Nuclear Transport: A Switch for the Oxidative Stress—Signaling Circuit?
Identifieur interne : 000919 ( Pmc/Checkpoint ); précédent : 000918; suivant : 000920Nuclear Transport: A Switch for the Oxidative Stress—Signaling Circuit?
Auteurs : Mohamed Kodiha ; Ursula StochajSource :
- Journal of Signal Transduction [ 2090-1739 ] ; 2011.
Abstract
Imbalances in the formation and clearance of reactive oxygen species (ROS) can lead to oxidative stress and subsequent changes that affect all aspects of physiology. To limit and repair the damage generated by ROS, cells have developed a multitude of responses. A hallmark of these responses is the activation of signaling pathways that modulate the function of downstream targets in different cellular locations. To this end, critical steps of the stress response that occur in the nucleus and cytoplasm have to be coordinated, which makes the proper communication between both compartments mandatory. Here, we discuss the interdependence of ROS-mediated signaling and the transport of macromolecules across the nuclear envelope. We highlight examples of oxidant-dependent nuclear trafficking and describe the impact of oxidative stress on the transport apparatus. Our paper concludes by proposing a cellular circuit of ROS-induced signaling, nuclear transport and repair.
Url:
DOI: 10.1155/2012/208650
PubMed: 22028962
PubMed Central: 3195498
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Nuclear Transport: A Switch for the Oxidative Stress—Signaling Circuit?</title><author><name sortKey="Kodiha, Mohamed" sort="Kodiha, Mohamed" uniqKey="Kodiha M" first="Mohamed" last="Kodiha">Mohamed Kodiha</name></author><author><name sortKey="Stochaj, Ursula" sort="Stochaj, Ursula" uniqKey="Stochaj U" first="Ursula" last="Stochaj">Ursula Stochaj</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">22028962</idno><idno type="pmc">3195498</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3195498</idno><idno type="RBID">PMC:3195498</idno><idno type="doi">10.1155/2012/208650</idno><date when="2011">2011</date><idno type="wicri:Area/Pmc/Corpus">000C54</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000C54</idno><idno type="wicri:Area/Pmc/Curation">000C54</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000C54</idno><idno type="wicri:Area/Pmc/Checkpoint">000919</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000919</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Nuclear Transport: A Switch for the Oxidative Stress—Signaling Circuit?</title><author><name sortKey="Kodiha, Mohamed" sort="Kodiha, Mohamed" uniqKey="Kodiha M" first="Mohamed" last="Kodiha">Mohamed Kodiha</name></author><author><name sortKey="Stochaj, Ursula" sort="Stochaj, Ursula" uniqKey="Stochaj U" first="Ursula" last="Stochaj">Ursula Stochaj</name></author></analytic><series><title level="j">Journal of Signal Transduction</title><idno type="ISSN">2090-1739</idno><idno type="eISSN">2090-1747</idno><imprint><date when="2011">2011</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Imbalances in the formation and clearance of reactive oxygen species (ROS) can lead to oxidative stress and subsequent changes that affect all aspects of physiology. To limit and repair the damage generated by ROS, cells have developed a multitude of responses. A hallmark of these responses is the activation of signaling pathways that modulate the function of downstream targets in different cellular locations. To this end, critical steps of the stress response that occur in the nucleus and cytoplasm have to be coordinated, which makes the proper communication between both compartments mandatory. Here, we discuss the interdependence of ROS-mediated signaling and the transport of macromolecules across the nuclear envelope. We highlight examples of oxidant-dependent nuclear trafficking and describe the impact of oxidative stress on the transport apparatus. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Signal Transduct</journal-id><journal-id journal-id-type="publisher-id">JST</journal-id><journal-title-group><journal-title>Journal of Signal Transduction</journal-title></journal-title-group><issn pub-type="ppub">2090-1739</issn><issn pub-type="epub">2090-1747</issn><publisher><publisher-name>Hindawi Publishing Corporation</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">22028962</article-id><article-id pub-id-type="pmc">3195498</article-id><article-id pub-id-type="doi">10.1155/2012/208650</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review Article</subject></subj-group></article-categories><title-group><article-title>Nuclear Transport: A Switch for the Oxidative Stress—Signaling Circuit?</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Kodiha</surname><given-names>Mohamed</given-names></name></contrib><contrib contrib-type="author"><name><surname>Stochaj</surname><given-names>Ursula</given-names></name><xref ref-type="corresp" rid="cor1">*</xref></contrib></contrib-group><aff id="I1">Department of Physiology, McGill University, Montreal, QC, Canada H3G 1Y6</aff><author-notes><corresp id="cor1">*Ursula Stochaj: <email>ursula.stochaj@mcgill.ca</email></corresp><fn fn-type="other"><p>Academic Editor: Paola Chiarugi</p></fn></author-notes><pub-date pub-type="ppub"><year>2012</year></pub-date><pub-date pub-type="epub"><day>15</day><month>10</month><year>2011</year></pub-date><volume>2012</volume><elocation-id>208650</elocation-id><history><date date-type="received"><day>24</day><month>5</month><year>2011</year></date><date date-type="accepted"><day>5</day><month>7</month><year>2011</year></date></history><permissions><copyright-statement>Copyright © 2012 M. Kodiha and U. Stochaj.</copyright-statement><copyright-year>2012</copyright-year><license license-type="open-access"><license-p>This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p></license></permissions><abstract><p>Imbalances in the formation and clearance of reactive oxygen species (ROS) can lead to oxidative stress and subsequent changes that affect all aspects of physiology. To limit and repair the damage generated by ROS, cells have developed a multitude of responses. A hallmark of these responses is the activation of signaling pathways that modulate the function of downstream targets in different cellular locations. To this end, critical steps of the stress response that occur in the nucleus and cytoplasm have to be coordinated, which makes the proper communication between both compartments mandatory. Here, we discuss the interdependence of ROS-mediated signaling and the transport of macromolecules across the nuclear envelope. We highlight examples of oxidant-dependent nuclear trafficking and describe the impact of oxidative stress on the transport apparatus. Our paper concludes by proposing a cellular circuit of ROS-induced signaling, nuclear transport and repair.</p></abstract></article-meta></front><floats-group><fig id="fig1" position="float"><label>Figure 1</label><caption><p>Simplified model for classical nuclear import and Crm1-mediated export, two essential transport pathways. Classical nuclear import depends on the carrier importin-<italic>β</italic> and the adaptor protein importin-<italic>α</italic>. Together, importin-<italic>α</italic>/<italic>β</italic> move NLS-containing cargos to the nucleus. The absence of RanGTP from the cytoplasm permits the assembly of import complexes in the cytoplasm. Conversely, the high RanGTP concentration in the nucleus promotes the dissociation of classical import complexes after they translocate across the NPC. RanGTP in the nucleus is also necessary to generate export complexes that contain Crm1 and NES-containing cargo. The function of Crm1 is inhibited by leptomycin B (LMB).</p></caption><graphic xlink:href="JST2012-208650.001"></graphic></fig><fig id="fig2" position="float"><label>Figure 2</label><caption><p>Oxidative stress inhibits classical nuclear import and Crm1-mediated export. (a) Nuclear import. HeLa cells transiently synthesizing the import substrates NLS-mCherry or GFP-tagged glucocorticoid receptor (GR-GFP) were incubated under nonstress conditions (control) or with DEM as described [<xref ref-type="bibr" rid="B69">69</xref>]. Note that a significant amount of the reporter proteins relocated to the cytoplasm upon oxidant treatment, indicating that classical nuclear import was inhibited. (b) Nuclear export. HeLa cells synthesizing the fluorescent reporter protein mCit-NES, a Crm1 cargo, were exposed to DEM and processed as in part a. The Crm1 export cargo was excluded from the nucleus under control conditions, but relocated to nuclei upon oxidative stress. Size bar is 20 <italic>μ</italic>m.</p></caption><graphic xlink:href="JST2012-208650.002"></graphic></fig><fig id="fig3" position="float"><label>Figure 3</label><caption><p>Oxidative stress interferes with importin-<italic>α</italic>1-dependent import of endogenous cargos. The import of two endogenous proteins, the RNA-binding protein HuR and galectin-3, was monitored in HeLa cells under the conditions described for <xref ref-type="fig" rid="fig2">Figure 2(a)</xref>. Importin-<italic>α</italic>1 promotes nuclear import of both proteins. HuR and galectin-3 were visualized by indirect immunofluorescence and nuclei were stained with DAPI [<xref ref-type="bibr" rid="B69">69</xref>]. HuR was nuclear in control cells and redistributed to the cytoplasm of stressed cells, where it accumulated in stress granules (SGs). Similarly, galectin-3 was more concentrated in the nuclei of control cells and relocated to the cytoplasm upon DEM treatment. Arrows indicate the position of some of the SGs.</p></caption><graphic xlink:href="JST2012-208650.003"></graphic></fig><fig id="fig4" position="float"><label>Figure 4</label><caption><p>Mild and severe oxidative stress have different effects on nuclear transport factors. The effects of mild (2 mM DEM) and severe oxidative stress (10 mM H<sub>2</sub>O<sub>2</sub>) on the subcellular distribution of importin-<italic>α</italic>1, Ran, and HuR were analyzed in HeLa cells. Proteins were located by indirect immunofluorescence [<xref ref-type="bibr" rid="B39">39</xref>, <xref ref-type="bibr" rid="B69">69</xref>, <xref ref-type="bibr" rid="B119">79</xref>]. DEM treatment accumulated importin-<italic>α</italic>1 in nuclei but did not drastically affect the distribution of Ran. By contrast, severe oxidative stress induced by H<sub>2</sub>O<sub>2</sub> caused a pronounced nuclear accumulation of importin-<italic>α</italic>1 and collapsed the nucleocytoplasmic Ran gradient. Both treatments relocated HuR to the cytoplasm. However, DEM triggered the assembly of HuR-containing SGs, which were rare or absent upon incubation with H<sub>2</sub>O<sub>2</sub>.</p></caption><graphic xlink:href="JST2012-208650.004"></graphic></fig><fig id="fig5" position="float"><label>Figure 5</label><caption><p>Simplified model for the crosstalk between signaling and nuclear transport in response to oxidative stress. Oxidative stress impinges on signaling molecules and the nuclear transport apparatus, with chaperones modulating both processes. Different scenarios can explain the communication between nuclear transport and signaling pathways in oxidant-treated cells. In one case, oxidative stress alters the localization and activity of transport factors. This will change the subcellular distribution of key signaling molecules, which in turn affects the modification of downstream targets. Alternatively, the signaling pathways activated by oxidative stress cause the modification and redistribution of transport factors. Both scenarios are likely to take place side-by-side, and the balance of these events will ultimately determine cell fate.</p></caption><graphic xlink:href="JST2012-208650.005"></graphic></fig><table-wrap id="tab1" position="float"><label>Table 1</label><caption><p>Redox-sensitive cellular targets in eukaryotic cells. Components that alter their activity and/or nucleocytoplasmic distribution when ROS concentrations increase are listed. See text for details. </p></caption><table frame="hsides" rules="groups"><thead><tr><th align="left" rowspan="1" colspan="1">Component or process</th><th align="left" rowspan="1" colspan="1">Effect of ROS</th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1"><italic>Signaling proteins, transcriptional regulators</italic></td><td align="left" rowspan="1" colspan="1"> </td></tr><tr><td align="left" rowspan="1" colspan="1">JNK, MAPK</td><td align="left" rowspan="1" colspan="1">Activation</td></tr><tr><td align="left" rowspan="1" colspan="1">p38, MAPK</td><td align="left" rowspan="1" colspan="1">Activation, nuclear translocation</td></tr><tr><td align="left" rowspan="1" colspan="1">ERK1/2, MAPK</td><td align="left" rowspan="1" colspan="1">Activation, nuclear accumulation</td></tr><tr><td align="left" rowspan="1" colspan="1">PI3 kinase (some isoforms)</td><td align="left" rowspan="1" colspan="1">Activation, changes in nucleocytoplasmic distribution</td></tr><tr><td align="left" rowspan="1" colspan="1">5′-AMP activated kinase</td><td align="left" rowspan="1" colspan="1">Inhibition, nuclear accumulation; possibly by reduced nuclear export <italic>via</italic> Crm1</td></tr><tr><td align="left" rowspan="1" colspan="1">Human insulin receptor kinase activity</td><td align="left" rowspan="1" colspan="1">Activation</td></tr><tr><td align="left" rowspan="1" colspan="1">Src family kinases</td><td align="left" rowspan="1" colspan="1">Activation</td></tr><tr><td align="left" rowspan="1" colspan="1">EGFR</td><td align="left" rowspan="1" colspan="1">Nuclear translocation; DNA repair</td></tr><tr><td align="left" rowspan="1" colspan="1">Protein tyrosine phosphatases</td><td align="left" rowspan="1" colspan="1">Inactivation</td></tr><tr><td align="left" rowspan="1" colspan="1">PTEN</td><td align="left" rowspan="1" colspan="1">Nuclear accumulation; association with p53</td></tr><tr><td align="left" rowspan="1" colspan="1">STAT3</td><td align="left" rowspan="1" colspan="1">Nuclear translocation</td></tr><tr><td align="left" rowspan="1" colspan="1">NF-<italic>κ</italic>B, transcription factor</td><td align="left" rowspan="1" colspan="1">Nuclear accumulation; transcription</td></tr><tr><td align="left" rowspan="1" colspan="1">FoxO transcription factors</td><td align="left" rowspan="1" colspan="1">Nuclear translocation (i.e., FOXO1, FOXO3a, and FOXO4)</td></tr><tr><td align="left" rowspan="1" colspan="1">yAP-1, yeast transcription factor</td><td align="left" rowspan="1" colspan="1">Nuclear translocation</td></tr><tr><td align="left" rowspan="1" colspan="1">Msn2p, Msn4p, yeast transcription factors</td><td align="left" rowspan="1" colspan="1">Nuclear translocation, transcription</td></tr><tr><td align="left" rowspan="1" colspan="1">CREB</td><td align="left" rowspan="1" colspan="1">Phosphorylation, nuclear translocation</td></tr><tr><td align="left" rowspan="1" colspan="1">Nrf2</td><td align="left" rowspan="1" colspan="1">Nuclear accumulation</td></tr><tr><td align="left" rowspan="1" colspan="1">HMGB1</td><td align="left" rowspan="1" colspan="1">Cytoplasmic translocation</td></tr><tr><td align="left" rowspan="1" colspan="1">HuR, RNA-binding protein</td><td align="left" rowspan="1" colspan="1">Relocation to cytoplasm, accumulation in stress granules </td></tr><tr><td align="center" colspan="2" rowspan="1"><hr></hr></td></tr><tr><td align="left" rowspan="1" colspan="1"><italic>Nuclear transport apparatus</italic></td><td align="left" rowspan="1" colspan="1"> </td></tr><tr><td align="left" rowspan="1" colspan="1">Classical nuclear import</td><td align="left" rowspan="1" colspan="1">Inhibition</td></tr><tr><td align="left" rowspan="1" colspan="1">Crm1-dependent nuclear export</td><td align="left" rowspan="1" colspan="1">Inhibition</td></tr><tr><td align="left" rowspan="1" colspan="1">Ran, small GTPase; Gsp1 in <italic>S. cerevisiae </italic></td><td align="left" rowspan="1" colspan="1">Relocation to cytoplasm upon severe oxidative stress</td></tr><tr><td align="left" rowspan="1" colspan="1">Importin-<italic>α</italic>1, adaptor for classical nuclear import</td><td align="left" rowspan="1" colspan="1">Accumulation in nuclei, accumulation in cytoplasmic stress granules</td></tr><tr><td align="left" rowspan="1" colspan="1">Crm1, nuclear exporter</td><td align="left" rowspan="1" colspan="1">Accumulation at nuclear envelope</td></tr><tr><td align="left" rowspan="1" colspan="1">CAS, exporter for importin-<italic>α</italic></td><td align="left" rowspan="1" colspan="1">Nuclear accumulation</td></tr><tr><td align="left" rowspan="1" colspan="1">Multiple nucleoporins located at different positions within the nuclear pore complex: Nup358, Nup214, Nup88, Nup62, Nup153, Nup50, Nup98, and others</td><td align="left" rowspan="1" colspan="1">Changes in the association with nuclear envelope; altered nucleocytoplasmic distribution; degradation upon severe stress, in some cases mediated by caspases.</td></tr></tbody></table></table-wrap></floats-group></pmc><affiliations><list></list><tree><noCountry><name sortKey="Kodiha, Mohamed" sort="Kodiha, Mohamed" uniqKey="Kodiha M" first="Mohamed" last="Kodiha">Mohamed Kodiha</name><name sortKey="Stochaj, Ursula" sort="Stochaj, Ursula" uniqKey="Stochaj U" first="Ursula" last="Stochaj">Ursula Stochaj</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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