Knockout of PRDX6 induces mitochondrial dysfunction and cell cycle arrest at G2/M in HepG2 hepatocarcinoma cells.
Identifieur interne : 000052 ( Main/Exploration ); précédent : 000051; suivant : 000053Knockout of PRDX6 induces mitochondrial dysfunction and cell cycle arrest at G2/M in HepG2 hepatocarcinoma cells.
Auteurs : María José L Pez-Grueso [Espagne] ; Daniel José Lagal [Espagne] ; Álvaro Fernando García-Jiménez [Espagne] ; Rosa María Tarradas [Espagne] ; Beatriz Carmona-Hidalgo [Espagne] ; José Peinado [Espagne] ; Raquel Requejo-Aguilar [Espagne] ; José Antonio Bárcena [Espagne] ; Carmen Alicia Padilla [Espagne]Source :
- Redox biology [ 2213-2317 ] ; 2020.
Abstract
Peroxiredoxin 6 (PRDX6) has been associated with tumor progression and cancer metastasis. Its acting on phospholipid hydroperoxides and its phospholipase-A2 activity are unique among the peroxiredoxin family and add complexity to its action mechanisms. As a first step towards the study of PRDX6 involvement in cancer, we have constructed a human hepatocarcinoma HepG2PRDX6-/- cell line using the CRISPR/Cas9 technique and have characterized the cellular response to lack of PRDX6. Applying quantitative global and redox proteomics, flow cytometry, in vivo extracellular flow analysis, Western blot and electron microscopy, we have detected diminished respiratory capacity, downregulation of mitochondrial proteins and altered mitochondrial morphology. Autophagic vesicles were abundant while the unfolded protein response (UPR), HIF1A and NRF2 transcription factors were not activated, despite increased levels of p62/SQSTM1 and reactive oxygen species (ROS). Insulin receptor (INSR), 3-phosphoinositide-dependent protein kinase 1 (PDPK1), uptake of glucose and hexokinase-2 (HK2) decreased markedly while nucleotide biosynthesis, lipogenesis and synthesis of long chain polyunsaturated fatty acids (LC-PUFA) increased. 254 Cys-peptides belonging to 202 proteins underwent significant redox changes. PRDX6 knockout had an antiproliferative effect due to cell cycle arrest at G2/M transition, without signs of apoptosis. Loss of PLA2 may affect the levels of specific lipids altering lipid signaling pathways, while loss of peroxidase activity could induce redox changes at critical sensitive cysteine residues in key proteins. Oxidation of specific cysteines in Proliferating Cell Nuclear Antigen (PCNA) could interfere with entry into mitosis. The GSH/Glutaredoxin system was downregulated likely contributing to these redox changes. Altogether the data demonstrate that loss of PRDX6 slows down cell division and alters metabolism and mitochondrial function, so that cell survival depends on glycolysis to lactate for ATP production and on AMPK-independent autophagy to obtain building blocks for biosynthesis. PRDX6 is an important link in the chain of elements connecting redox homeostasis and proliferation.
DOI: 10.1016/j.redox.2020.101737
PubMed: 33035814
PubMed Central: PMC7554216
Affiliations:
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Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba</wicri:regionArea><wicri:noRegion>Córdoba</wicri:noRegion></affiliation></author><author><name sortKey="Requejo Aguilar, Raquel" sort="Requejo Aguilar, Raquel" uniqKey="Requejo Aguilar R" first="Raquel" last="Requejo-Aguilar">Raquel Requejo-Aguilar</name><affiliation wicri:level="1"><nlm:affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba</wicri:regionArea><wicri:noRegion>Córdoba</wicri:noRegion></affiliation></author><author><name sortKey="Barcena, Jose Antonio" sort="Barcena, Jose Antonio" uniqKey="Barcena J" first="José Antonio" last="Bárcena">José Antonio Bárcena</name><affiliation wicri:level="1"><nlm:affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba, Spain. Electronic address: ja.barcena@uco.es.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba</wicri:regionArea><wicri:noRegion>Córdoba</wicri:noRegion></affiliation></author><author><name sortKey="Padilla, Carmen Alicia" sort="Padilla, Carmen Alicia" uniqKey="Padilla C" first="Carmen Alicia" last="Padilla">Carmen Alicia Padilla</name><affiliation wicri:level="1"><nlm:affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba, Spain.</nlm:affiliation><country xml:lang="fr">Espagne</country><wicri:regionArea>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba</wicri:regionArea><wicri:noRegion>Córdoba</wicri:noRegion></affiliation></author></analytic><series><title level="j">Redox biology</title><idno type="eISSN">2213-2317</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Peroxiredoxin 6 (PRDX6) has been associated with tumor progression and cancer metastasis. Its acting on phospholipid hydroperoxides and its phospholipase-A2 activity are unique among the peroxiredoxin family and add complexity to its action mechanisms. As a first step towards the study of PRDX6 involvement in cancer, we have constructed a human hepatocarcinoma HepG2<sup>PRDX6</sup><sup>-</sup><sup>/-</sup> cell line using the CRISPR/Cas9 technique and have characterized the cellular response to lack of PRDX6. Applying quantitative global and redox proteomics, flow cytometry, in vivo extracellular flow analysis, Western blot and electron microscopy, we have detected diminished respiratory capacity, downregulation of mitochondrial proteins and altered mitochondrial morphology. Autophagic vesicles were abundant while the unfolded protein response (UPR), HIF1A and NRF2 transcription factors were not activated, despite increased levels of p62/SQSTM1 and reactive oxygen species (ROS). Insulin receptor (INSR), 3-phosphoinositide-dependent protein kinase 1 (PDPK1), uptake of glucose and hexokinase-2 (HK2) decreased markedly while nucleotide biosynthesis, lipogenesis and synthesis of long chain polyunsaturated fatty acids (LC-PUFA) increased. 254 Cys-peptides belonging to 202 proteins underwent significant redox changes. PRDX6 knockout had an antiproliferative effect due to cell cycle arrest at G2/M transition, without signs of apoptosis. Loss of PLA2 may affect the levels of specific lipids altering lipid signaling pathways, while loss of peroxidase activity could induce redox changes at critical sensitive cysteine residues in key proteins. Oxidation of specific cysteines in Proliferating Cell Nuclear Antigen (PCNA) could interfere with entry into mitosis. The GSH/Glutaredoxin system was downregulated likely contributing to these redox changes. Altogether the data demonstrate that loss of PRDX6 slows down cell division and alters metabolism and mitochondrial function, so that cell survival depends on glycolysis to lactate for ATP production and on AMPK-independent autophagy to obtain building blocks for biosynthesis. PRDX6 is an important link in the chain of elements connecting redox homeostasis and proliferation.</div></front></TEI><pubmed><MedlineCitation Status="Publisher" Owner="NLM"><PMID Version="1">33035814</PMID><DateRevised><Year>2020</Year><Month>11</Month><Day>03</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">2213-2317</ISSN><JournalIssue CitedMedium="Internet"><Volume>37</Volume><PubDate><Year>2020</Year><Month>Sep</Month><Day>29</Day></PubDate></JournalIssue><Title>Redox biology</Title><ISOAbbreviation>Redox Biol</ISOAbbreviation></Journal><ArticleTitle>Knockout of PRDX6 induces mitochondrial dysfunction and cell cycle arrest at G2/M in HepG2 hepatocarcinoma cells.</ArticleTitle><Pagination><MedlinePgn>101737</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S2213-2317(20)30942-3</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.redox.2020.101737</ELocationID><Abstract><AbstractText>Peroxiredoxin 6 (PRDX6) has been associated with tumor progression and cancer metastasis. Its acting on phospholipid hydroperoxides and its phospholipase-A2 activity are unique among the peroxiredoxin family and add complexity to its action mechanisms. As a first step towards the study of PRDX6 involvement in cancer, we have constructed a human hepatocarcinoma HepG2<sup>PRDX6</sup><sup>-</sup><sup>/-</sup> cell line using the CRISPR/Cas9 technique and have characterized the cellular response to lack of PRDX6. Applying quantitative global and redox proteomics, flow cytometry, in vivo extracellular flow analysis, Western blot and electron microscopy, we have detected diminished respiratory capacity, downregulation of mitochondrial proteins and altered mitochondrial morphology. Autophagic vesicles were abundant while the unfolded protein response (UPR), HIF1A and NRF2 transcription factors were not activated, despite increased levels of p62/SQSTM1 and reactive oxygen species (ROS). Insulin receptor (INSR), 3-phosphoinositide-dependent protein kinase 1 (PDPK1), uptake of glucose and hexokinase-2 (HK2) decreased markedly while nucleotide biosynthesis, lipogenesis and synthesis of long chain polyunsaturated fatty acids (LC-PUFA) increased. 254 Cys-peptides belonging to 202 proteins underwent significant redox changes. PRDX6 knockout had an antiproliferative effect due to cell cycle arrest at G2/M transition, without signs of apoptosis. Loss of PLA2 may affect the levels of specific lipids altering lipid signaling pathways, while loss of peroxidase activity could induce redox changes at critical sensitive cysteine residues in key proteins. Oxidation of specific cysteines in Proliferating Cell Nuclear Antigen (PCNA) could interfere with entry into mitosis. The GSH/Glutaredoxin system was downregulated likely contributing to these redox changes. Altogether the data demonstrate that loss of PRDX6 slows down cell division and alters metabolism and mitochondrial function, so that cell survival depends on glycolysis to lactate for ATP production and on AMPK-independent autophagy to obtain building blocks for biosynthesis. PRDX6 is an important link in the chain of elements connecting redox homeostasis and proliferation.</AbstractText><CopyrightInformation>Copyright © 2020 The Author(s). Published by Elsevier B.V. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>López-Grueso</LastName><ForeName>María José</ForeName><Initials>MJ</Initials><AffiliationInfo><Affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lagal</LastName><ForeName>Daniel José</ForeName><Initials>DJ</Initials><AffiliationInfo><Affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>García-Jiménez</LastName><ForeName>Álvaro Fernando</ForeName><Initials>ÁF</Initials><AffiliationInfo><Affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Tarradas</LastName><ForeName>Rosa María</ForeName><Initials>RM</Initials><AffiliationInfo><Affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Carmona-Hidalgo</LastName><ForeName>Beatriz</ForeName><Initials>B</Initials><AffiliationInfo><Affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Peinado</LastName><ForeName>José</ForeName><Initials>J</Initials><AffiliationInfo><Affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Requejo-Aguilar</LastName><ForeName>Raquel</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba, Spain.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bárcena</LastName><ForeName>José Antonio</ForeName><Initials>JA</Initials><AffiliationInfo><Affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba, Spain. Electronic address: ja.barcena@uco.es.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Padilla</LastName><ForeName>Carmen Alicia</ForeName><Initials>CA</Initials><AffiliationInfo><Affiliation>Dept. of Biochemistry and Molecular Biology, University of Córdoba, Spain; Maimónides Biomedical Research Institute of Córdoba (IMIBIC), Córdoba, Spain.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>09</Month><Day>29</Day></ArticleDate></Article><MedlineJournalInfo><Country>Netherlands</Country><MedlineTA>Redox Biol</MedlineTA><NlmUniqueID>101605639</NlmUniqueID><ISSNLinking>2213-2317</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">CRISPR-Cas9</Keyword><Keyword MajorTopicYN="N">Carbohydrate metabolism</Keyword><Keyword MajorTopicYN="N">Cell cycle</Keyword><Keyword MajorTopicYN="N">Glucose metabolism</Keyword><Keyword MajorTopicYN="N">Lipokines</Keyword><Keyword MajorTopicYN="N">Mitochondria</Keyword><Keyword MajorTopicYN="N">NRF2</Keyword><Keyword MajorTopicYN="N">PCNA</Keyword><Keyword MajorTopicYN="N">Peroxiredoxin 6</Keyword><Keyword MajorTopicYN="N">Proteomics</Keyword><Keyword MajorTopicYN="N">Redox proteome</Keyword></KeywordList></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>06</Month><Day>16</Day></PubMedPubDate><PubMedPubDate PubStatus="revised"><Year>2020</Year><Month>09</Month><Day>21</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>09</Month><Day>22</Day></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>10</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>10</Month><Day>10</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>10</Month><Day>9</Day><Hour>20</Hour><Minute>13</Minute></PubMedPubDate></History><PublicationStatus>aheadofprint</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">33035814</ArticleId><ArticleId IdType="pii">S2213-2317(20)30942-3</ArticleId><ArticleId IdType="doi">10.1016/j.redox.2020.101737</ArticleId><ArticleId IdType="pmc">PMC7554216</ArticleId></ArticleIdList></PubmedData></pubmed><affiliations><list><country><li>Espagne</li></country></list><tree><country name="Espagne"><noRegion><name sortKey="L Pez Grueso, Maria Jose" sort="L Pez Grueso, Maria Jose" uniqKey="L Pez Grueso M" first="María José" last="L Pez-Grueso">María José L Pez-Grueso</name></noRegion><name sortKey="Barcena, Jose Antonio" sort="Barcena, Jose Antonio" uniqKey="Barcena J" first="José Antonio" last="Bárcena">José Antonio Bárcena</name><name sortKey="Carmona Hidalgo, Beatriz" sort="Carmona Hidalgo, Beatriz" uniqKey="Carmona Hidalgo B" first="Beatriz" last="Carmona-Hidalgo">Beatriz Carmona-Hidalgo</name><name sortKey="Garcia Jimenez, Alvaro Fernando" sort="Garcia Jimenez, Alvaro Fernando" uniqKey="Garcia Jimenez A" first="Álvaro Fernando" last="García-Jiménez">Álvaro Fernando García-Jiménez</name><name sortKey="Lagal, Daniel Jose" sort="Lagal, Daniel Jose" uniqKey="Lagal D" first="Daniel José" last="Lagal">Daniel José Lagal</name><name sortKey="Padilla, Carmen Alicia" sort="Padilla, Carmen Alicia" uniqKey="Padilla C" first="Carmen Alicia" last="Padilla">Carmen Alicia Padilla</name><name sortKey="Peinado, Jose" sort="Peinado, Jose" uniqKey="Peinado J" first="José" last="Peinado">José Peinado</name><name sortKey="Requejo Aguilar, Raquel" sort="Requejo Aguilar, Raquel" uniqKey="Requejo Aguilar R" first="Raquel" last="Requejo-Aguilar">Raquel Requejo-Aguilar</name><name sortKey="Tarradas, Rosa Maria" sort="Tarradas, Rosa Maria" uniqKey="Tarradas R" first="Rosa María" last="Tarradas">Rosa María Tarradas</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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