Zerumbone Protects against Carbon Tetrachloride (CCl4)-Induced Acute Liver Injury in Mice via Inhibiting Oxidative Stress and the Inflammatory Response: Involving the TLR4/NF-κB/COX-2 Pathway
Identifieur interne : 000644 ( Ncbi/Merge ); précédent : 000643; suivant : 000645Zerumbone Protects against Carbon Tetrachloride (CCl4)-Induced Acute Liver Injury in Mice via Inhibiting Oxidative Stress and the Inflammatory Response: Involving the TLR4/NF-κB/COX-2 Pathway
Auteurs : Meilin Wang ; Jingling Niu ; Lina Ou ; Bo Deng ; Yingyi Wang ; Sanqiang LiSource :
- Molecules [ 1420-3049 ] ; 2019.
Abstract
The natural compound Zerumbone (hereinafter referred to as ZER), a monocyclic sesquiterpenoid, has been reported to possess many pharmacological properties, including antioxidant and anti-inflammatory properties. This study aimed to investigate the underlying mechanism of ZER against acute liver injury (ALI) in CCl4-induced mice models. ICR mice were pretreated intraperitoneally with ZER for five days, then received a CCl4 injection two hours after the last ZER administration and were sacrificed 24 h later. Examination of serum aspartate aminotransferase (AST) and alanine aminotransferase (ALT) activities and the histopathological analysis confirmed the hepatoprotective effect of ZER. Biochemical assays revealed that ZER pretreatment recovered the activities of antioxidant enzymes superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px), restored the glutathione (GSH) reservoir, and reduced the production of malondialdehyde (MDA), all in a dose-dependent manner. Furthermore, administration of ZER in vivo reduced the release amounts of pro-inflammatory cytokines interleukin-6 (IL-6) and tumor necrosis factor alpha (TNF-α) and inhibited the increased protein levels of Toll-like receptor 4 (TLR4), nuclear factor-kappaB (NF-κB) p-p65, and cyclooxygenase (COX-2). Further studies in lipopolysaccharide (LPS)-induced Raw264.7 inflammatory cellular models verified that ZER could inhibit inflammation via inactivating the TLR4/NF-κB/COX-2 pathway. Thus, our study indicated that ZER exhibited a hepatoprotective effect against ALI through its antioxidant and anti-inflammatory activities and the possible mechanism might be mediated by the TLR4/NF-κB/COX-2 pathway. Collectively, our studies indicate ZER could be a potential candidate for chemical liver injury treatment.
Url:
DOI: 10.3390/molecules24101964
PubMed: 31121820
PubMed Central: 6571963
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Zerumbone Protects against Carbon Tetrachloride (CCl<sub>4</sub>)-Induced Acute Liver Injury in Mice via Inhibiting Oxidative Stress and the Inflammatory Response: Involving the TLR4/NF-κB/COX-2 Pathway</title><author><name sortKey="Wang, Meilin" sort="Wang, Meilin" uniqKey="Wang M" first="Meilin" last="Wang">Meilin Wang</name></author><author><name sortKey="Niu, Jingling" sort="Niu, Jingling" uniqKey="Niu J" first="Jingling" last="Niu">Jingling Niu</name></author><author><name sortKey="Ou, Lina" sort="Ou, Lina" uniqKey="Ou L" first="Lina" last="Ou">Lina Ou</name></author><author><name sortKey="Deng, Bo" sort="Deng, Bo" uniqKey="Deng B" first="Bo" last="Deng">Bo Deng</name></author><author><name sortKey="Wang, Yingyi" sort="Wang, Yingyi" uniqKey="Wang Y" first="Yingyi" last="Wang">Yingyi Wang</name></author><author><name sortKey="Li, Sanqiang" sort="Li, Sanqiang" uniqKey="Li S" first="Sanqiang" last="Li">Sanqiang Li</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31121820</idno><idno type="pmc">6571963</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6571963</idno><idno type="RBID">PMC:6571963</idno><idno type="doi">10.3390/molecules24101964</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">000713</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000713</idno><idno type="wicri:Area/Pmc/Curation">000713</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Curation">000713</idno><idno type="wicri:Area/Pmc/Checkpoint">000232</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Checkpoint">000232</idno><idno type="wicri:Area/Ncbi/Merge">000644</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Zerumbone Protects against Carbon Tetrachloride (CCl<sub>4</sub>)-Induced Acute Liver Injury in Mice via Inhibiting Oxidative Stress and the Inflammatory Response: Involving the TLR4/NF-κB/COX-2 Pathway</title><author><name sortKey="Wang, Meilin" sort="Wang, Meilin" uniqKey="Wang M" first="Meilin" last="Wang">Meilin Wang</name></author><author><name sortKey="Niu, Jingling" sort="Niu, Jingling" uniqKey="Niu J" first="Jingling" last="Niu">Jingling Niu</name></author><author><name sortKey="Ou, Lina" sort="Ou, Lina" uniqKey="Ou L" first="Lina" last="Ou">Lina Ou</name></author><author><name sortKey="Deng, Bo" sort="Deng, Bo" uniqKey="Deng B" first="Bo" last="Deng">Bo Deng</name></author><author><name sortKey="Wang, Yingyi" sort="Wang, Yingyi" uniqKey="Wang Y" first="Yingyi" last="Wang">Yingyi Wang</name></author><author><name sortKey="Li, Sanqiang" sort="Li, Sanqiang" uniqKey="Li S" first="Sanqiang" last="Li">Sanqiang Li</name></author></analytic><series><title level="j">Molecules</title><idno type="eISSN">1420-3049</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>The natural compound Zerumbone (hereinafter referred to as ZER), a monocyclic sesquiterpenoid, has been reported to possess many pharmacological properties, including antioxidant and anti-inflammatory properties. This study aimed to investigate the underlying mechanism of ZER against acute liver injury (ALI) in CCl<sub>4</sub>-induced mice models. ICR mice were pretreated intraperitoneally with ZER for five days, then received a CCl<sub>4</sub> injection two hours after the last ZER administration and were sacrificed 24 h later. Examination of serum aspartate aminotransferase (AST) and alanine aminotransferase (ALT) activities and the histopathological analysis confirmed the hepatoprotective effect of ZER. Biochemical assays revealed that ZER pretreatment recovered the activities of antioxidant enzymes superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px), restored the glutathione (GSH) reservoir, and reduced the production of malondialdehyde (MDA), all in a dose-dependent manner. Furthermore, administration of ZER in vivo reduced the release amounts of pro-inflammatory cytokines interleukin-6 (IL-6) and tumor necrosis factor alpha (TNF-α) and inhibited the increased protein levels of Toll-like receptor 4 (TLR4), nuclear factor-kappaB (NF-κB) p-p65, and cyclooxygenase (COX-2). Further studies in lipopolysaccharide (LPS)-induced Raw264.7 inflammatory cellular models verified that ZER could inhibit inflammation via inactivating the TLR4/NF-κB/COX-2 pathway. Thus, our study indicated that ZER exhibited a hepatoprotective effect against ALI through its antioxidant and anti-inflammatory activities and the possible mechanism might be mediated by the TLR4/NF-κB/COX-2 pathway. Collectively, our studies indicate ZER could be a potential candidate for chemical liver injury treatment.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Patten, D A" uniqKey="Patten D">D.A. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Molecules</journal-id><journal-id journal-id-type="iso-abbrev">Molecules</journal-id><journal-id journal-id-type="publisher-id">molecules</journal-id><journal-title-group><journal-title>Molecules</journal-title></journal-title-group><issn pub-type="epub">1420-3049</issn><publisher><publisher-name>MDPI</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31121820</article-id><article-id pub-id-type="pmc">6571963</article-id><article-id pub-id-type="doi">10.3390/molecules24101964</article-id><article-id pub-id-type="publisher-id">molecules-24-01964</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Zerumbone Protects against Carbon Tetrachloride (CCl<sub>4</sub>)-Induced Acute Liver Injury in Mice via Inhibiting Oxidative Stress and the Inflammatory Response: Involving the TLR4/NF-κB/COX-2 Pathway</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Meilin</given-names></name><xref ref-type="author-notes" rid="fn1-molecules-24-01964">†</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-6638-2692</contrib-id><name><surname>Niu</surname><given-names>Jingling</given-names></name><xref ref-type="author-notes" rid="fn1-molecules-24-01964">†</xref></contrib><contrib contrib-type="author"><name><surname>Ou</surname><given-names>Lina</given-names></name></contrib><contrib contrib-type="author"><name><surname>Deng</surname><given-names>Bo</given-names></name></contrib><contrib contrib-type="author"><name><surname>Wang</surname><given-names>Yingyi</given-names></name></contrib><contrib contrib-type="author"><name><surname>Li</surname><given-names>Sanqiang</given-names></name><xref rid="c1-molecules-24-01964" ref-type="corresp">*</xref></contrib></contrib-group><aff id="af1-molecules-24-01964">Medical College, Henan University of Science and Technology, Luoyang 471023, China;<email>meilin11954@163.com</email> (M.W.);<email>18438591806@163.com</email> (J.N.);<email>lina.ou@163.com</email> (L.O.);<email>deng_bo888@163.com</email> (B.D.);<email>yingyiwang2019@163.com</email> (Y.W.)</aff><author-notes><corresp id="c1-molecules-24-01964"><label>*</label>Correspondence: <email>sanqiangli2001@163.com</email>; Tel.: +86-152-9059-6918</corresp><fn id="fn1-molecules-24-01964"><label>†</label><p>These two authors contributed equally to this paper.</p></fn></author-notes><pub-date pub-type="epub"><day>22</day><month>5</month><year>2019</year></pub-date><pub-date pub-type="collection"><month>5</month><year>2019</year></pub-date><volume>24</volume><issue>10</issue><elocation-id>1964</elocation-id><history><date date-type="received"><day>16</day><month>4</month><year>2019</year></date><date date-type="accepted"><day>15</day><month>5</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>The natural compound Zerumbone (hereinafter referred to as ZER), a monocyclic sesquiterpenoid, has been reported to possess many pharmacological properties, including antioxidant and anti-inflammatory properties. This study aimed to investigate the underlying mechanism of ZER against acute liver injury (ALI) in CCl<sub>4</sub>-induced mice models. ICR mice were pretreated intraperitoneally with ZER for five days, then received a CCl<sub>4</sub> injection two hours after the last ZER administration and were sacrificed 24 h later. Examination of serum aspartate aminotransferase (AST) and alanine aminotransferase (ALT) activities and the histopathological analysis confirmed the hepatoprotective effect of ZER. Biochemical assays revealed that ZER pretreatment recovered the activities of antioxidant enzymes superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px), restored the glutathione (GSH) reservoir, and reduced the production of malondialdehyde (MDA), all in a dose-dependent manner. Furthermore, administration of ZER in vivo reduced the release amounts of pro-inflammatory cytokines interleukin-6 (IL-6) and tumor necrosis factor alpha (TNF-α) and inhibited the increased protein levels of Toll-like receptor 4 (TLR4), nuclear factor-kappaB (NF-κB) p-p65, and cyclooxygenase (COX-2). Further studies in lipopolysaccharide (LPS)-induced Raw264.7 inflammatory cellular models verified that ZER could inhibit inflammation via inactivating the TLR4/NF-κB/COX-2 pathway. Thus, our study indicated that ZER exhibited a hepatoprotective effect against ALI through its antioxidant and anti-inflammatory activities and the possible mechanism might be mediated by the TLR4/NF-κB/COX-2 pathway. Collectively, our studies indicate ZER could be a potential candidate for chemical liver injury treatment.</p></abstract><kwd-group><kwd>Zerumbone</kwd><kwd>acute liver injury</kwd><kwd>antioxidant</kwd><kwd>anti-inflammation</kwd><kwd>pro-inflammatory cytokine</kwd><kwd>TNF-α</kwd><kwd>IL-6</kwd><kwd>TLR4</kwd><kwd>NF-κB</kwd><kwd>COX-2</kwd></kwd-group></article-meta></front><floats-group><fig id="molecules-24-01964-f001" orientation="portrait" position="float"><label>Figure 1</label><caption><p>The structure of ZER (<bold>A</bold>) and the inhibitory effects of ZER on serum aspartate aminotransferase AST (<bold>B</bold>), alanine aminotransferase ALT (<bold>C</bold>), and liver index (<bold>D</bold>) on CCl<sub>4</sub>-induced acute liver injury (ALI) in mice. ZER-L, low dose group; ZER-M, medium dose group; ZER-L, high dose group. Values represent the mean ± SD (<italic>n</italic> = 10). <sup>###</sup><italic>p</italic> < 0.001 compared with the control group; * <italic>p</italic> < 0.05 and *** <italic>p</italic> < 0.001 compared with the CCl<sub>4</sub>-treated group.</p></caption><graphic xlink:href="molecules-24-01964-g001"></graphic></fig><fig id="molecules-24-01964-f002" orientation="portrait" position="float"><label>Figure 2</label><caption><p>Protective effects of ZER on liver histopathology in CCl<sub>4</sub>-induced ALI mice. Liver tissues were stained with Hematoxylin and Eosin (H&E) staining (40×). (<bold>A</bold>), control group; (<bold>B</bold>), CCl<sub>4</sub> group; (<bold>C</bold>), ZER-L group; (<bold>D</bold>), ZER-M group; (<bold>E</bold>), ZER-H group; (<bold>F</bold>), Bifendate (BIF) group. The pale pink areas are the necrotic areas. (<bold>G</bold>) Quantification of liver necrosis in histological sections (<italic>n</italic> = 10). Values represent the mean ± SD. <sup>###</sup><italic>p</italic> < 0.001 compared with the control group; * <italic>p</italic> < 0.05, ** <italic>p</italic> < 0.01, and *** <italic>p</italic> < 0.001 compared with the CCl<sub>4</sub>-treated group.</p></caption><graphic xlink:href="molecules-24-01964-g002"></graphic></fig><fig id="molecules-24-01964-f003" orientation="portrait" position="float"><label>Figure 3</label><caption><p>Effects of ZER on oxidative stress parameters (<bold>A</bold>) MDA, (<bold>B</bold>) GSH, (<bold>C</bold>) SOD, and (<bold>D</bold>) GSH-Px in liver tissue of CCl<sub>4</sub>-induced ALI mice. Values represent the mean ± SD (<italic>n</italic> = 10). <sup>###</sup><italic>p</italic> < 0.001 compared with the control group; * <italic>p</italic> < 0.05, ** <italic>p</italic> < 0.01, and *** <italic>p</italic> < 0.001 compared with the CCl<sub>4</sub>-treated group.</p></caption><graphic xlink:href="molecules-24-01964-g003"></graphic></fig><fig id="molecules-24-01964-f004" orientation="portrait" position="float"><label>Figure 4</label><caption><p>Effects of ZER on the levels of IL-6 ((<bold>A</bold>) serum and (<bold>C</bold>) liver tissue) and TNF-α ((<bold>B</bold>) serum and (<bold>D</bold>) liver tissue) in CCl<sub>4</sub>-induced ALI mice. Values represent the mean ± SD (<italic>n</italic> = 10). <sup>###</sup><italic>p</italic> < 0.001 compared with the control group; * <italic>p</italic> < 0.05, ** <italic>p</italic> < 0.01, and *** <italic>p</italic> < 0.001 compared with the CCl<sub>4</sub>-treated group.</p></caption><graphic xlink:href="molecules-24-01964-g004"></graphic></fig><fig id="molecules-24-01964-f005" orientation="portrait" position="float"><label>Figure 5</label><caption><p>Effects of ZER on the protein levels of TLR4, NF-κB (p-p65), and COX-2 in liver tissue of CCl<sub>4</sub>-induced ALI mice. (<bold>A</bold>) Western blotting analysis of TLR4, NF-κB (p-p65), and COX-2; Glyceraldehyde-3-phosphate dehydrogenase (GAPDH) was used as the loading control. (<bold>B</bold>) Quantification of the relative protein levels of TLR4, NF-κB (p-p65), and COX-2. Values represent the mean ± SD (<italic>n</italic> = 3). <sup>#</sup><italic>p</italic> < 0.05 and <sup>##</sup><italic>p</italic> < 0.01 compared with the control group; * <italic>p</italic> < 0.05 and ** <italic>p</italic> < 0.01 compared with the CCl<sub>4</sub>-treated group.</p></caption><graphic xlink:href="molecules-24-01964-g005"></graphic></fig><fig id="molecules-24-01964-f006" orientation="portrait" position="float"><label>Figure 6</label><caption><p>Effects of ZER on TLR4/NF-κB/COX-2 signaling in LPS-induced Raw264.7 cells. (<bold>A</bold>) The cytotoxicity of ZER was evaluated by MTT assay. (<bold>B</bold>) The cytotoxicity of LPS was evaluated by MTT assay. (<bold>C</bold>) Western blotting analysis of TLR4, NF-κB (p-p65), and COX-2; GAPDH was used as the loading control. (<bold>D</bold>) Quantification of the relative protein levels of TLR4, NF-κB (p-p65), and COX-2. Values represent the mean ± SD (<italic>n</italic> = 3). <sup>##</sup><italic>p</italic> < 0.01 and <sup>###</sup><italic>p</italic> < 0.001 compared with the control group; * <italic>p</italic> < 0.05 and ** <italic>p</italic> < 0.01 compared with the LPS treated group.</p></caption><graphic xlink:href="molecules-24-01964-g006"></graphic></fig></floats-group></pmc><affiliations><list></list><tree><noCountry><name sortKey="Deng, Bo" sort="Deng, Bo" uniqKey="Deng B" first="Bo" last="Deng">Bo Deng</name><name sortKey="Li, Sanqiang" sort="Li, Sanqiang" uniqKey="Li S" first="Sanqiang" last="Li">Sanqiang Li</name><name sortKey="Niu, Jingling" sort="Niu, Jingling" uniqKey="Niu J" first="Jingling" last="Niu">Jingling Niu</name><name sortKey="Ou, Lina" sort="Ou, Lina" uniqKey="Ou L" first="Lina" last="Ou">Lina Ou</name><name sortKey="Wang, Meilin" sort="Wang, Meilin" uniqKey="Wang M" first="Meilin" last="Wang">Meilin Wang</name><name sortKey="Wang, Yingyi" sort="Wang, Yingyi" uniqKey="Wang Y" first="Yingyi" last="Wang">Yingyi Wang</name></noCountry></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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