Role of Interaction and Nucleoside Diphosphate Kinase B in Regulation of the Cystic Fibrosis Transmembrane Conductance Regulator Function by cAMP-Dependent Protein Kinase A.
Identifieur interne : 001221 ( PubMed/Curation ); précédent : 001220; suivant : 001222Role of Interaction and Nucleoside Diphosphate Kinase B in Regulation of the Cystic Fibrosis Transmembrane Conductance Regulator Function by cAMP-Dependent Protein Kinase A.
Auteurs : Lee A. Borthwick [Royaume-Uni] ; Mathieu Kerbiriou [Royaume-Uni] ; Christopher J. Taylor [Royaume-Uni] ; Giorgio Cozza [Italie] ; Ioan Lascu [France] ; Edith H. Postel [États-Unis] ; Diane Cassidy [Royaume-Uni] ; Pascal Trouvé [France] ; Anil Mehta [Royaume-Uni] ; Louise Robson [Royaume-Uni] ; Richmond Muimo [Royaume-Uni]Source :
- PloS one [ 1932-6203 ] ; 2016.
Descripteurs français
- KwdFr :
- AMP cyclique (métabolisme), Animaux, Appareil respiratoire (cytologie), Cellules épithéliales (cytologie), Cyclic AMP-Dependent Protein Kinases (métabolisme), Cytosol (métabolisme), Données de séquences moléculaires, Humains, Jeune adulte, Liaison aux protéines, Lignée cellulaire, Membrane cellulaire (métabolisme), Modèles moléculaires, NM23 Nucleoside Diphosphate kinases (), NM23 Nucleoside Diphosphate kinases (métabolisme), Polarité de la cellule, Protéine CFTR (), Protéine CFTR (métabolisme), Sites de fixation, Structure tertiaire des protéines, Séquence d'acides aminés, Transport de protéines.
- MESH :
- cytologie : Appareil respiratoire, Cellules épithéliales.
- métabolisme : AMP cyclique, Cyclic AMP-Dependent Protein Kinases, Cytosol, Membrane cellulaire, NM23 Nucleoside Diphosphate kinases, Protéine CFTR.
- Animaux, Données de séquences moléculaires, Humains, Jeune adulte, Liaison aux protéines, Lignée cellulaire, Modèles moléculaires, NM23 Nucleoside Diphosphate kinases, Polarité de la cellule, Protéine CFTR, Sites de fixation, Structure tertiaire des protéines, Séquence d'acides aminés, Transport de protéines.
English descriptors
- KwdEn :
- Amino Acid Sequence, Animals, Binding Sites, Cell Line, Cell Membrane (metabolism), Cell Polarity, Cyclic AMP (metabolism), Cyclic AMP-Dependent Protein Kinases (metabolism), Cystic Fibrosis Transmembrane Conductance Regulator (chemistry), Cystic Fibrosis Transmembrane Conductance Regulator (metabolism), Cytosol (metabolism), Epithelial Cells (cytology), Humans, Models, Molecular, Molecular Sequence Data, NM23 Nucleoside Diphosphate Kinases (chemistry), NM23 Nucleoside Diphosphate Kinases (metabolism), Protein Binding, Protein Structure, Tertiary, Protein Transport, Respiratory System (cytology), Young Adult.
- MESH :
- chemical , chemistry : Cystic Fibrosis Transmembrane Conductance Regulator, NM23 Nucleoside Diphosphate Kinases.
- chemical , metabolism : Cyclic AMP, Cyclic AMP-Dependent Protein Kinases, Cystic Fibrosis Transmembrane Conductance Regulator, NM23 Nucleoside Diphosphate Kinases.
- cytology : Epithelial Cells, Respiratory System.
- metabolism : Cell Membrane, Cytosol.
- Amino Acid Sequence, Animals, Binding Sites, Cell Line, Cell Polarity, Humans, Models, Molecular, Molecular Sequence Data, Protein Binding, Protein Structure, Tertiary, Protein Transport, Young Adult.
Abstract
Cystic fibrosis results from mutations in the cystic fibrosis transmembrane conductance regulator (CFTR), a cAMP-dependent protein kinase A (PKA) and ATP-regulated chloride channel. Here, we demonstrate that nucleoside diphosphate kinase B (NDPK-B, NM23-H2) forms a functional complex with CFTR. In airway epithelia forskolin/IBMX significantly increases NDPK-B co-localisation with CFTR whereas PKA inhibitors attenuate complex formation. Furthermore, an NDPK-B derived peptide (but not its NDPK-A equivalent) disrupts the NDPK-B/CFTR complex in vitro (19-mers comprising amino acids 36-54 from NDPK-B or NDPK-A). Overlay (Far-Western) and Surface Plasmon Resonance (SPR) analysis both demonstrate that NDPK-B binds CFTR within its first nucleotide binding domain (NBD1, CFTR amino acids 351-727). Analysis of chloride currents reflective of CFTR or outwardly rectifying chloride channels (ORCC, DIDS-sensitive) showed that the 19-mer NDPK-B peptide (but not its NDPK-A equivalent) reduced both chloride conductances. Additionally, the NDPK-B (but not NDPK-A) peptide also attenuated acetylcholine-induced intestinal short circuit currents. In silico analysis of the NBD1/NDPK-B complex reveals an extended interaction surface between the two proteins. This binding zone is also target of the 19-mer NDPK-B peptide, thus confirming its capability to disrupt NDPK-B/CFTR complex. We propose that NDPK-B forms part of the complex that controls chloride currents in epithelia.
DOI: 10.1371/journal.pone.0149097
PubMed: 26950439
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<country xml:lang="fr">France</country>
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<term>Animals</term>
<term>Binding Sites</term>
<term>Cell Line</term>
<term>Cell Membrane (metabolism)</term>
<term>Cell Polarity</term>
<term>Cyclic AMP (metabolism)</term>
<term>Cyclic AMP-Dependent Protein Kinases (metabolism)</term>
<term>Cystic Fibrosis Transmembrane Conductance Regulator (chemistry)</term>
<term>Cystic Fibrosis Transmembrane Conductance Regulator (metabolism)</term>
<term>Cytosol (metabolism)</term>
<term>Epithelial Cells (cytology)</term>
<term>Humans</term>
<term>Models, Molecular</term>
<term>Molecular Sequence Data</term>
<term>NM23 Nucleoside Diphosphate Kinases (chemistry)</term>
<term>NM23 Nucleoside Diphosphate Kinases (metabolism)</term>
<term>Protein Binding</term>
<term>Protein Structure, Tertiary</term>
<term>Protein Transport</term>
<term>Respiratory System (cytology)</term>
<term>Young Adult</term>
</keywords>
<keywords scheme="KwdFr" xml:lang="fr"><term>AMP cyclique (métabolisme)</term>
<term>Animaux</term>
<term>Appareil respiratoire (cytologie)</term>
<term>Cellules épithéliales (cytologie)</term>
<term>Cyclic AMP-Dependent Protein Kinases (métabolisme)</term>
<term>Cytosol (métabolisme)</term>
<term>Données de séquences moléculaires</term>
<term>Humains</term>
<term>Jeune adulte</term>
<term>Liaison aux protéines</term>
<term>Lignée cellulaire</term>
<term>Membrane cellulaire (métabolisme)</term>
<term>Modèles moléculaires</term>
<term>NM23 Nucleoside Diphosphate kinases ()</term>
<term>NM23 Nucleoside Diphosphate kinases (métabolisme)</term>
<term>Polarité de la cellule</term>
<term>Protéine CFTR ()</term>
<term>Protéine CFTR (métabolisme)</term>
<term>Sites de fixation</term>
<term>Structure tertiaire des protéines</term>
<term>Séquence d'acides aminés</term>
<term>Transport de protéines</term>
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<keywords scheme="MESH" type="chemical" qualifier="chemistry" xml:lang="en"><term>Cystic Fibrosis Transmembrane Conductance Regulator</term>
<term>NM23 Nucleoside Diphosphate Kinases</term>
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<term>Cyclic AMP-Dependent Protein Kinases</term>
<term>Cystic Fibrosis Transmembrane Conductance Regulator</term>
<term>NM23 Nucleoside Diphosphate Kinases</term>
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<term>Cellules épithéliales</term>
</keywords>
<keywords scheme="MESH" qualifier="cytology" xml:lang="en"><term>Epithelial Cells</term>
<term>Respiratory System</term>
</keywords>
<keywords scheme="MESH" qualifier="metabolism" xml:lang="en"><term>Cell Membrane</term>
<term>Cytosol</term>
</keywords>
<keywords scheme="MESH" qualifier="métabolisme" xml:lang="fr"><term>AMP cyclique</term>
<term>Cyclic AMP-Dependent Protein Kinases</term>
<term>Cytosol</term>
<term>Membrane cellulaire</term>
<term>NM23 Nucleoside Diphosphate kinases</term>
<term>Protéine CFTR</term>
</keywords>
<keywords scheme="MESH" xml:lang="en"><term>Amino Acid Sequence</term>
<term>Animals</term>
<term>Binding Sites</term>
<term>Cell Line</term>
<term>Cell Polarity</term>
<term>Humans</term>
<term>Models, Molecular</term>
<term>Molecular Sequence Data</term>
<term>Protein Binding</term>
<term>Protein Structure, Tertiary</term>
<term>Protein Transport</term>
<term>Young Adult</term>
</keywords>
<keywords scheme="MESH" xml:lang="fr"><term>Animaux</term>
<term>Données de séquences moléculaires</term>
<term>Humains</term>
<term>Jeune adulte</term>
<term>Liaison aux protéines</term>
<term>Lignée cellulaire</term>
<term>Modèles moléculaires</term>
<term>NM23 Nucleoside Diphosphate kinases</term>
<term>Polarité de la cellule</term>
<term>Protéine CFTR</term>
<term>Sites de fixation</term>
<term>Structure tertiaire des protéines</term>
<term>Séquence d'acides aminés</term>
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<front><div type="abstract" xml:lang="en">Cystic fibrosis results from mutations in the cystic fibrosis transmembrane conductance regulator (CFTR), a cAMP-dependent protein kinase A (PKA) and ATP-regulated chloride channel. Here, we demonstrate that nucleoside diphosphate kinase B (NDPK-B, NM23-H2) forms a functional complex with CFTR. In airway epithelia forskolin/IBMX significantly increases NDPK-B co-localisation with CFTR whereas PKA inhibitors attenuate complex formation. Furthermore, an NDPK-B derived peptide (but not its NDPK-A equivalent) disrupts the NDPK-B/CFTR complex in vitro (19-mers comprising amino acids 36-54 from NDPK-B or NDPK-A). Overlay (Far-Western) and Surface Plasmon Resonance (SPR) analysis both demonstrate that NDPK-B binds CFTR within its first nucleotide binding domain (NBD1, CFTR amino acids 351-727). Analysis of chloride currents reflective of CFTR or outwardly rectifying chloride channels (ORCC, DIDS-sensitive) showed that the 19-mer NDPK-B peptide (but not its NDPK-A equivalent) reduced both chloride conductances. Additionally, the NDPK-B (but not NDPK-A) peptide also attenuated acetylcholine-induced intestinal short circuit currents. In silico analysis of the NBD1/NDPK-B complex reveals an extended interaction surface between the two proteins. This binding zone is also target of the 19-mer NDPK-B peptide, thus confirming its capability to disrupt NDPK-B/CFTR complex. We propose that NDPK-B forms part of the complex that controls chloride currents in epithelia. </div>
</front>
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<ELocationID EIdType="doi" ValidYN="Y">10.1371/journal.pone.0149097</ELocationID>
<Abstract><AbstractText>Cystic fibrosis results from mutations in the cystic fibrosis transmembrane conductance regulator (CFTR), a cAMP-dependent protein kinase A (PKA) and ATP-regulated chloride channel. Here, we demonstrate that nucleoside diphosphate kinase B (NDPK-B, NM23-H2) forms a functional complex with CFTR. In airway epithelia forskolin/IBMX significantly increases NDPK-B co-localisation with CFTR whereas PKA inhibitors attenuate complex formation. Furthermore, an NDPK-B derived peptide (but not its NDPK-A equivalent) disrupts the NDPK-B/CFTR complex in vitro (19-mers comprising amino acids 36-54 from NDPK-B or NDPK-A). Overlay (Far-Western) and Surface Plasmon Resonance (SPR) analysis both demonstrate that NDPK-B binds CFTR within its first nucleotide binding domain (NBD1, CFTR amino acids 351-727). Analysis of chloride currents reflective of CFTR or outwardly rectifying chloride channels (ORCC, DIDS-sensitive) showed that the 19-mer NDPK-B peptide (but not its NDPK-A equivalent) reduced both chloride conductances. Additionally, the NDPK-B (but not NDPK-A) peptide also attenuated acetylcholine-induced intestinal short circuit currents. In silico analysis of the NBD1/NDPK-B complex reveals an extended interaction surface between the two proteins. This binding zone is also target of the 19-mer NDPK-B peptide, thus confirming its capability to disrupt NDPK-B/CFTR complex. We propose that NDPK-B forms part of the complex that controls chloride currents in epithelia. </AbstractText>
</Abstract>
<AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Borthwick</LastName>
<ForeName>Lee A</ForeName>
<Initials>LA</Initials>
<AffiliationInfo><Affiliation>Academic Unit of Respiratory Medicine, Department of Infection and Immunity, The University of Sheffield, The Medical School, Sheffield, S10 2RX, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Kerbiriou</LastName>
<ForeName>Mathieu</ForeName>
<Initials>M</Initials>
<AffiliationInfo><Affiliation>Academic Unit of Respiratory Medicine, Department of Infection and Immunity, The University of Sheffield, The Medical School, Sheffield, S10 2RX, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Taylor</LastName>
<ForeName>Christopher J</ForeName>
<Initials>CJ</Initials>
<AffiliationInfo><Affiliation>Academic Unit of Child Health, University of Sheffield, Stephenson Wing, Sheffield Children's Hospital, Sheffield, S10 2TH, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Cozza</LastName>
<ForeName>Giorgio</ForeName>
<Initials>G</Initials>
<AffiliationInfo><Affiliation>Department of Biomedical Sciences, University of Padova, Via Ugo Bassi 58/B 35131, Padova, Italy.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Lascu</LastName>
<ForeName>Ioan</ForeName>
<Initials>I</Initials>
<AffiliationInfo><Affiliation>University of Bordeaux, France, and Institut de Biochimie et Genetique Cellulaires, Centre Nationale de la Recherche Scientifique UMR 5095, 33077, Bordeaux, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Postel</LastName>
<ForeName>Edith H</ForeName>
<Initials>EH</Initials>
<AffiliationInfo><Affiliation>Robert Wood Johnson Medical School, UMDNJ, New Brunswick, New Jersey, United States of America.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Cassidy</LastName>
<ForeName>Diane</ForeName>
<Initials>D</Initials>
<AffiliationInfo><Affiliation>Medical Research Institute/CVS Diabetes Lung, Ninewells Hospital and Medical School, University of Dundee, Dundee, DD1 9SY, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Trouvé</LastName>
<ForeName>Pascal</ForeName>
<Initials>P</Initials>
<AffiliationInfo><Affiliation>Inserm UMR 1078, Génétique, Génomique Fonctionnelle et Biotechnologies, 46 rue Félix Le Dantec, 29218, Brest Cedex2, France.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Mehta</LastName>
<ForeName>Anil</ForeName>
<Initials>A</Initials>
<AffiliationInfo><Affiliation>Medical Research Institute/CVS Diabetes Lung, Ninewells Hospital and Medical School, University of Dundee, Dundee, DD1 9SY, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Robson</LastName>
<ForeName>Louise</ForeName>
<Initials>L</Initials>
<AffiliationInfo><Affiliation>Department of Biomedical Science, The University of Sheffield, Western Bank, Sheffield, S10 2TN, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
<Author ValidYN="Y"><LastName>Muimo</LastName>
<ForeName>Richmond</ForeName>
<Initials>R</Initials>
<AffiliationInfo><Affiliation>Academic Unit of Respiratory Medicine, Department of Infection and Immunity, The University of Sheffield, The Medical School, Sheffield, S10 2RX, United Kingdom.</Affiliation>
</AffiliationInfo>
</Author>
</AuthorList>
<Language>eng</Language>
<GrantList CompleteYN="Y"><Grant><GrantID>086370/Z/08/Z</GrantID>
<Agency>Wellcome Trust</Agency>
<Country>United Kingdom</Country>
</Grant>
</GrantList>
<PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType>
<PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType>
</PublicationTypeList>
<ArticleDate DateType="Electronic"><Year>2016</Year>
<Month>03</Month>
<Day>07</Day>
</ArticleDate>
</Article>
<MedlineJournalInfo><Country>United States</Country>
<MedlineTA>PLoS One</MedlineTA>
<NlmUniqueID>101285081</NlmUniqueID>
<ISSNLinking>1932-6203</ISSNLinking>
</MedlineJournalInfo>
<ChemicalList><Chemical><RegistryNumber>0</RegistryNumber>
<NameOfSubstance UI="D054778">NM23 Nucleoside Diphosphate Kinases</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>126880-72-6</RegistryNumber>
<NameOfSubstance UI="D019005">Cystic Fibrosis Transmembrane Conductance Regulator</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>E0399OZS9N</RegistryNumber>
<NameOfSubstance UI="D000242">Cyclic AMP</NameOfSubstance>
</Chemical>
<Chemical><RegistryNumber>EC 2.7.11.11</RegistryNumber>
<NameOfSubstance UI="D017868">Cyclic AMP-Dependent Protein Kinases</NameOfSubstance>
</Chemical>
</ChemicalList>
<CitationSubset>IM</CitationSubset>
<MeshHeadingList><MeshHeading><DescriptorName UI="D000595" MajorTopicYN="N">Amino Acid Sequence</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D000818" MajorTopicYN="N">Animals</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D001665" MajorTopicYN="N">Binding Sites</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D002460" MajorTopicYN="N">Cell Line</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="D000242" MajorTopicYN="N">Cyclic AMP</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D017868" MajorTopicYN="N">Cyclic AMP-Dependent Protein Kinases</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D019005" MajorTopicYN="N">Cystic Fibrosis Transmembrane Conductance Regulator</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D003600" MajorTopicYN="N">Cytosol</DescriptorName>
<QualifierName UI="Q000378" MajorTopicYN="N">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D004847" MajorTopicYN="N">Epithelial Cells</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D006801" MajorTopicYN="N">Humans</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008958" MajorTopicYN="N">Models, Molecular</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D008969" MajorTopicYN="N">Molecular Sequence Data</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D054778" MajorTopicYN="N">NM23 Nucleoside Diphosphate Kinases</DescriptorName>
<QualifierName UI="Q000737" MajorTopicYN="N">chemistry</QualifierName>
<QualifierName UI="Q000378" MajorTopicYN="Y">metabolism</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D011485" MajorTopicYN="N">Protein Binding</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D017434" MajorTopicYN="N">Protein Structure, Tertiary</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D021381" MajorTopicYN="N">Protein Transport</DescriptorName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D012137" MajorTopicYN="N">Respiratory System</DescriptorName>
<QualifierName UI="Q000166" MajorTopicYN="N">cytology</QualifierName>
</MeshHeading>
<MeshHeading><DescriptorName UI="D055815" MajorTopicYN="N">Young Adult</DescriptorName>
</MeshHeading>
</MeshHeadingList>
</MedlineCitation>
<PubmedData><History><PubMedPubDate PubStatus="received"><Year>2015</Year>
<Month>08</Month>
<Day>26</Day>
</PubMedPubDate>
<PubMedPubDate PubStatus="accepted"><Year>2016</Year>
<Month>01</Month>
<Day>27</Day>
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<PubMedPubDate PubStatus="medline"><Year>2016</Year>
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