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Endogenous and Exogenous Modulation of Nrf2 Mediated Oxidative Stress Response in Bovine Granulosa Cells: Potential Implication for Ovarian Function

Identifieur interne : 000784 ( Pmc/Checkpoint ); précédent : 000783; suivant : 000785

Endogenous and Exogenous Modulation of Nrf2 Mediated Oxidative Stress Response in Bovine Granulosa Cells: Potential Implication for Ovarian Function

Auteurs : Omar Khadrawy ; Samuel Gebremedhn ; Dessie Salilew-Wondim ; Mohamed Omar Taqi ; Christiane Neuhoff ; Ernst Tholen ; Michael Hoelker [Allemagne] ; Karl Schellander [Allemagne] ; Dawit Tesfaye [Allemagne]

Source :

RBID : PMC:6480527

Abstract

Nrf2 is a redox sensitive transcription factor regulating the expression of antioxidant genes as defense mechanism against various stressors. The aim of this study is to investigate the potential role of noncoding miRNAs as endogenous and quercetin as exogenous regulators of Nrf2 pathway in bovine granulosa cells. For this cultured granulosa cells were used for modulation of miRNAs (miR-28, 153 and miR-708) targeting the bovine Nrf2 and supplementation of quercentin to investigate the regulatory mechanisms of the Nrf2 antioxidant system. Moreover, cultured cells were treated with hydrogen peroxide to induce oxidative stress in those cells. Our results showed that, oxidative stress activated the expression of Nrf2 as a defense mechanism, while suppressing the expression of those miRNAs. Overexpression of those miRNAs resulted in downregulation of Nrf2 expression resulted in higher ROS accumulation, reduced mitochondrial activity and cellular proliferation. Quercetin supplementation showed its protective role against oxidative stress induced by H2O2 by inducing the expression of antioxidant enzymes. In conclusion, this study highlighted the involvement of miR-153, miR-28 and miR-708 in regulatory network of Nrf2 mediated antioxidant system in bovine granulosa cells function. Furthermore, quercetin at a low dose played a protective role in bovine granulosa cells against oxidative stress damage.


Url:
DOI: 10.3390/ijms20071635
PubMed: 30986945
PubMed Central: 6480527


Affiliations:

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PMC:6480527

Le document en format XML

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<title xml:lang="en" level="a" type="main">Endogenous and Exogenous Modulation of Nrf2 Mediated Oxidative Stress Response in Bovine Granulosa Cells: Potential Implication for Ovarian Function</title>
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<name sortKey="Khadrawy, Omar" sort="Khadrawy, Omar" uniqKey="Khadrawy O" first="Omar" last="Khadrawy">Omar Khadrawy</name>
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<nlm:aff id="af1-ijms-20-01635">Institute of Animal Science, Department of Animal Breeding and Husbandry, University of Bonn, 53175 Bonn, Germany;
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<email>seta@itw.uni-bonn.de</email>
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<nlm:aff id="af1-ijms-20-01635">Institute of Animal Science, Department of Animal Breeding and Husbandry, University of Bonn, 53175 Bonn, Germany;
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<nlm:aff id="af1-ijms-20-01635">Institute of Animal Science, Department of Animal Breeding and Husbandry, University of Bonn, 53175 Bonn, Germany;
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(O.K.);
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<name sortKey="Hoelker, Michael" sort="Hoelker, Michael" uniqKey="Hoelker M" first="Michael" last="Hoelker">Michael Hoelker</name>
<affiliation>
<nlm:aff id="af1-ijms-20-01635">Institute of Animal Science, Department of Animal Breeding and Husbandry, University of Bonn, 53175 Bonn, Germany;
<email>okha@itw.uni-bonn.de</email>
(O.K.);
<email>seta@itw.uni-bonn.de</email>
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<email>cneu@itw.uni-bonn.de</email>
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(K.S.)</nlm:aff>
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<affiliation wicri:level="1">
<nlm:aff id="af2-ijms-20-01635">Teaching and Research Station Frankenforst, Faculty of Agriculture, University of Bonn, 53639 Königswinter, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Teaching and Research Station Frankenforst, Faculty of Agriculture, University of Bonn, 53639 Königswinter</wicri:regionArea>
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<nlm:aff id="af3-ijms-20-01635">Center of Integrated Dairy Research, University of Bonn, 53175 Bonn, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Center of Integrated Dairy Research, University of Bonn, 53175 Bonn</wicri:regionArea>
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<region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region>
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<author>
<name sortKey="Schellander, Karl" sort="Schellander, Karl" uniqKey="Schellander K" first="Karl" last="Schellander">Karl Schellander</name>
<affiliation>
<nlm:aff id="af1-ijms-20-01635">Institute of Animal Science, Department of Animal Breeding and Husbandry, University of Bonn, 53175 Bonn, Germany;
<email>okha@itw.uni-bonn.de</email>
(O.K.);
<email>seta@itw.uni-bonn.de</email>
(S.G.);
<email>dsal@itw.uni-bonn.de</email>
(D.S.-W.);
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(K.S.)</nlm:aff>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="af3-ijms-20-01635">Center of Integrated Dairy Research, University of Bonn, 53175 Bonn, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Center of Integrated Dairy Research, University of Bonn, 53175 Bonn</wicri:regionArea>
<placeName>
<region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region>
<region type="district" nuts="2">District de Cologne</region>
<settlement type="city">Bonn</settlement>
</placeName>
</affiliation>
</author>
<author>
<name sortKey="Tesfaye, Dawit" sort="Tesfaye, Dawit" uniqKey="Tesfaye D" first="Dawit" last="Tesfaye">Dawit Tesfaye</name>
<affiliation>
<nlm:aff id="af1-ijms-20-01635">Institute of Animal Science, Department of Animal Breeding and Husbandry, University of Bonn, 53175 Bonn, Germany;
<email>okha@itw.uni-bonn.de</email>
(O.K.);
<email>seta@itw.uni-bonn.de</email>
(S.G.);
<email>dsal@itw.uni-bonn.de</email>
(D.S.-W.);
<email>mtaq@itw.uni-bonn.de</email>
(M.O.T.);
<email>cneu@itw.uni-bonn.de</email>
(C.N.);
<email>etho@itw.uni-bonn.de</email>
(E.T.);
<email>mhoe@itw.uni-bonn.de</email>
(M.H.);
<email>ksch@itw.uni-bonn.de</email>
(K.S.)</nlm:aff>
</affiliation>
<affiliation wicri:level="3">
<nlm:aff id="af3-ijms-20-01635">Center of Integrated Dairy Research, University of Bonn, 53175 Bonn, Germany</nlm:aff>
<country xml:lang="fr">Allemagne</country>
<wicri:regionArea>Center of Integrated Dairy Research, University of Bonn, 53175 Bonn</wicri:regionArea>
<placeName>
<region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region>
<region type="district" nuts="2">District de Cologne</region>
<settlement type="city">Bonn</settlement>
</placeName>
</affiliation>
</author>
</analytic>
<series>
<title level="j">International Journal of Molecular Sciences</title>
<idno type="eISSN">1422-0067</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>Nrf2 is a redox sensitive transcription factor regulating the expression of antioxidant genes as defense mechanism against various stressors. The aim of this study is to investigate the potential role of noncoding miRNAs as endogenous and quercetin as exogenous regulators of Nrf2 pathway in bovine granulosa cells. For this cultured granulosa cells were used for modulation of miRNAs (miR-28, 153 and miR-708) targeting the bovine Nrf2 and supplementation of quercentin to investigate the regulatory mechanisms of the Nrf2 antioxidant system. Moreover, cultured cells were treated with hydrogen peroxide to induce oxidative stress in those cells. Our results showed that, oxidative stress activated the expression of Nrf2 as a defense mechanism, while suppressing the expression of those miRNAs. Overexpression of those miRNAs resulted in downregulation of Nrf2 expression resulted in higher ROS accumulation, reduced mitochondrial activity and cellular proliferation. Quercetin supplementation showed its protective role against oxidative stress induced by H
<sub>2</sub>
O
<sub>2</sub>
by inducing the expression of antioxidant enzymes. In conclusion, this study highlighted the involvement of miR-153, miR-28 and miR-708 in regulatory network of Nrf2 mediated antioxidant system in bovine granulosa cells function. Furthermore, quercetin at a low dose played a protective role in bovine granulosa cells against oxidative stress damage.</p>
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</TEI>
<pmc article-type="research-article">
<pmc-dir>properties open_access</pmc-dir>
<front>
<journal-meta>
<journal-id journal-id-type="nlm-ta">Int J Mol Sci</journal-id>
<journal-id journal-id-type="iso-abbrev">Int J Mol Sci</journal-id>
<journal-id journal-id-type="publisher-id">ijms</journal-id>
<journal-title-group>
<journal-title>International Journal of Molecular Sciences</journal-title>
</journal-title-group>
<issn pub-type="epub">1422-0067</issn>
<publisher>
<publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta>
<article-id pub-id-type="pmid">30986945</article-id>
<article-id pub-id-type="pmc">6480527</article-id>
<article-id pub-id-type="doi">10.3390/ijms20071635</article-id>
<article-id pub-id-type="publisher-id">ijms-20-01635</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Endogenous and Exogenous Modulation of Nrf2 Mediated Oxidative Stress Response in Bovine Granulosa Cells: Potential Implication for Ovarian Function</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-1319-3089</contrib-id>
<name>
<surname>Khadrawy</surname>
<given-names>Omar</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-01635">1</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-9977-2347</contrib-id>
<name>
<surname>Gebremedhn</surname>
<given-names>Samuel</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-01635">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Salilew-Wondim</surname>
<given-names>Dessie</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-01635">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Taqi</surname>
<given-names>Mohamed Omar</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-01635">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Neuhoff</surname>
<given-names>Christiane</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-01635">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Tholen</surname>
<given-names>Ernst</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-01635">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Hoelker</surname>
<given-names>Michael</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-01635">1</xref>
<xref ref-type="aff" rid="af2-ijms-20-01635">2</xref>
<xref ref-type="aff" rid="af3-ijms-20-01635">3</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Schellander</surname>
<given-names>Karl</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-01635">1</xref>
<xref ref-type="aff" rid="af3-ijms-20-01635">3</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-8166-0606</contrib-id>
<name>
<surname>Tesfaye</surname>
<given-names>Dawit</given-names>
</name>
<xref ref-type="aff" rid="af1-ijms-20-01635">1</xref>
<xref ref-type="aff" rid="af3-ijms-20-01635">3</xref>
<xref rid="c1-ijms-20-01635" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="af1-ijms-20-01635">
<label>1</label>
Institute of Animal Science, Department of Animal Breeding and Husbandry, University of Bonn, 53175 Bonn, Germany;
<email>okha@itw.uni-bonn.de</email>
(O.K.);
<email>seta@itw.uni-bonn.de</email>
(S.G.);
<email>dsal@itw.uni-bonn.de</email>
(D.S.-W.);
<email>mtaq@itw.uni-bonn.de</email>
(M.O.T.);
<email>cneu@itw.uni-bonn.de</email>
(C.N.);
<email>etho@itw.uni-bonn.de</email>
(E.T.);
<email>mhoe@itw.uni-bonn.de</email>
(M.H.);
<email>ksch@itw.uni-bonn.de</email>
(K.S.)</aff>
<aff id="af2-ijms-20-01635">
<label>2</label>
Teaching and Research Station Frankenforst, Faculty of Agriculture, University of Bonn, 53639 Königswinter, Germany</aff>
<aff id="af3-ijms-20-01635">
<label>3</label>
Center of Integrated Dairy Research, University of Bonn, 53175 Bonn, Germany</aff>
<author-notes>
<corresp id="c1-ijms-20-01635">
<label>*</label>
Correspondence:
<email>tesfaye@itw.uni-bonn.de</email>
</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>02</day>
<month>4</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection">
<month>4</month>
<year>2019</year>
</pub-date>
<volume>20</volume>
<issue>7</issue>
<elocation-id>1635</elocation-id>
<history>
<date date-type="received">
<day>18</day>
<month>2</month>
<year>2019</year>
</date>
<date date-type="accepted">
<day>29</day>
<month>3</month>
<year>2019</year>
</date>
</history>
<permissions>
<copyright-statement>© 2019 by the authors.</copyright-statement>
<copyright-year>2019</copyright-year>
<license license-type="open-access">
<license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (
<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<abstract>
<p>Nrf2 is a redox sensitive transcription factor regulating the expression of antioxidant genes as defense mechanism against various stressors. The aim of this study is to investigate the potential role of noncoding miRNAs as endogenous and quercetin as exogenous regulators of Nrf2 pathway in bovine granulosa cells. For this cultured granulosa cells were used for modulation of miRNAs (miR-28, 153 and miR-708) targeting the bovine Nrf2 and supplementation of quercentin to investigate the regulatory mechanisms of the Nrf2 antioxidant system. Moreover, cultured cells were treated with hydrogen peroxide to induce oxidative stress in those cells. Our results showed that, oxidative stress activated the expression of Nrf2 as a defense mechanism, while suppressing the expression of those miRNAs. Overexpression of those miRNAs resulted in downregulation of Nrf2 expression resulted in higher ROS accumulation, reduced mitochondrial activity and cellular proliferation. Quercetin supplementation showed its protective role against oxidative stress induced by H
<sub>2</sub>
O
<sub>2</sub>
by inducing the expression of antioxidant enzymes. In conclusion, this study highlighted the involvement of miR-153, miR-28 and miR-708 in regulatory network of Nrf2 mediated antioxidant system in bovine granulosa cells function. Furthermore, quercetin at a low dose played a protective role in bovine granulosa cells against oxidative stress damage.</p>
</abstract>
<kwd-group>
<kwd>Nrf2 signaling pathway</kwd>
<kwd>miRNAs</kwd>
<kwd>oxidative stress</kwd>
<kwd>quercetin</kwd>
<kwd>bovine granulosa cells</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group>
<fig id="ijms-20-01635-f001" orientation="portrait" position="float">
<label>Figure 1</label>
<caption>
<p>Conserved binding site of miR-153, miR-28 and miR-708 are located between 105–112 and 58–65, respectively in bovine
<italic>Nrf2</italic>
3′-UTR (
<bold>A</bold>
). The luciferase firefly activity is reduced in granulosa cells co-transfected with bta-miR-153, miR-28 and miR-708 mimics with the wild type pmiRGlo expression vector (
<bold>B</bold>
). H
<sub>2</sub>
O
<sub>2</sub>
-induced oxidative stress increased cellular mRNA expression level of
<italic>Nrf2</italic>
(
<bold>C</bold>
), as well as decreased miR-153, miR-28 and miR-708 expression level (
<bold>D</bold>
). qRT-PCR analysis of
<italic>Nrf2</italic>
, miR-153, miR-28 and miR-708 in granulosa cells under normal condition (white bar) and oxidative stress condition (black bar). Data are presented mean ± SEM of three independent biological replicates. Bars with different letters (a,b) showed statistically significant differences (
<italic>p</italic>
< 0.05).</p>
</caption>
<graphic xlink:href="ijms-20-01635-g001"></graphic>
</fig>
<fig id="ijms-20-01635-f002" orientation="portrait" position="float">
<label>Figure 2</label>
<caption>
<p>Quantitative RT-PCR of
<italic>Nrf2</italic>
and its downstream antioxidants in bovine granulosa cells co-transfected with miR-153, miR-28 and miR-708 mimics (
<bold>A</bold>
). Immunocytochemistry of Nrf2 in bovine granulosa cells co-transfected with miR-153, miR-28 and miR-708 mimics (
<bold>B</bold>
). Data are presented as mean ± SEM of three independent biological replicates. Bars with different letters (a,b) showed statistically significant differences (
<italic>p</italic>
< 0.05).</p>
</caption>
<graphic xlink:href="ijms-20-01635-g002"></graphic>
</fig>
<fig id="ijms-20-01635-f003" orientation="portrait" position="float">
<label>Figure 3</label>
<caption>
<p>Higher level of intracellular Reactive oxygen species (ROS) level accompanied with lower mitochondrial activity in bovine granulosa cells co-transfected with miR-153, miR-28 and miR-708 (
<bold>A</bold>
). Moreover, overexpression of miR-153, miR-28 and miR-708 resulted in reduced bovine granulosa cell proliferation (
<bold>B</bold>
). White bar indicates the proliferation rate of the negative control and black bars represent proliferation rate of cells co-transfected with miRNA mimics. Data are presented as mean ± SEM of three independent biological replicates. Bars with different letters (a,b) showed statistically significant differences (
<italic>p</italic>
< 0.05).</p>
</caption>
<graphic xlink:href="ijms-20-01635-g003"></graphic>
</fig>
<fig id="ijms-20-01635-f004" orientation="portrait" position="float">
<label>Figure 4</label>
<caption>
<p>Selective knockdown of
<italic>Nrf2</italic>
reduced cellular mRNA expression level of
<italic>Nrf2</italic>
and its downstream antioxidant genes (
<bold>A</bold>
). Selective knockdown of
<italic>Nrf2</italic>
reduced bovine granulosa cell proliferation (
<bold>B</bold>
). Immunocytochemistry of
<italic>Nrf2</italic>
in bovine granulosa cells co-transfected with siRNA targeting the
<italic>Nrf2</italic>
(
<bold>C</bold>
). Moreover, higher intracellular ROS level and reduced mitochondrial activity (
<bold>D</bold>
) was observed in Nrf2-knockdown cells compared to the control counterparts. White bars indicate the cells transfected with the NC and the dark bars indicate cells transfected with siRNA targeting Nrf2. Data are presented as mean ± SEM of three independent biological replicates. Bars with different letters (a,b) showed statistically significant differences (
<italic>p</italic>
< 0.05).</p>
</caption>
<graphic xlink:href="ijms-20-01635-g004"></graphic>
</fig>
<fig id="ijms-20-01635-f005" orientation="portrait" position="float">
<label>Figure 5</label>
<caption>
<p>Overexpression of miR-153, miR-28 and miR-708 under oxidative stress conditions reduced mRNA expression level of Nrf2 and its downstream antioxidants(
<bold>A</bold>
). Immunocytochemistry of
<italic>Nrf2</italic>
in bovine granulosa cells co-transfected with miR-153, miR-28 and miR-708 mimics under oxidative stress conditions. The Nrf2 protein expression level was reduced under oxidative stress conditions followed by transfection with miR-153, miR-28 and miR-708 mimics individually compared to H
<sub>2</sub>
O
<sub>2</sub>
- treated group (
<bold>B</bold>
). White bars indicate the cells transfected with negative control without H
<sub>2</sub>
O
<sub>2</sub>
. Dark bars indicate cells transfected with negative control under H
<sub>2</sub>
O
<sub>2</sub>
and gray bars represent cells transfected with miRNA mimics under the H
<sub>2</sub>
O
<sub>2</sub>
challenge. Data are presented as mean ± SEM of three independent biological replicates. Bars with different letters (a,b,c) showed statistically significant differences (
<italic>p</italic>
< 0.05).</p>
</caption>
<graphic xlink:href="ijms-20-01635-g005"></graphic>
</fig>
<fig id="ijms-20-01635-f006" orientation="portrait" position="float">
<label>Figure 6</label>
<caption>
<p>Overexpression of miR-153, miR-28 and miR-708 under oxidative stress conditions increased the intracellular ROS level and reduced the mitochondrial activity compared to cells treated with only H
<sub>2</sub>
O
<sub>2</sub>
(
<bold>A</bold>
). Moreover, bovine granulosa cell proliferation was significantly reduced in cells transfected with miRNA mimics under H
<sub>2</sub>
O
<sub>2</sub>
(
<bold>B</bold>
). White bars indicate the cells transfected with negative control without H
<sub>2</sub>
O
<sub>2</sub>
. Dark bars indicate cells transfected with negative control under H
<sub>2</sub>
O
<sub>2</sub>
and gray bars represent cells transfected with miRNA mimics under the H
<sub>2</sub>
O
<sub>2</sub>
challenge. Data are presented as mean ± SEM of three independent biological replicates. Bars with different letters (a,b,c) showed statistically significant differences (
<italic>p</italic>
< 0.05).</p>
</caption>
<graphic xlink:href="ijms-20-01635-g006"></graphic>
</fig>
<fig id="ijms-20-01635-f007" orientation="portrait" position="float">
<label>Figure 7</label>
<caption>
<p>Treatment of cells with quercetin showed slight increment in the expression of
<italic>Nrf2</italic>
under oxidative stress (
<bold>A</bold>
). Bovine granulosa cells co-incubated with quercetin under oxidative stress condition showed upregulation of
<italic>Nrf2</italic>
at protein level (
<bold>B</bold>
). The white bar indicates the control group and the gray and black bars indicateH
<sub>2</sub>
O
<sub>2</sub>
treated and cells treated with both H
<sub>2</sub>
O
<sub>2</sub>
and quercetin, respectively. Data are presented as mean ±SEM of three independent biological replicates. Bars with different letters (a,b,c) showed statistically significant differences (
<italic>p</italic>
< 0.05).</p>
</caption>
<graphic xlink:href="ijms-20-01635-g007"></graphic>
</fig>
<fig id="ijms-20-01635-f008" orientation="portrait" position="float">
<label>Figure 8</label>
<caption>
<p>Quercetin rescue bovine granulosa cells from the oxidative stress damage induced by H
<sub>2</sub>
O
<sub>2</sub>
. Supplementation of quercetin following H
<sub>2</sub>
O
<sub>2</sub>
treatment increased granulosa cells proliferation (
<bold>A</bold>
), reduced intracellular ROS level (
<bold>B</bold>
) and increase mitochondrial activity (
<bold>C</bold>
) compared to cells treated with only H
<sub>2</sub>
O
<sub>2</sub>
. The white bar indicates the control group, while the gray and dark bars represent cells treated with only H
<sub>2</sub>
O
<sub>2</sub>
and cells treated with both H
<sub>2</sub>
O
<sub>2</sub>
and quercetin, respectively. Data are presented as mean ± SEM of three independent biological replicates. Bars with different letters (a,b,c) showed statistically significant differences (
<italic>p</italic>
< 0.05).</p>
</caption>
<graphic xlink:href="ijms-20-01635-g008"></graphic>
</fig>
<fig id="ijms-20-01635-f009" orientation="portrait" position="float">
<label>Figure 9</label>
<caption>
<p>Quercetin increased cellular mRNA expression level of
<italic>Nrf2</italic>
(
<bold>A</bold>
). The expression of miR-153, miR-28 and miR-708 was downregulated following quercetin treatment of cells (
<bold>B</bold>
). White bar represent the control groups and dark bars represent quercetin treated group. Data are presented as mean ± SEM of three independent biological replicates. Bars with different letters (a,b) showed statistically significant differences (
<italic>p</italic>
< 0.05).</p>
</caption>
<graphic xlink:href="ijms-20-01635-g009"></graphic>
</fig>
<fig id="ijms-20-01635-f010" orientation="portrait" position="float">
<label>Figure 10</label>
<caption>
<p>Model of the Nrf2-mediated oxidative stress response pathway in bovine granulosa cells under moderate oxidative stress conditions and under antioxidant (quercetin) supplementation. Oxidative stress and Que modulate
<italic>Nrf2</italic>
post transcriptionally through the inhibition of miR-153, miR-28 and miR-708, which targeted bovine
<italic>Nrf2</italic>
. After that, Nrf2 protein was activated and localized to the nucleus, where it binds to the antioxidants reactive element (ARE) in the promoters of antioxidant genes. This activates antioxidant gene expression so the respective proteins can scavenge the excessive ROS and subsequently maintain the activity of mitochondria.</p>
</caption>
<graphic xlink:href="ijms-20-01635-g010"></graphic>
</fig>
</floats-group>
</pmc>
<affiliations>
<list>
<country>
<li>Allemagne</li>
</country>
<region>
<li>District de Cologne</li>
<li>Rhénanie-du-Nord-Westphalie</li>
</region>
<settlement>
<li>Bonn</li>
</settlement>
</list>
<tree>
<noCountry>
<name sortKey="Gebremedhn, Samuel" sort="Gebremedhn, Samuel" uniqKey="Gebremedhn S" first="Samuel" last="Gebremedhn">Samuel Gebremedhn</name>
<name sortKey="Khadrawy, Omar" sort="Khadrawy, Omar" uniqKey="Khadrawy O" first="Omar" last="Khadrawy">Omar Khadrawy</name>
<name sortKey="Neuhoff, Christiane" sort="Neuhoff, Christiane" uniqKey="Neuhoff C" first="Christiane" last="Neuhoff">Christiane Neuhoff</name>
<name sortKey="Salilew Wondim, Dessie" sort="Salilew Wondim, Dessie" uniqKey="Salilew Wondim D" first="Dessie" last="Salilew-Wondim">Dessie Salilew-Wondim</name>
<name sortKey="Taqi, Mohamed Omar" sort="Taqi, Mohamed Omar" uniqKey="Taqi M" first="Mohamed Omar" last="Taqi">Mohamed Omar Taqi</name>
<name sortKey="Tholen, Ernst" sort="Tholen, Ernst" uniqKey="Tholen E" first="Ernst" last="Tholen">Ernst Tholen</name>
</noCountry>
<country name="Allemagne">
<noRegion>
<name sortKey="Hoelker, Michael" sort="Hoelker, Michael" uniqKey="Hoelker M" first="Michael" last="Hoelker">Michael Hoelker</name>
</noRegion>
<name sortKey="Hoelker, Michael" sort="Hoelker, Michael" uniqKey="Hoelker M" first="Michael" last="Hoelker">Michael Hoelker</name>
<name sortKey="Schellander, Karl" sort="Schellander, Karl" uniqKey="Schellander K" first="Karl" last="Schellander">Karl Schellander</name>
<name sortKey="Tesfaye, Dawit" sort="Tesfaye, Dawit" uniqKey="Tesfaye D" first="Dawit" last="Tesfaye">Dawit Tesfaye</name>
</country>
</tree>
</affiliations>
</record>

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