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 : 001022 ( Pmc/Curation ); précédent : 001021; suivant : 001023Role 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.
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
Url:
DOI: 10.1371/journal.pone.0149097
PubMed: 26950439
PubMed Central: 4780765
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<front><div type="abstract" xml:lang="en"><p>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 <italic>in vitro</italic>
(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. <italic>In silico</italic>
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.</p>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">PLoS One</journal-id>
<journal-id journal-id-type="iso-abbrev">PLoS ONE</journal-id>
<journal-id journal-id-type="publisher-id">plos</journal-id>
<journal-id journal-id-type="pmc">plosone</journal-id>
<journal-title-group><journal-title>PLoS ONE</journal-title>
</journal-title-group>
<issn pub-type="epub">1932-6203</issn>
<publisher><publisher-name>Public Library of Science</publisher-name>
<publisher-loc>San Francisco, CA USA</publisher-loc>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">26950439</article-id>
<article-id pub-id-type="pmc">4780765</article-id>
<article-id pub-id-type="doi">10.1371/journal.pone.0149097</article-id>
<article-id pub-id-type="publisher-id">PONE-D-15-37442</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Research Article</subject>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Cellular Structures and Organelles</subject>
<subj-group><subject>Cell Membranes</subject>
<subj-group><subject>Membrane Proteins</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Proteins</subject>
<subj-group><subject>Protein Interactions</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject>
<subj-group><subject>Precipitation Techniques</subject>
<subj-group><subject>Immunoprecipitation</subject>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Physical Sciences</subject>
<subj-group><subject>Chemistry</subject>
<subj-group><subject>Chemical Compounds</subject>
<subj-group><subject>Chlorides</subject>
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<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Biochemistry</subject>
<subj-group><subject>Proteins</subject>
<subj-group><subject>Post-Translational Modification</subject>
<subj-group><subject>Phosphorylation</subject>
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</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Cellular Structures and Organelles</subject>
<subj-group><subject>Cell Membranes</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Molecular Biology</subject>
<subj-group><subject>Molecular Biology Techniques</subject>
<subj-group><subject>Molecular Probe Techniques</subject>
<subj-group><subject>Immunoblotting</subject>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
</subj-group>
<subj-group subj-group-type="Discipline-v3"><subject>Research and Analysis Methods</subject>
<subj-group><subject>Molecular Biology Techniques</subject>
<subj-group><subject>Molecular Probe Techniques</subject>
<subj-group><subject>Immunoblotting</subject>
</subj-group>
</subj-group>
</subj-group>
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<subj-group subj-group-type="Discipline-v3"><subject>Biology and Life Sciences</subject>
<subj-group><subject>Cell Biology</subject>
<subj-group><subject>Cytosol</subject>
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<title-group><article-title>Role of Interaction and Nucleoside Diphosphate Kinase B in Regulation of the Cystic Fibrosis Transmembrane Conductance Regulator Function by cAMP-Dependent Protein Kinase A</article-title>
<alt-title alt-title-type="running-head">NDPK-B Binds and Regulates CFTR</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Borthwick</surname>
<given-names>Lee A.</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="econtrib001"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kerbiriou</surname>
<given-names>Mathieu</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="currentaff001"><sup>¤</sup>
</xref>
<xref ref-type="author-notes" rid="econtrib001"><sup>‡</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Taylor</surname>
<given-names>Christopher J.</given-names>
</name>
<xref ref-type="aff" rid="aff002"><sup>2</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cozza</surname>
<given-names>Giorgio</given-names>
</name>
<xref ref-type="aff" rid="aff004"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lascu</surname>
<given-names>Ioan</given-names>
</name>
<xref ref-type="aff" rid="aff005"><sup>5</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Postel</surname>
<given-names>Edith H.</given-names>
</name>
<xref ref-type="aff" rid="aff006"><sup>6</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Cassidy</surname>
<given-names>Diane</given-names>
</name>
<xref ref-type="aff" rid="aff007"><sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Trouvé</surname>
<given-names>Pascal</given-names>
</name>
<xref ref-type="aff" rid="aff008"><sup>8</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Mehta</surname>
<given-names>Anil</given-names>
</name>
<xref ref-type="aff" rid="aff007"><sup>7</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Robson</surname>
<given-names>Louise</given-names>
</name>
<xref ref-type="aff" rid="aff003"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Muimo</surname>
<given-names>Richmond</given-names>
</name>
<xref ref-type="aff" rid="aff001"><sup>1</sup>
</xref>
<xref ref-type="corresp" rid="cor001">*</xref>
</contrib>
</contrib-group>
<aff id="aff001"><label>1</label>
<addr-line>Academic Unit of Respiratory Medicine, Department of Infection and Immunity, The University of Sheffield, The Medical School, Sheffield, S10 2RX, United Kingdom</addr-line>
</aff>
<aff id="aff002"><label>2</label>
<addr-line>Academic Unit of Child Health, University of Sheffield, Stephenson Wing, Sheffield Children's Hospital, Sheffield, S10 2TH, United Kingdom</addr-line>
</aff>
<aff id="aff003"><label>3</label>
<addr-line>Department of Biomedical Science, The University of Sheffield, Western Bank, Sheffield, S10 2TN, United Kingdom</addr-line>
</aff>
<aff id="aff004"><label>4</label>
<addr-line>Department of Biomedical Sciences, University of Padova, Via Ugo Bassi 58/B 35131, Padova, Italy</addr-line>
</aff>
<aff id="aff005"><label>5</label>
<addr-line>University of Bordeaux, France, and Institut de Biochimie et Genetique Cellulaires, Centre Nationale de la Recherche Scientifique UMR 5095, 33077, Bordeaux, France</addr-line>
</aff>
<aff id="aff006"><label>6</label>
<addr-line>Robert Wood Johnson Medical School, UMDNJ, New Brunswick, New Jersey, United States of America</addr-line>
</aff>
<aff id="aff007"><label>7</label>
<addr-line>Medical Research Institute/CVS Diabetes Lung, Ninewells Hospital and Medical School, University of Dundee, Dundee, DD1 9SY, United Kingdom</addr-line>
</aff>
<aff id="aff008"><label>8</label>
<addr-line>Inserm UMR 1078, Génétique, Génomique Fonctionnelle et Biotechnologies, 46 rue Félix Le Dantec, 29218, Brest Cedex2, France</addr-line>
</aff>
<contrib-group><contrib contrib-type="editor"><name><surname>Ai</surname>
<given-names>Tomohiko</given-names>
</name>
<role>Editor</role>
<xref ref-type="aff" rid="edit1"></xref>
</contrib>
</contrib-group>
<aff id="edit1"><addr-line>Indiana University, UNITED STATES</addr-line>
</aff>
<author-notes><fn fn-type="COI-statement" id="coi001"><p><bold>Competing Interests: </bold>
The authors have declared that no competing interests exist.</p>
</fn>
<fn fn-type="con" id="contrib001"><p>Conceived and designed the experiments: RM AM CJT LR. Performed the experiments: LAB MK GC DC IL EHP LR PT. Analyzed the data: LAB MK PT GC CJT IL DC AM RM. Contributed reagents/materials/analysis tools: IL EHP. Wrote the paper: MK GC IL LR AM RM.</p>
</fn>
<fn fn-type="current-aff" id="currentaff001"><label>¤</label>
<p>Current address: Inserm UMR 1078, Génétique, Génomique Fonctionnelle et Biotechnologies, 46 rue Félix Le Dantec, 29218, Brest Cedex2, France</p>
</fn>
<fn fn-type="other" id="econtrib001"><p>‡ These authors are joint first authors on this work.</p>
</fn>
<corresp id="cor001">* E-mail: <email>r.muimo@sheffield.ac.uk</email>
</corresp>
</author-notes>
<pub-date pub-type="epub"><day>7</day>
<month>3</month>
<year>2016</year>
</pub-date>
<pub-date pub-type="collection"><year>2016</year>
</pub-date>
<volume>11</volume>
<issue>3</issue>
<elocation-id>e0149097</elocation-id>
<history><date date-type="received"><day>26</day>
<month>8</month>
<year>2015</year>
</date>
<date date-type="accepted"><day>27</day>
<month>1</month>
<year>2016</year>
</date>
</history>
<permissions><copyright-statement>© 2016 Borthwick et al</copyright-statement>
<copyright-year>2016</copyright-year>
<copyright-holder>Borthwick et al</copyright-holder>
<license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open access article distributed under the terms of the <ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">Creative Commons Attribution License</ext-link>
, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.</license-p>
</license>
</permissions>
<self-uri content-type="pdf" xlink:type="simple" xlink:href="pone.0149097.pdf"></self-uri>
<abstract><p>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 <italic>in vitro</italic>
(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. <italic>In silico</italic>
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.</p>
</abstract>
<funding-group><funding-statement>This study was supported, in part, by grants from the Wellcome Trust (086370/Z/08/Z) (RM), the Cystic Fibrosis Trust and from the association Gaëtan Salaün and the French CF foundation “Vaincre la Mucoviscidose” (MK, PT).</funding-statement>
</funding-group>
<counts><fig-count count="8"></fig-count>
<table-count count="0"></table-count>
<page-count count="25"></page-count>
</counts>
<custom-meta-group><custom-meta id="data-availability"><meta-name>Data Availability</meta-name>
<meta-value>All relevant data are within the paper and its Supporting Information files.</meta-value>
</custom-meta>
</custom-meta-group>
</article-meta>
<notes><title>Data Availability</title>
<p>All relevant data are within the paper and its Supporting Information files.</p>
</notes>
</front>
</pmc>
</record>
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