Manganese activates autophagy to alleviate endoplasmic reticulum stress–induced apoptosis via PERK pathway
Overexposure to manganese (Mn) is neurotoxic. Our previous research has demonstrated that the interaction of endoplasmic reticulum (ER) stress and autophagy participates in the early stage of Mn‐mediated neurotoxicity in mouse. However, the mechanisms of ER stress signalling pathways in the initiati...
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| Veröffentlicht in: | Journal of cellular and molecular medicine 2020-01, Vol.24 (1), p.328-341 |
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| creator | Liu, Chang Yan, Dong‐Ying Wang, Can Ma, Zhuo Deng, Yu Liu, Wei Xu, Bin |
| description | Overexposure to manganese (Mn) is neurotoxic. Our previous research has demonstrated that the interaction of endoplasmic reticulum (ER) stress and autophagy participates in the early stage of Mn‐mediated neurotoxicity in mouse. However, the mechanisms of ER stress signalling pathways in the initiation of autophagy remain confused. In the current study, we first validated that ER stress–mediated cell apoptosis is accompanied by autophagy in SH‐SY5Y cells. Then, we found that inhibiting ER stress with 4‐phenylbutyrate (4‐PBA) decreased ER stress–related protein expression and reduced cell apoptosis, whereas blocking autophagy with 3‐methyladenine (3‐MA) increased cell apoptosis. These data indicate that protective autophagy was activated to alleviate ER stress–mediated apoptosis. Knockdown of the protein kinase RNA‐like ER kinase (PERK) gene inhibited Mn‐induced autophagy and weakened the interaction between ATF4 and the LC3 promoter. Our results reveal a novel molecular mechanism in which ER stress may regulate autophagy via the PERK/eIF2α/ATF4 signalling pathway. Additionally, Mn may activate protective autophagy to alleviate ER stress–mediated apoptosis via the PERK/eIF2α/ATF4 signalling pathway in SH‐SY5Y cells. |
| doi_str_mv | 10.1111/jcmm.14732 |
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Our previous research has demonstrated that the interaction of endoplasmic reticulum (ER) stress and autophagy participates in the early stage of Mn‐mediated neurotoxicity in mouse. However, the mechanisms of ER stress signalling pathways in the initiation of autophagy remain confused. In the current study, we first validated that ER stress–mediated cell apoptosis is accompanied by autophagy in SH‐SY5Y cells. Then, we found that inhibiting ER stress with 4‐phenylbutyrate (4‐PBA) decreased ER stress–related protein expression and reduced cell apoptosis, whereas blocking autophagy with 3‐methyladenine (3‐MA) increased cell apoptosis. These data indicate that protective autophagy was activated to alleviate ER stress–mediated apoptosis. Knockdown of the protein kinase RNA‐like ER kinase (PERK) gene inhibited Mn‐induced autophagy and weakened the interaction between ATF4 and the LC3 promoter. Our results reveal a novel molecular mechanism in which ER stress may regulate autophagy via the PERK/eIF2α/ATF4 signalling pathway. Additionally, Mn may activate protective autophagy to alleviate ER stress–mediated apoptosis via the PERK/eIF2α/ATF4 signalling pathway in SH‐SY5Y cells.</description><identifier>ISSN: 1582-1838</identifier><identifier>EISSN: 1582-4934</identifier><identifier>DOI: 10.1111/jcmm.14732</identifier><identifier>PMID: 31639278</identifier><language>eng</language><publisher>England: John Wiley & Sons, Inc</publisher><subject>Activating Transcription Factor 4 - metabolism ; Apoptosis ; Apoptosis - drug effects ; Autophagy ; Autophagy - drug effects ; Cell Line, Tumor ; Cytotoxicity ; eIF-2 Kinase - metabolism ; Endoplasmic reticulum ; endoplasmic reticulum stress ; Endoplasmic Reticulum Stress - drug effects ; Enzymes ; Flow cytometry ; Gene expression ; Gene Knockdown Techniques ; Homeostasis ; Humans ; Kinases ; Manganese ; Manganese - pharmacology ; Microtubule-Associated Proteins - genetics ; Neurotoxicity ; Original ; PERK signalling pathway ; Phagocytosis ; Phenylbutyric acid ; Promoter Regions, Genetic - genetics ; Protein kinase ; Proteins ; Reagents ; Ribonucleic acid ; RNA ; Signal transduction ; Signal Transduction - drug effects ; Stress</subject><ispartof>Journal of cellular and molecular medicine, 2020-01, Vol.24 (1), p.328-341</ispartof><rights>2019 The Authors. published by Foundation for Cellular and Molecular Medicine and John Wiley & Sons Ltd</rights><rights>2019 The Authors. Journal of Cellular and Molecular Medicine published by Foundation for Cellular and Molecular Medicine and John Wiley & Sons Ltd.</rights><rights>2020. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4762-cad6379ca0ee151ee1eb5d192e8c8cd74c2773b83f6c33bf05f9f8f8e1dc0d843</citedby><cites>FETCH-LOGICAL-c4762-cad6379ca0ee151ee1eb5d192e8c8cd74c2773b83f6c33bf05f9f8f8e1dc0d843</cites><orcidid>0000-0001-8024-2066</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6933331/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6933331/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,1417,11562,27924,27925,45574,45575,46052,46476,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31639278$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Chang</creatorcontrib><creatorcontrib>Yan, Dong‐Ying</creatorcontrib><creatorcontrib>Wang, Can</creatorcontrib><creatorcontrib>Ma, Zhuo</creatorcontrib><creatorcontrib>Deng, Yu</creatorcontrib><creatorcontrib>Liu, Wei</creatorcontrib><creatorcontrib>Xu, Bin</creatorcontrib><title>Manganese activates autophagy to alleviate endoplasmic reticulum stress–induced apoptosis via PERK pathway</title><title>Journal of cellular and molecular medicine</title><addtitle>J Cell Mol Med</addtitle><description>Overexposure to manganese (Mn) is neurotoxic. Our previous research has demonstrated that the interaction of endoplasmic reticulum (ER) stress and autophagy participates in the early stage of Mn‐mediated neurotoxicity in mouse. However, the mechanisms of ER stress signalling pathways in the initiation of autophagy remain confused. In the current study, we first validated that ER stress–mediated cell apoptosis is accompanied by autophagy in SH‐SY5Y cells. Then, we found that inhibiting ER stress with 4‐phenylbutyrate (4‐PBA) decreased ER stress–related protein expression and reduced cell apoptosis, whereas blocking autophagy with 3‐methyladenine (3‐MA) increased cell apoptosis. These data indicate that protective autophagy was activated to alleviate ER stress–mediated apoptosis. Knockdown of the protein kinase RNA‐like ER kinase (PERK) gene inhibited Mn‐induced autophagy and weakened the interaction between ATF4 and the LC3 promoter. Our results reveal a novel molecular mechanism in which ER stress may regulate autophagy via the PERK/eIF2α/ATF4 signalling pathway. Additionally, Mn may activate protective autophagy to alleviate ER stress–mediated apoptosis via the PERK/eIF2α/ATF4 signalling pathway in SH‐SY5Y cells.</description><subject>Activating Transcription Factor 4 - metabolism</subject><subject>Apoptosis</subject><subject>Apoptosis - drug effects</subject><subject>Autophagy</subject><subject>Autophagy - drug effects</subject><subject>Cell Line, Tumor</subject><subject>Cytotoxicity</subject><subject>eIF-2 Kinase - metabolism</subject><subject>Endoplasmic reticulum</subject><subject>endoplasmic reticulum stress</subject><subject>Endoplasmic Reticulum Stress - drug effects</subject><subject>Enzymes</subject><subject>Flow cytometry</subject><subject>Gene expression</subject><subject>Gene Knockdown Techniques</subject><subject>Homeostasis</subject><subject>Humans</subject><subject>Kinases</subject><subject>Manganese</subject><subject>Manganese - pharmacology</subject><subject>Microtubule-Associated Proteins - genetics</subject><subject>Neurotoxicity</subject><subject>Original</subject><subject>PERK signalling pathway</subject><subject>Phagocytosis</subject><subject>Phenylbutyric acid</subject><subject>Promoter Regions, Genetic - genetics</subject><subject>Protein kinase</subject><subject>Proteins</subject><subject>Reagents</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Signal transduction</subject><subject>Signal Transduction - drug effects</subject><subject>Stress</subject><issn>1582-1838</issn><issn>1582-4934</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>WIN</sourceid><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kc9uEzEQxi0EoiVw4QGQJW5IKbZn_3gvSCgqUGgEQnC2HHs2cbS7Xmxvqtx4B96QJ6lL0qpcOoexNf7Np0_-CHnJ2RnP9XZr-v6MFzWIR-SUl1LMiwaKx8c7lyBPyLMYt4xBxaF5Sk6AV9CIWp6SbqmHtR4wItUmuZ1OGKmekh83er2nyVPddbhzeU5xsH7sdOydoQGTM1M39TSmgDH-_f3HDXYyaKke_Zh8dJHmNfrt_PsXOuq0udL75-RJq7uIL47njPz8cP5j8Wl--fXjxeL95dwUdSXmRtsK6sZohshLnhuuSssbgdJIY-vCiLqGlYS2MgCrlpVt08pWIreGWVnAjLw76I7TqkdrcEhBd2oMrtdhr7x26v-XwW3U2u9U1UAungVeHwWC_zVhTGrrpzBkz0qUopQSmGAPUgAs51Hnf56RNwfKBB9jwPbOB2fqJj91k5_6l1-GX913fofeBpYBfgCuXIf7B6TU58VyeRC9BrZhqcc</recordid><startdate>202001</startdate><enddate>202001</enddate><creator>Liu, Chang</creator><creator>Yan, Dong‐Ying</creator><creator>Wang, Can</creator><creator>Ma, Zhuo</creator><creator>Deng, Yu</creator><creator>Liu, Wei</creator><creator>Xu, Bin</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>24P</scope><scope>WIN</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QP</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>RC3</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-8024-2066</orcidid></search><sort><creationdate>202001</creationdate><title>Manganese activates autophagy to alleviate endoplasmic reticulum stress–induced apoptosis via PERK pathway</title><author>Liu, Chang ; Yan, Dong‐Ying ; Wang, Can ; Ma, Zhuo ; Deng, Yu ; Liu, Wei ; Xu, Bin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4762-cad6379ca0ee151ee1eb5d192e8c8cd74c2773b83f6c33bf05f9f8f8e1dc0d843</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Activating Transcription Factor 4 - metabolism</topic><topic>Apoptosis</topic><topic>Apoptosis - drug effects</topic><topic>Autophagy</topic><topic>Autophagy - drug effects</topic><topic>Cell Line, Tumor</topic><topic>Cytotoxicity</topic><topic>eIF-2 Kinase - metabolism</topic><topic>Endoplasmic reticulum</topic><topic>endoplasmic reticulum stress</topic><topic>Endoplasmic Reticulum Stress - drug effects</topic><topic>Enzymes</topic><topic>Flow cytometry</topic><topic>Gene expression</topic><topic>Gene Knockdown Techniques</topic><topic>Homeostasis</topic><topic>Humans</topic><topic>Kinases</topic><topic>Manganese</topic><topic>Manganese - pharmacology</topic><topic>Microtubule-Associated Proteins - genetics</topic><topic>Neurotoxicity</topic><topic>Original</topic><topic>PERK signalling pathway</topic><topic>Phagocytosis</topic><topic>Phenylbutyric acid</topic><topic>Promoter Regions, Genetic - genetics</topic><topic>Protein kinase</topic><topic>Proteins</topic><topic>Reagents</topic><topic>Ribonucleic acid</topic><topic>RNA</topic><topic>Signal transduction</topic><topic>Signal Transduction - drug effects</topic><topic>Stress</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Chang</creatorcontrib><creatorcontrib>Yan, Dong‐Ying</creatorcontrib><creatorcontrib>Wang, Can</creatorcontrib><creatorcontrib>Ma, Zhuo</creatorcontrib><creatorcontrib>Deng, Yu</creatorcontrib><creatorcontrib>Liu, Wei</creatorcontrib><creatorcontrib>Xu, Bin</creatorcontrib><collection>Wiley-Blackwell Open Access Titles</collection><collection>Wiley Online Library (Open Access Collection)</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Science Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Science Database</collection><collection>Biological Science Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of cellular and molecular medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Chang</au><au>Yan, Dong‐Ying</au><au>Wang, Can</au><au>Ma, Zhuo</au><au>Deng, Yu</au><au>Liu, Wei</au><au>Xu, Bin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Manganese activates autophagy to alleviate endoplasmic reticulum stress–induced apoptosis via PERK pathway</atitle><jtitle>Journal of cellular and molecular medicine</jtitle><addtitle>J Cell Mol Med</addtitle><date>2020-01</date><risdate>2020</risdate><volume>24</volume><issue>1</issue><spage>328</spage><epage>341</epage><pages>328-341</pages><issn>1582-1838</issn><eissn>1582-4934</eissn><abstract>Overexposure to manganese (Mn) is neurotoxic. Our previous research has demonstrated that the interaction of endoplasmic reticulum (ER) stress and autophagy participates in the early stage of Mn‐mediated neurotoxicity in mouse. However, the mechanisms of ER stress signalling pathways in the initiation of autophagy remain confused. In the current study, we first validated that ER stress–mediated cell apoptosis is accompanied by autophagy in SH‐SY5Y cells. Then, we found that inhibiting ER stress with 4‐phenylbutyrate (4‐PBA) decreased ER stress–related protein expression and reduced cell apoptosis, whereas blocking autophagy with 3‐methyladenine (3‐MA) increased cell apoptosis. These data indicate that protective autophagy was activated to alleviate ER stress–mediated apoptosis. Knockdown of the protein kinase RNA‐like ER kinase (PERK) gene inhibited Mn‐induced autophagy and weakened the interaction between ATF4 and the LC3 promoter. Our results reveal a novel molecular mechanism in which ER stress may regulate autophagy via the PERK/eIF2α/ATF4 signalling pathway. Additionally, Mn may activate protective autophagy to alleviate ER stress–mediated apoptosis via the PERK/eIF2α/ATF4 signalling pathway in SH‐SY5Y cells.</abstract><cop>England</cop><pub>John Wiley & Sons, Inc</pub><pmid>31639278</pmid><doi>10.1111/jcmm.14732</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-8024-2066</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Activating Transcription Factor 4 - metabolism Apoptosis Apoptosis - drug effects Autophagy Autophagy - drug effects Cell Line, Tumor Cytotoxicity eIF-2 Kinase - metabolism Endoplasmic reticulum endoplasmic reticulum stress Endoplasmic Reticulum Stress - drug effects Enzymes Flow cytometry Gene expression Gene Knockdown Techniques Homeostasis Humans Kinases Manganese Manganese - pharmacology Microtubule-Associated Proteins - genetics Neurotoxicity Original PERK signalling pathway Phagocytosis Phenylbutyric acid Promoter Regions, Genetic - genetics Protein kinase Proteins Reagents Ribonucleic acid RNA Signal transduction Signal Transduction - drug effects Stress |
| title | Manganese activates autophagy to alleviate endoplasmic reticulum stress–induced apoptosis via PERK pathway |
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