Activation of the Ca2+ sensing receptor and the PKC/WNK4 downstream signaling cascade induces incorporation of ZO-2 to tight junctions and its separation from 14-3-3
Identifieur interne : 000699 ( Pmc/Curation ); précédent : 000698; suivant : 000700Activation of the Ca2+ sensing receptor and the PKC/WNK4 downstream signaling cascade induces incorporation of ZO-2 to tight junctions and its separation from 14-3-3
Auteurs : Elida Amaya [Mexique] ; Lourdes Alarc N [Mexique] ; Dolores Martín-Tapia [Mexique] ; Francisco Cuellar-Pérez [Mexique] ; Misael Cano-Cortina [Mexique] ; Jose Mario Ortega-Olvera [Mexique] ; Bulmaro Cisneros [Mexique] ; Alexis J. Rodriguez [États-Unis] ; Gerardo Gamba [Mexique] ; Lorenza González-Mariscal [Mexique]Source :
- Molecular Biology of the Cell [ 1059-1524 ] ; 2019.
Abstract
Zonula occludens-2 (ZO-2) is a tight junction (TJ) cytoplasmic protein, whose localization varies according to cell density and Ca2+ in the media. In cells cultured in low calcium (LC), ZO-2 displays a diffuse cytoplasmic distribution, but activation of the Ca2+ sensing receptor (CaSR) with Gd3+ triggers the appearance of ZO-2 at the cell borders. CaSR downstream signaling involves activation of protein kinase C, which phosphorylates and activates with no lysine kinase-4 that phosphorylates ZO-2 inducing its concentration at TJs. In LC, ZO-2 is protected from degradation by association to 14-3-3 proteins. When monolayers are transferred to normal calcium, the complexes ZO-2/14-3-3ζ and ZO-2/14-3-3σ move to the cell borders and dissociate. The 14-3-3 proteins are then degraded in proteosomes, whereas ZO-2 integrates to TJs. From the plasma membrane residual ZO-2 is endocyted and degradaded in lysosomes. The unique region 2 of ZO-2, and S261 located within a nuclear localization signal, are critical for the interaction with 14-3-3 ζ and σ and for the efficient nuclear importation of ZO-2. These results explain the molecular mechanism through which extracellular Ca2+ triggers the appearance of ZO-2 at TJs in epithelial cells and reveal the novel interaction between ZO-2 and 14-3-3 proteins, which is critical for ZO-2 protection and intracellular traffic.
Url:
DOI: 10.1091/mbc.E18-09-0591
PubMed: 31318316
PubMed Central: 6741067
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wicri:level="1"><nlm:aff id="aff5">Department of Nephrology and Mineral Metabolism, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14080, Mexico</nlm:aff><country xml:lang="fr">Mexique</country><wicri:regionArea>Department of Nephrology and Mineral Metabolism, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14080</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff6">Tecnológico de Monterrey, Escuela de Medicina y Ciencias de la Salud, 64710 Monterrey, Nuevo Leon, México</nlm:aff><country xml:lang="fr" wicri:curation="lc">Mexique</country><wicri:regionArea>Tecnológico de Monterrey, Escuela de Medicina y Ciencias de la Salud, 64710 Monterrey, Nuevo Leon</wicri:regionArea></affiliation></author><author><name sortKey="Gonzalez Mariscal, Lorenza" sort="Gonzalez Mariscal, Lorenza" uniqKey="Gonzalez Mariscal L" first="Lorenza" last="González-Mariscal">Lorenza González-Mariscal</name><affiliation wicri:level="1"><nlm:aff id="aff1">Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360, Mexico</nlm:aff><country xml:lang="fr">Mexique</country><wicri:regionArea>Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360</wicri:regionArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31318316</idno><idno type="pmc">6741067</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6741067</idno><idno type="RBID">PMC:6741067</idno><idno type="doi">10.1091/mbc.E18-09-0591</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000699</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000699</idno><idno type="wicri:Area/Pmc/Curation">000699</idno><idno type="wicri:explorRef" wicri:stream="Pmc" 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N</name><affiliation wicri:level="1"><nlm:aff id="aff1">Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360, Mexico</nlm:aff><country xml:lang="fr">Mexique</country><wicri:regionArea>Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360</wicri:regionArea></affiliation></author><author><name sortKey="Martin Tapia, Dolores" sort="Martin Tapia, Dolores" uniqKey="Martin Tapia D" first="Dolores" last="Martín-Tapia">Dolores Martín-Tapia</name><affiliation wicri:level="1"><nlm:aff id="aff1">Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360, Mexico</nlm:aff><country xml:lang="fr">Mexique</country><wicri:regionArea>Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360</wicri:regionArea></affiliation></author><author><name sortKey="Cuellar Perez, Francisco" sort="Cuellar Perez, Francisco" uniqKey="Cuellar Perez F" first="Francisco" last="Cuellar-Pérez">Francisco Cuellar-Pérez</name><affiliation wicri:level="1"><nlm:aff id="aff1">Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360, Mexico</nlm:aff><country xml:lang="fr">Mexique</country><wicri:regionArea>Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360</wicri:regionArea></affiliation></author><author><name sortKey="Cano Cortina, Misael" sort="Cano Cortina, Misael" uniqKey="Cano Cortina M" first="Misael" last="Cano-Cortina">Misael Cano-Cortina</name><affiliation wicri:level="1"><nlm:aff id="aff1">Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360, Mexico</nlm:aff><country xml:lang="fr">Mexique</country><wicri:regionArea>Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360</wicri:regionArea></affiliation></author><author><name sortKey="Ortega Olvera, Jose Mario" sort="Ortega Olvera, Jose Mario" uniqKey="Ortega Olvera J" first="Jose Mario" last="Ortega-Olvera">Jose Mario Ortega-Olvera</name><affiliation wicri:level="1"><nlm:aff id="aff1">Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360, Mexico</nlm:aff><country xml:lang="fr">Mexique</country><wicri:regionArea>Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360</wicri:regionArea></affiliation></author><author><name sortKey="Cisneros, Bulmaro" sort="Cisneros, Bulmaro" uniqKey="Cisneros B" first="Bulmaro" last="Cisneros">Bulmaro Cisneros</name><affiliation wicri:level="1"><nlm:aff id="aff2">Department of Genetics and Molecular Biology, Mexico City 07360, Mexico</nlm:aff><country xml:lang="fr">Mexique</country><wicri:regionArea>Department of Genetics and Molecular Biology, Mexico City 07360</wicri:regionArea></affiliation></author><author><name sortKey="Rodriguez, Alexis J" sort="Rodriguez, Alexis J" uniqKey="Rodriguez A" first="Alexis J." last="Rodriguez">Alexis J. Rodriguez</name><affiliation wicri:level="2"><nlm:aff id="aff3">Department of Biological Science, Rutgers, The State University of New Jersey, Newark, NJ 07102</nlm:aff><country xml:lang="fr">États-Unis</country><placeName><region type="state">New Jersey</region></placeName><wicri:cityArea>Department of Biological Science, Rutgers, The State University of New Jersey, Newark</wicri:cityArea></affiliation></author><author><name sortKey="Gamba, Gerardo" sort="Gamba, Gerardo" uniqKey="Gamba G" first="Gerardo" last="Gamba">Gerardo Gamba</name><affiliation wicri:level="1"><nlm:aff id="aff4">Molecular Physiology Unit, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Mexico City 14080, México</nlm:aff><country xml:lang="fr" wicri:curation="lc">Mexique</country><wicri:regionArea>Molecular Physiology Unit, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Mexico City 14080</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff5">Department of Nephrology and Mineral Metabolism, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14080, Mexico</nlm:aff><country xml:lang="fr">Mexique</country><wicri:regionArea>Department of Nephrology and Mineral Metabolism, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14080</wicri:regionArea></affiliation><affiliation wicri:level="1"><nlm:aff id="aff6">Tecnológico de Monterrey, Escuela de Medicina y Ciencias de la Salud, 64710 Monterrey, Nuevo Leon, México</nlm:aff><country xml:lang="fr" wicri:curation="lc">Mexique</country><wicri:regionArea>Tecnológico de Monterrey, Escuela de Medicina y Ciencias de la Salud, 64710 Monterrey, Nuevo Leon</wicri:regionArea></affiliation></author><author><name sortKey="Gonzalez Mariscal, Lorenza" sort="Gonzalez Mariscal, Lorenza" uniqKey="Gonzalez Mariscal L" first="Lorenza" last="González-Mariscal">Lorenza González-Mariscal</name><affiliation wicri:level="1"><nlm:aff id="aff1">Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360, Mexico</nlm:aff><country xml:lang="fr">Mexique</country><wicri:regionArea>Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360</wicri:regionArea></affiliation></author></analytic><series><title level="j">Molecular Biology of the Cell</title><idno type="ISSN">1059-1524</idno><idno type="eISSN">1939-4586</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Zonula occludens-2 (ZO-2) is a tight junction (TJ) cytoplasmic protein, whose localization varies according to cell density and Ca<sup>2+</sup> in the media. In cells cultured in low calcium (LC), ZO-2 displays a diffuse cytoplasmic distribution, but activation of the Ca<sup>2+</sup> sensing receptor (CaSR) with Gd<sup>3+</sup> triggers the appearance of ZO-2 at the cell borders. CaSR downstream signaling involves activation of protein kinase C, which phosphorylates and activates with no lysine kinase-4 that phosphorylates ZO-2 inducing its concentration at TJs. In LC, ZO-2 is protected from degradation by association to 14-3-3 proteins. When monolayers are transferred to normal calcium, the complexes ZO-2/14-3-3ζ and ZO-2/14-3-3σ move to the cell borders and dissociate. The 14-3-3 proteins are then degraded in proteosomes, whereas ZO-2 integrates to TJs. From the plasma membrane residual ZO-2 is endocyted and degradaded in lysosomes. The unique region 2 of ZO-2, and S261 located within a nuclear localization signal, are critical for the interaction with 14-3-3 ζ and σ and for the efficient nuclear importation of ZO-2. These results explain the molecular mechanism through which extracellular Ca<sup>2+</sup> triggers the appearance of ZO-2 at TJs in epithelial cells and reveal the novel interaction between ZO-2 and 14-3-3 proteins, which is critical for ZO-2 protection and intracellular traffic.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Apodaca, G" uniqKey="Apodaca G">G Apodaca</name></author><author><name sortKey="Gallo, Li" uniqKey="Gallo L">LI Gallo</name></author><author><name sortKey="Bryant, Dm" uniqKey="Bryant D">DM Bryant</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Avila Flores, A" uniqKey="Avila Flores A">A Avila-Flores</name></author><author><name sortKey="Rendon Huerta, E" uniqKey="Rendon Huerta E">E Rendon-Huerta</name></author><author><name sortKey="Moreno, J" uniqKey="Moreno J">J Moreno</name></author><author><name sortKey="Islas, S" uniqKey="Islas S">S Islas</name></author><author><name 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Mol Biol Cell</journal-id><journal-id journal-id-type="iso-abbrev">Mol. Biol. Cell</journal-id><journal-id journal-id-type="hwp">molbiolcell</journal-id><journal-id journal-id-type="pmc">mbc</journal-id><journal-id journal-id-type="publisher-id">mboc</journal-id><journal-title-group><journal-title>Molecular Biology of the Cell</journal-title></journal-title-group><issn pub-type="ppub">1059-1524</issn><issn pub-type="epub">1939-4586</issn><publisher><publisher-name>The American Society for Cell Biology</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31318316</article-id><article-id pub-id-type="pmc">6741067</article-id><article-id pub-id-type="publisher-id">E18-09-0591</article-id><article-id pub-id-type="doi">10.1091/mbc.E18-09-0591</article-id><article-categories><subj-group subj-group-type="heading"><subject>Articles</subject><subj-group><subject>Cell Physiology</subject></subj-group></subj-group></article-categories><title-group><article-title>Activation of the Ca<sup>2+</sup> sensing receptor and the PKC/WNK4 downstream signaling cascade induces incorporation of ZO-2 to tight junctions and its separation from 14-3-3</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Amaya</surname><given-names>Elida</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Alarcón</surname><given-names>Lourdes</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Martín-Tapia</surname><given-names>Dolores</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Cuellar-Pérez</surname><given-names>Francisco</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Cano-Cortina</surname><given-names>Misael</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Ortega-Olvera</surname><given-names>Jose Mario</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Cisneros</surname><given-names>Bulmaro</given-names></name><xref ref-type="aff" rid="aff2"><sup>b</sup></xref></contrib><contrib contrib-type="author"><name><surname>Rodriguez</surname><given-names>Alexis J.</given-names></name><xref ref-type="aff" rid="aff3"><sup>c</sup></xref></contrib><contrib contrib-type="author"><name><surname>Gamba</surname><given-names>Gerardo</given-names></name><xref ref-type="aff" rid="aff4"><sup>d</sup></xref><xref ref-type="aff" rid="aff5"><sup>e</sup></xref><xref ref-type="aff" rid="aff6"><sup>f</sup></xref></contrib><contrib contrib-type="author"><name><surname>González-Mariscal</surname><given-names>Lorenza</given-names></name><xref ref-type="aff" rid="aff1"><sup>a</sup></xref><xref ref-type="corresp" rid="cor1">*</xref></contrib><aff id="aff1"><label>a</label>Center for Research and Advanced Studies (Cinvestav), Department of Physiology, Biophysics and Neuroscience, Mexico City 07360, Mexico</aff><aff id="aff2"><label>b</label>Department of Genetics and Molecular Biology, Mexico City 07360, Mexico</aff><aff id="aff3"><label>c</label>Department of Biological Science, Rutgers, The State University of New Jersey, Newark, NJ 07102</aff><aff id="aff4"><label>d</label>Molecular Physiology Unit, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Mexico City 14080, México</aff><aff id="aff5"><label>e</label>Department of Nephrology and Mineral Metabolism, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City 14080, Mexico</aff><aff id="aff6"><label>f</label>Tecnológico de Monterrey, Escuela de Medicina y Ciencias de la Salud, 64710 Monterrey, Nuevo Leon, México</aff></contrib-group><contrib-group><contrib contrib-type="editor"><name><surname>Nusrat</surname><given-names>Asma</given-names></name><role>Monitoring Editor</role></contrib><aff>University of Michigan</aff></contrib-group><author-notes><corresp id="cor1">*Address correspondence to: Lorenza González-Mariscal (<email xlink:href="mailto:lorenza@fisio.cinvestav.mx">lorenza@fisio.cinvestav.mx</email>).</corresp></author-notes><pub-date pub-type="ppub"><day>15</day><month>8</month><year>2019</year></pub-date><volume>30</volume><issue>18</issue><fpage>2377</fpage><lpage>2398</lpage><history><date date-type="received"><day>20</day><month>9</month><year>2018</year></date><date date-type="rev-recd"><day>06</day><month>7</month><year>2019</year></date><date date-type="accepted"><day>06</day><month>7</month><year>2019</year></date></history><permissions><copyright-statement>© 2019 Amaya <italic>et al.</italic> “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology.</copyright-statement><copyright-year>2019</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-sa/3.0"><license-p>This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License.</license-p></license></permissions><self-uri content-type="pdf" xlink:type="simple" xlink:href="mbc-30-2377.pdf"></self-uri><abstract><p>Zonula occludens-2 (ZO-2) is a tight junction (TJ) cytoplasmic protein, whose localization varies according to cell density and Ca<sup>2+</sup> in the media. In cells cultured in low calcium (LC), ZO-2 displays a diffuse cytoplasmic distribution, but activation of the Ca<sup>2+</sup> sensing receptor (CaSR) with Gd<sup>3+</sup> triggers the appearance of ZO-2 at the cell borders. CaSR downstream signaling involves activation of protein kinase C, which phosphorylates and activates with no lysine kinase-4 that phosphorylates ZO-2 inducing its concentration at TJs. In LC, ZO-2 is protected from degradation by association to 14-3-3 proteins. When monolayers are transferred to normal calcium, the complexes ZO-2/14-3-3ζ and ZO-2/14-3-3σ move to the cell borders and dissociate. The 14-3-3 proteins are then degraded in proteosomes, whereas ZO-2 integrates to TJs. From the plasma membrane residual ZO-2 is endocyted and degradaded in lysosomes. The unique region 2 of ZO-2, and S261 located within a nuclear localization signal, are critical for the interaction with 14-3-3 ζ and σ and for the efficient nuclear importation of ZO-2. These results explain the molecular mechanism through which extracellular Ca<sup>2+</sup> triggers the appearance of ZO-2 at TJs in epithelial cells and reveal the novel interaction between ZO-2 and 14-3-3 proteins, which is critical for ZO-2 protection and intracellular traffic.</p></abstract></article-meta></front></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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