval Yilmaz ; Françoise Hullin-Matsuda ; Takuma Kishimoto ; Nicole L. Schieber ; Tomohiko Taguchi ; Hiroyuki Arai ; Gregor Anderluh ; Robert G. Parton ; Toshihide Kobayashi

Source :

RBID : pubmed:25389132

English descriptors

Abstract

Sphingomyelin (SM) is a major sphingolipid in mammalian cells and is reported to form specific lipid domains together with cholesterol. However, methods to examine the membrane distribution of SM are limited. We demonstrated in model membranes that fluorescent protein conjugates of 2 specific SM-binding toxins, lysenin (Lys) and equinatoxin II (EqtII), recognize different membrane distributions of SM; Lys exclusively binds clustered SM, whereas EqtII preferentially binds dispersed SM. Freeze-fracture immunoelectron microscopy showed that clustered but not dispersed SM formed lipid domains on the cell surface. Glycolipids and the membrane concentration of SM affect the SM distribution pattern on the plasma membrane. Using derivatives of Lys and EqtII as SM distribution-sensitive probes, we revealed the exclusive accumulation of SM clusters in the midbody at the time of cytokinesis. Interestingly, apical membranes of differentiated epithelial cells exhibited dispersed SM distribution, whereas SM was clustered in basolateral membranes. Clustered but not dispersed SM was absent from the cell surface of acid sphingomyelinase-deficient Niemann-Pick type A cells. These data suggest that both the SM content and membrane distribution are crucial for pathophysiological events bringing therapeutic perspective in the role of SM membrane distribution.

DOI: 10.1096/fj.13-247585
PubMed: 25389132

Links to Exploration step

pubmed:25389132

Le document en format XML

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<name sortKey="Hullin Matsuda, Francoise" sort="Hullin Matsuda, Francoise" uniqKey="Hullin Matsuda F" first="Françoise" last="Hullin-Matsuda">Françoise Hullin-Matsuda</name>
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<name sortKey="Inaba, Takehiko" sort="Inaba, Takehiko" uniqKey="Inaba T" first="Takehiko" last="Inaba">Takehiko Inaba</name>
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<nlm:affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</nlm:affiliation>
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<nlm:affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</nlm:affiliation>
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<name sortKey="Hullin Matsuda, Francoise" sort="Hullin Matsuda, Francoise" uniqKey="Hullin Matsuda F" first="Françoise" last="Hullin-Matsuda">Françoise Hullin-Matsuda</name>
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<nlm:affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</nlm:affiliation>
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<name sortKey="Kishimoto, Takuma" sort="Kishimoto, Takuma" uniqKey="Kishimoto T" first="Takuma" last="Kishimoto">Takuma Kishimoto</name>
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<nlm:affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</nlm:affiliation>
</affiliation>
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<name sortKey="Schieber, Nicole L" sort="Schieber, Nicole L" uniqKey="Schieber N" first="Nicole L" last="Schieber">Nicole L. Schieber</name>
<affiliation>
<nlm:affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</nlm:affiliation>
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<name sortKey="Taguchi, Tomohiko" sort="Taguchi, Tomohiko" uniqKey="Taguchi T" first="Tomohiko" last="Taguchi">Tomohiko Taguchi</name>
<affiliation>
<nlm:affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</nlm:affiliation>
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<name sortKey="Arai, Hiroyuki" sort="Arai, Hiroyuki" uniqKey="Arai H" first="Hiroyuki" last="Arai">Hiroyuki Arai</name>
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<nlm:affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</nlm:affiliation>
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<name sortKey="Anderluh, Gregor" sort="Anderluh, Gregor" uniqKey="Anderluh G" first="Gregor" last="Anderluh">Gregor Anderluh</name>
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<nlm:affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</nlm:affiliation>
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<name sortKey="Parton, Robert G" sort="Parton, Robert G" uniqKey="Parton R" first="Robert G" last="Parton">Robert G. Parton</name>
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<nlm:affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</nlm:affiliation>
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<name sortKey="Kobayashi, Toshihide" sort="Kobayashi, Toshihide" uniqKey="Kobayashi T" first="Toshihide" last="Kobayashi">Toshihide Kobayashi</name>
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<nlm:affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia kobayasi@riken.jp.</nlm:affiliation>
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<term>Animals</term>
<term>COS Cells</term>
<term>Cell Membrane (metabolism)</term>
<term>Cell Polarity</term>
<term>Cell Survival</term>
<term>Cercopithecus aethiops</term>
<term>Cytokinesis (physiology)</term>
<term>DNA, Complementary (metabolism)</term>
<term>Enzyme-Linked Immunosorbent Assay</term>
<term>Epithelial Cells (cytology)</term>
<term>Fibroblasts (metabolism)</term>
<term>HeLa Cells</term>
<term>Humans</term>
<term>Infant</term>
<term>Liposomes (metabolism)</term>
<term>Male</term>
<term>Microscopy, Atomic Force</term>
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<term>Microscopy, Immunoelectron</term>
<term>Niemann-Pick Disease, Type A (genetics)</term>
<term>Recombinant Proteins (metabolism)</term>
<term>Sphingomyelins (metabolism)</term>
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<term>DNA, Complementary</term>
<term>Liposomes</term>
<term>Recombinant Proteins</term>
<term>Sphingomyelins</term>
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<term>Epithelial Cells</term>
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<term>Niemann-Pick Disease, Type A</term>
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<term>Cell Membrane</term>
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<term>Cytokinesis</term>
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<term>Animals</term>
<term>COS Cells</term>
<term>Cell Polarity</term>
<term>Cell Survival</term>
<term>Cercopithecus aethiops</term>
<term>Enzyme-Linked Immunosorbent Assay</term>
<term>HeLa Cells</term>
<term>Humans</term>
<term>Infant</term>
<term>Male</term>
<term>Microscopy, Atomic Force</term>
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<div type="abstract" xml:lang="en">Sphingomyelin (SM) is a major sphingolipid in mammalian cells and is reported to form specific lipid domains together with cholesterol. However, methods to examine the membrane distribution of SM are limited. We demonstrated in model membranes that fluorescent protein conjugates of 2 specific SM-binding toxins, lysenin (Lys) and equinatoxin II (EqtII), recognize different membrane distributions of SM; Lys exclusively binds clustered SM, whereas EqtII preferentially binds dispersed SM. Freeze-fracture immunoelectron microscopy showed that clustered but not dispersed SM formed lipid domains on the cell surface. Glycolipids and the membrane concentration of SM affect the SM distribution pattern on the plasma membrane. Using derivatives of Lys and EqtII as SM distribution-sensitive probes, we revealed the exclusive accumulation of SM clusters in the midbody at the time of cytokinesis. Interestingly, apical membranes of differentiated epithelial cells exhibited dispersed SM distribution, whereas SM was clustered in basolateral membranes. Clustered but not dispersed SM was absent from the cell surface of acid sphingomyelinase-deficient Niemann-Pick type A cells. These data suggest that both the SM content and membrane distribution are crucial for pathophysiological events bringing therapeutic perspective in the role of SM membrane distribution.</div>
</front>
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<Abstract>
<AbstractText>Sphingomyelin (SM) is a major sphingolipid in mammalian cells and is reported to form specific lipid domains together with cholesterol. However, methods to examine the membrane distribution of SM are limited. We demonstrated in model membranes that fluorescent protein conjugates of 2 specific SM-binding toxins, lysenin (Lys) and equinatoxin II (EqtII), recognize different membrane distributions of SM; Lys exclusively binds clustered SM, whereas EqtII preferentially binds dispersed SM. Freeze-fracture immunoelectron microscopy showed that clustered but not dispersed SM formed lipid domains on the cell surface. Glycolipids and the membrane concentration of SM affect the SM distribution pattern on the plasma membrane. Using derivatives of Lys and EqtII as SM distribution-sensitive probes, we revealed the exclusive accumulation of SM clusters in the midbody at the time of cytokinesis. Interestingly, apical membranes of differentiated epithelial cells exhibited dispersed SM distribution, whereas SM was clustered in basolateral membranes. Clustered but not dispersed SM was absent from the cell surface of acid sphingomyelinase-deficient Niemann-Pick type A cells. These data suggest that both the SM content and membrane distribution are crucial for pathophysiological events bringing therapeutic perspective in the role of SM membrane distribution.</AbstractText>
<CopyrightInformation>© FASEB.</CopyrightInformation>
</Abstract>
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<LastName>Makino</LastName>
<ForeName>Asami</ForeName>
<Initials>A</Initials>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</Affiliation>
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<LastName>Abe</LastName>
<ForeName>Mitsuhiro</ForeName>
<Initials>M</Initials>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</Affiliation>
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<LastName>Murate</LastName>
<ForeName>Motohide</ForeName>
<Initials>M</Initials>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</Affiliation>
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<LastName>Inaba</LastName>
<ForeName>Takehiko</ForeName>
<Initials>T</Initials>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</Affiliation>
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<LastName>Yilmaz</LastName>
<ForeName>Neval</ForeName>
<Initials>N</Initials>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</Affiliation>
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<LastName>Hullin-Matsuda</LastName>
<ForeName>Françoise</ForeName>
<Initials>F</Initials>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</Affiliation>
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<LastName>Kishimoto</LastName>
<ForeName>Takuma</ForeName>
<Initials>T</Initials>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</Affiliation>
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<LastName>Schieber</LastName>
<ForeName>Nicole L</ForeName>
<Initials>NL</Initials>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</Affiliation>
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<LastName>Taguchi</LastName>
<ForeName>Tomohiko</ForeName>
<Initials>T</Initials>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</Affiliation>
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<Author ValidYN="Y">
<LastName>Arai</LastName>
<ForeName>Hiroyuki</ForeName>
<Initials>H</Initials>
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<Author ValidYN="Y">
<LastName>Anderluh</LastName>
<ForeName>Gregor</ForeName>
<Initials>G</Initials>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.</Affiliation>
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<LastName>Parton</LastName>
<ForeName>Robert G</ForeName>
<Initials>RG</Initials>
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<LastName>Kobayashi</LastName>
<ForeName>Toshihide</ForeName>
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<Affiliation>*Lipid Biology Laboratory, RIKEN, Hirosawa, Wako-shi, Saitama, Japan; INSERM U1060-Université Lyon, Villeurbanne, France; Institute for Molecular Bioscience and Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia; Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo, Japan; National Institute of Chemistry, Ljubljana, Slovenia; and Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia kobayasi@riken.jp.</Affiliation>
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<Language>eng</Language>
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<PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
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<ArticleDate DateType="Electronic">
<Year>2014</Year>
<Month>11</Month>
<Day>11</Day>
</ArticleDate>
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<Country>United States</Country>
<MedlineTA>FASEB J</MedlineTA>
<NlmUniqueID>8804484</NlmUniqueID>
<ISSNLinking>0892-6638</ISSNLinking>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D018076">DNA, Complementary</NameOfSubstance>
</Chemical>
<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D008081">Liposomes</NameOfSubstance>
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<Chemical>
<RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D011994">Recombinant Proteins</NameOfSubstance>
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<Chemical>
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<NameOfSubstance UI="D013109">Sphingomyelins</NameOfSubstance>
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<CitationSubset>IM</CitationSubset>
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<MeshHeading>
<DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D019556" MajorTopicYN="N">COS Cells</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002462" MajorTopicYN="N">Cell Membrane</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D016764" MajorTopicYN="N">Cell Polarity</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002470" MajorTopicYN="N">Cell Survival</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D002522" MajorTopicYN="N">Cercopithecus aethiops</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D048749" MajorTopicYN="N">Cytokinesis</DescriptorName>
<QualifierName UI="Q000502" MajorTopicYN="Y">physiology</QualifierName>
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<DescriptorName UI="D004797" MajorTopicYN="N">Enzyme-Linked Immunosorbent Assay</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D004847" MajorTopicYN="N">Epithelial Cells</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D005347" MajorTopicYN="N">Fibroblasts</DescriptorName>
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<DescriptorName UI="D006367" MajorTopicYN="N">HeLa Cells</DescriptorName>
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<DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
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<DescriptorName UI="D007223" MajorTopicYN="N">Infant</DescriptorName>
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<MeshHeading>
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<MeshHeading>
<DescriptorName UI="D018625" MajorTopicYN="N">Microscopy, Atomic Force</DescriptorName>
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<MeshHeading>
<DescriptorName UI="D018613" MajorTopicYN="N">Microscopy, Confocal</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D016253" MajorTopicYN="N">Microscopy, Immunoelectron</DescriptorName>
</MeshHeading>
<MeshHeading>
<DescriptorName UI="D052536" MajorTopicYN="N">Niemann-Pick Disease, Type A</DescriptorName>
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<KeywordList Owner="NOTNLM">
<Keyword MajorTopicYN="N">lipid binding protein</Keyword>
<Keyword MajorTopicYN="N">lipid raft</Keyword>
<Keyword MajorTopicYN="N">membrane lipids</Keyword>
<Keyword MajorTopicYN="N">sphingolipid</Keyword>
<Keyword MajorTopicYN="N">toxins</Keyword>
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   |texte=   Visualization of the heterogeneous membrane distribution of sphingomyelin associated with cytokinesis, cell polarity, and sphingolipidosis.
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