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 : 000B14 ( Main/Exploration ); précédent : 000B13; suivant : 000B15Activation 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
Affiliations:
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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><wicri:noRegion>Mexico City 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14-3-3</title><author><name sortKey="Amaya, Elida" sort="Amaya, Elida" uniqKey="Amaya E" first="Elida" last="Amaya">Elida Amaya</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><wicri:noRegion>Mexico City 07360</wicri:noRegion></affiliation></author><author><name sortKey="Alarc N, Lourdes" sort="Alarc N, Lourdes" uniqKey="Alarc N L" first="Lourdes" last="Alarc N">Lourdes Alarc 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><wicri:noRegion>Mexico City 07360</wicri:noRegion></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><wicri:noRegion>Mexico City 07360</wicri:noRegion></affiliation></author><author><name sortKey="Cuellar Perez, Francisco" sort="Cuellar Perez, Francisco" uniqKey="Cuellar Perez F" first="Francisco" last="Cuellar-Pérez">Francisco 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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><wicri:noRegion>Mexico City 07360</wicri:noRegion></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><wicri:noRegion>Mexico City 14080</wicri:noRegion></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><wicri:noRegion>Mexico City 14080</wicri:noRegion></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><wicri:noRegion>Nuevo Leon</wicri:noRegion></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><wicri:noRegion>Mexico City 07360</wicri:noRegion></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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sortKey="Alarc N, Lourdes" sort="Alarc N, Lourdes" uniqKey="Alarc N L" first="Lourdes" last="Alarc N">Lourdes Alarc N</name><name sortKey="Cano Cortina, Misael" sort="Cano Cortina, Misael" uniqKey="Cano Cortina M" first="Misael" last="Cano-Cortina">Misael Cano-Cortina</name><name sortKey="Cisneros, Bulmaro" sort="Cisneros, Bulmaro" uniqKey="Cisneros B" first="Bulmaro" last="Cisneros">Bulmaro Cisneros</name><name sortKey="Cuellar Perez, Francisco" sort="Cuellar Perez, Francisco" uniqKey="Cuellar Perez F" first="Francisco" last="Cuellar-Pérez">Francisco Cuellar-Pérez</name><name sortKey="Gamba, Gerardo" sort="Gamba, Gerardo" uniqKey="Gamba G" first="Gerardo" last="Gamba">Gerardo Gamba</name><name sortKey="Gamba, Gerardo" sort="Gamba, Gerardo" uniqKey="Gamba G" first="Gerardo" last="Gamba">Gerardo Gamba</name><name sortKey="Gamba, Gerardo" sort="Gamba, Gerardo" uniqKey="Gamba G" first="Gerardo" last="Gamba">Gerardo Gamba</name><name sortKey="Gonzalez Mariscal, Lorenza" sort="Gonzalez Mariscal, Lorenza" uniqKey="Gonzalez Mariscal L" first="Lorenza" last="González-Mariscal">Lorenza González-Mariscal</name><name sortKey="Martin Tapia, Dolores" sort="Martin Tapia, Dolores" uniqKey="Martin Tapia D" first="Dolores" last="Martín-Tapia">Dolores Martín-Tapia</name><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></country><country name="États-Unis"><region name="New Jersey"><name sortKey="Rodriguez, Alexis J" sort="Rodriguez, Alexis J" uniqKey="Rodriguez A" first="Alexis J." last="Rodriguez">Alexis J. 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