miR-218 Inhibits Mitochondrial Clearance by Targeting PRKN E3 Ubiquitin Ligase
Identifieur interne : 000002 ( Pmc/Checkpoint ); précédent : 000001; suivant : 000003miR-218 Inhibits Mitochondrial Clearance by Targeting PRKN E3 Ubiquitin Ligase
Auteurs : Anthea Di Rita [Italie] ; Teresa Maiorino ; Krenare Bruqi [Italie] ; Floriana Volpicelli [Italie] ; Gian Carlo Bellenchi [Italie] ; Flavie StrappazzonSource :
- International Journal of Molecular Sciences [ 1422-0067 ] ; 2020.
Abstract
The selective elimination of dysfunctional mitochondria through mitophagy is crucial for preserving mitochondrial quality and cellular homeostasis. The most described mitophagy pathway is regulated by a positive ubiquitylation feedback loop in which the PINK1 (PTEN induced kinase 1) kinase phosphorylates both ubiquitin and the E3 ubiquitin ligase PRKN (Parkin RBR E3 ubiquitin ligase), also known as PARKIN. This event recruits PRKN to the mitochondria, thus amplifying ubiquitylation signal. Here we report that miR-218 targets PRKN and negatively regulates PINK1/PRKN-mediated mitophagy. Overexpression of miR-218 reduces PRKN mRNA levels, thus also reducing protein content and deregulating the E3 ubiquitin ligase action. In fact, following miR-218 overexpression, mitochondria result less ubiquitylated and the autophagy machinery fails to proceed with correct mitochondrial clearance. Since mitophagy defects are associated with various human diseases, these results qualify miR-218 as a promising therapeutic target for human diseases.
Url:
DOI: 10.3390/ijms21010355
PubMed: 31948106
PubMed Central: 6981953
Affiliations:
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sort="Maiorino, Teresa" uniqKey="Maiorino T" first="Teresa" last="Maiorino">Teresa Maiorino</name><affiliation><nlm:aff id="af1-ijms-21-00355">IRCCS Fondazione Santa Lucia, 00143 Rome, Italy;<email>antheadirita@gmail.com</email> (A.D.R.);<email>maiorino.teresa@gmail.com</email> (T.M.);<email>krenare.bruqi@gmail.com</email> (K.B.);<email>bellenchi@igb.cnr.it</email> (G.C.B.)</nlm:aff></affiliation></author><author><name sortKey="Bruqi, Krenare" sort="Bruqi, Krenare" uniqKey="Bruqi K" first="Krenare" last="Bruqi">Krenare Bruqi</name><affiliation><nlm:aff id="af1-ijms-21-00355">IRCCS Fondazione Santa Lucia, 00143 Rome, Italy;<email>antheadirita@gmail.com</email> (A.D.R.);<email>maiorino.teresa@gmail.com</email> (T.M.);<email>krenare.bruqi@gmail.com</email> (K.B.);<email>bellenchi@igb.cnr.it</email> (G.C.B.)</nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-ijms-21-00355">University of Rome Tor Vergata, 00133 Rome, Italy</nlm:aff><country 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Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>University of Rome Tor Vergata, 00133 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Maiorino, Teresa" sort="Maiorino, Teresa" uniqKey="Maiorino T" first="Teresa" last="Maiorino">Teresa Maiorino</name><affiliation><nlm:aff id="af1-ijms-21-00355">IRCCS Fondazione Santa Lucia, 00143 Rome, Italy;<email>antheadirita@gmail.com</email> (A.D.R.);<email>maiorino.teresa@gmail.com</email> (T.M.);<email>krenare.bruqi@gmail.com</email> (K.B.);<email>bellenchi@igb.cnr.it</email> (G.C.B.)</nlm:aff></affiliation></author><author><name sortKey="Bruqi, Krenare" sort="Bruqi, Krenare" uniqKey="Bruqi K" first="Krenare" last="Bruqi">Krenare Bruqi</name><affiliation><nlm:aff id="af1-ijms-21-00355">IRCCS Fondazione Santa Lucia, 00143 Rome, Italy;<email>antheadirita@gmail.com</email> (A.D.R.);<email>maiorino.teresa@gmail.com</email> (T.M.);<email>krenare.bruqi@gmail.com</email> (K.B.);<email>bellenchi@igb.cnr.it</email> (G.C.B.)</nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af2-ijms-21-00355">University of Rome Tor Vergata, 00133 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>University of Rome Tor Vergata, 00133 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Volpicelli, Floriana" sort="Volpicelli, Floriana" uniqKey="Volpicelli F" first="Floriana" last="Volpicelli">Floriana Volpicelli</name><affiliation><nlm:aff id="af3-ijms-21-00355">Institute of Genetics and Biophysics “Adriano Buzzati Traverso”, CNR, 80131 Naples, Italy;<email>floriana.volpicelli@unina.it</email></nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af4-ijms-21-00355">Department of Pharmacy, University of Naples Federico II, 80131 Naples, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Pharmacy, University of Naples Federico II, 80131 Naples</wicri:regionArea><wicri:noRegion>80131 Naples</wicri:noRegion></affiliation></author><author><name sortKey="Bellenchi, Gian Carlo" sort="Bellenchi, Gian Carlo" uniqKey="Bellenchi G" first="Gian Carlo" last="Bellenchi">Gian Carlo Bellenchi</name><affiliation><nlm:aff id="af1-ijms-21-00355">IRCCS Fondazione Santa Lucia, 00143 Rome, Italy;<email>antheadirita@gmail.com</email> (A.D.R.);<email>maiorino.teresa@gmail.com</email> (T.M.);<email>krenare.bruqi@gmail.com</email> (K.B.);<email>bellenchi@igb.cnr.it</email> (G.C.B.)</nlm:aff></affiliation><affiliation><nlm:aff id="af3-ijms-21-00355">Institute of Genetics and Biophysics “Adriano Buzzati Traverso”, CNR, 80131 Naples, Italy;<email>floriana.volpicelli@unina.it</email></nlm:aff></affiliation><affiliation wicri:level="1"><nlm:aff id="af5-ijms-21-00355">Department of Systems Medicine, University of Rome Tor Vergata, 00133 Rome, Italy</nlm:aff><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Systems Medicine, University of Rome Tor Vergata, 00133 Rome</wicri:regionArea><placeName><settlement type="city">Rome</settlement><region nuts="2">Latium</region></placeName></affiliation></author><author><name sortKey="Strappazzon, Flavie" sort="Strappazzon, Flavie" uniqKey="Strappazzon F" first="Flavie" last="Strappazzon">Flavie Strappazzon</name><affiliation><nlm:aff id="af1-ijms-21-00355">IRCCS Fondazione Santa Lucia, 00143 Rome, Italy;<email>antheadirita@gmail.com</email> (A.D.R.);<email>maiorino.teresa@gmail.com</email> (T.M.);<email>krenare.bruqi@gmail.com</email> (K.B.);<email>bellenchi@igb.cnr.it</email> (G.C.B.)</nlm:aff></affiliation></author></analytic><series><title level="j">International Journal of Molecular Sciences</title><idno type="eISSN">1422-0067</idno><imprint><date when="2020">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The selective elimination of dysfunctional mitochondria through mitophagy is crucial for preserving mitochondrial quality and cellular homeostasis. The most described mitophagy pathway is regulated by a positive ubiquitylation feedback loop in which the PINK1 (PTEN induced kinase 1) kinase phosphorylates both ubiquitin and the E3 ubiquitin ligase PRKN (Parkin RBR E3 ubiquitin ligase), also known as PARKIN. This event recruits PRKN to the mitochondria, thus amplifying ubiquitylation signal. Here we report that miR-218 targets PRKN and negatively regulates PINK1/PRKN-mediated mitophagy. Overexpression of miR-218 reduces PRKN mRNA levels, thus also reducing protein content and deregulating the E3 ubiquitin ligase action. In fact, following miR-218 overexpression, mitochondria result less ubiquitylated and the autophagy machinery fails to proceed with correct mitochondrial clearance. Since mitophagy defects are associated with various human diseases, these results qualify miR-218 as a promising therapeutic target for human diseases.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Cecconi, F" uniqKey="Cecconi F">F. Cecconi</name></author><author><name sortKey="Levine, B" uniqKey="Levine B">B. Levine</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lemasters, J J" uniqKey="Lemasters J">J.J. Lemasters</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tatsuta, T" uniqKey="Tatsuta T">T. Tatsuta</name></author><author><name sortKey="Langer, T" uniqKey="Langer T">T. Langer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Wang, D D" uniqKey="Wang D">D.D. Wang</name></author><author><name sortKey="Jin, M F" uniqKey="Jin M">M.F. Jin</name></author><author><name sortKey="Zhao, D J" uniqKey="Zhao D">D.J. 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<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">31948106</article-id><article-id pub-id-type="pmc">6981953</article-id><article-id pub-id-type="doi">10.3390/ijms21010355</article-id><article-id pub-id-type="publisher-id">ijms-21-00355</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>miR-218 Inhibits Mitochondrial Clearance by Targeting PRKN E3 Ubiquitin Ligase</article-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-6266-5054</contrib-id><name><surname>Di Rita</surname><given-names>Anthea</given-names></name><xref ref-type="aff" rid="af1-ijms-21-00355">1</xref><xref ref-type="aff" rid="af2-ijms-21-00355">2</xref></contrib><contrib contrib-type="author"><name><surname>Maiorino</surname><given-names>Teresa</given-names></name><xref ref-type="aff" rid="af1-ijms-21-00355">1</xref></contrib><contrib contrib-type="author"><name><surname>Bruqi</surname><given-names>Krenare</given-names></name><xref ref-type="aff" rid="af1-ijms-21-00355">1</xref><xref ref-type="aff" rid="af2-ijms-21-00355">2</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-0618-5504</contrib-id><name><surname>Volpicelli</surname><given-names>Floriana</given-names></name><xref ref-type="aff" rid="af3-ijms-21-00355">3</xref><xref ref-type="aff" rid="af4-ijms-21-00355">4</xref></contrib><contrib contrib-type="author"><name><surname>Bellenchi</surname><given-names>Gian Carlo</given-names></name><xref ref-type="aff" rid="af1-ijms-21-00355">1</xref><xref ref-type="aff" rid="af3-ijms-21-00355">3</xref><xref ref-type="aff" rid="af5-ijms-21-00355">5</xref></contrib><contrib contrib-type="author"><name><surname>Strappazzon</surname><given-names>Flavie</given-names></name><xref ref-type="aff" rid="af1-ijms-21-00355">1</xref><xref rid="c1-ijms-21-00355" ref-type="corresp">*</xref></contrib></contrib-group><aff id="af1-ijms-21-00355"><label>1</label>IRCCS Fondazione Santa Lucia, 00143 Rome, Italy;<email>antheadirita@gmail.com</email> (A.D.R.);<email>maiorino.teresa@gmail.com</email> (T.M.);<email>krenare.bruqi@gmail.com</email> (K.B.);<email>bellenchi@igb.cnr.it</email> (G.C.B.)</aff><aff id="af2-ijms-21-00355"><label>2</label>University of Rome Tor Vergata, 00133 Rome, Italy</aff><aff id="af3-ijms-21-00355"><label>3</label>Institute of Genetics and Biophysics “Adriano Buzzati Traverso”, CNR, 80131 Naples, Italy;<email>floriana.volpicelli@unina.it</email></aff><aff id="af4-ijms-21-00355"><label>4</label>Department of Pharmacy, University of Naples Federico II, 80131 Naples, Italy</aff><aff id="af5-ijms-21-00355"><label>5</label>Department of Systems Medicine, University of Rome Tor Vergata, 00133 Rome, Italy</aff><author-notes><corresp id="c1-ijms-21-00355"><label>*</label>Correspondence: <email>f.strappazzon@hsantalucia.it</email>; Tel.: +39-06501703093</corresp></author-notes><pub-date pub-type="epub"><day>05</day><month>1</month><year>2020</year></pub-date><pub-date pub-type="collection"><month>1</month><year>2020</year></pub-date><volume>21</volume><issue>1</issue><elocation-id>355</elocation-id><history><date date-type="received"><day>02</day><month>12</month><year>2019</year></date><date date-type="accepted"><day>03</day><month>1</month><year>2020</year></date></history><permissions><copyright-statement>© 2020 by the authors.</copyright-statement><copyright-year>2020</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 selective elimination of dysfunctional mitochondria through mitophagy is crucial for preserving mitochondrial quality and cellular homeostasis. The most described mitophagy pathway is regulated by a positive ubiquitylation feedback loop in which the PINK1 (PTEN induced kinase 1) kinase phosphorylates both ubiquitin and the E3 ubiquitin ligase PRKN (Parkin RBR E3 ubiquitin ligase), also known as PARKIN. This event recruits PRKN to the mitochondria, thus amplifying ubiquitylation signal. Here we report that miR-218 targets PRKN and negatively regulates PINK1/PRKN-mediated mitophagy. Overexpression of miR-218 reduces PRKN mRNA levels, thus also reducing protein content and deregulating the E3 ubiquitin ligase action. In fact, following miR-218 overexpression, mitochondria result less ubiquitylated and the autophagy machinery fails to proceed with correct mitochondrial clearance. Since mitophagy defects are associated with various human diseases, these results qualify miR-218 as a promising therapeutic target for human diseases.</p></abstract><kwd-group><kwd>microRNA</kwd><kwd>mitochondria</kwd><kwd>miR-218</kwd><kwd>PARKIN/PRKN</kwd><kwd>mitophagy</kwd></kwd-group></article-meta></front><floats-group><fig id="ijms-21-00355-f001" orientation="portrait" position="float"><label>Figure 1</label><caption><p>(<bold>a</bold>) Scheme of the 3’UTR (Untranslated region) of PRKN (Parkin RBR E3 ubiquitin ligase). The location of the two predicted binding sites for miR-218 are indicated in red. The region cloned in the pMiR Report miRNA expression vector is shown below the 3′UTR. The restriction enzymes used are indicated as well. (<bold>b</bold>) Luciferase assay. pMiR-Reports containing a portion of the PRKN 3’UTR (pMiR-3’UTR) or the empty pMiR vector (pMiR) were co-transfected in presence or absence of miR-218. All luciferase data have been normalized to the Renilla (RL-SV40) activity. The graph reports the Luciferase/renilla ratio. (<bold>c</bold>) Representative images of HEK293 cells transfected with GFP (Green Fluorescence Protein) or GFP-miR-218 vectors (left part) that were then analyzed by quantitative PCR (qPCR) in order to analyze the mRNA of PRKN (right part). Scale bar 100μm. (<bold>d</bold>) The graph shows the relative expression of PRKN, normalized on B2M as loading control. (<bold>e</bold>) Protein lysates of GFP or GFP-miR-218 transfected HEK293 cells were subjected to western blot analysis against PRKN antibody. (<bold>f</bold>) The graph reports the PRKN/VCL ratio. VCL/Vinculin is used as loading control. All data are representative of experimental triplicate (± s.e.m.). Statistical analysis was performed using Student t-test with Welch’s correction. * <italic>p</italic> < 0.05; ** <italic>p</italic> < 0.01; *** <italic>p</italic> < 0.001 M<sub>r</sub>(K) = relative molecular mass expressed in Kilo Dalton.</p></caption><graphic xlink:href="ijms-21-00355-g001"></graphic></fig><fig id="ijms-21-00355-f002" orientation="portrait" position="float"><label>Figure 2</label><caption><p>(<bold>a</bold>) HEK293 cells transfected with GFP or GFP-miR-218 vectors and then treated with O/A (Oligomycin and Antimycin A 2.5 μM, 0.8 μM, 8 h) were immunoblotted for the indicated antibodies. (<bold>b</bold>,<bold>c</bold>) The graphs show the SOD2 (superoxide dismutase 2) and TOMM20 (translocase of outer mitochondria membrane 20) protein level normalized on the VCL (Vinculin) loading control. (<bold>d</bold>,<bold>e</bold>) Representative immunofluorescence image and related graph in which GFP or GFP-miR-218 overexpressing HEK293 cells were immunostained with an anti-TOMM20 to detect mitochondria (red). Magnifications (3X) of the areas localized in the white frames are illustrated for each immunofluorescence. Scale bar, 10 μm. All data represent the mean of experimental triplicate (±s.e.m.). Statistical analysis was performed using One-Way ANOVA with Sidak’s correction. * <italic>p</italic> < 0.05; ** <italic>p</italic> < 0.01; *** <italic>p</italic> < 0.001. Mr(K) = relative molecular mass expressed in Kilo Dalton.</p></caption><graphic xlink:href="ijms-21-00355-g002"></graphic></fig><fig id="ijms-21-00355-f003" orientation="portrait" position="float"><label>Figure 3</label><caption><p>(<bold>a</bold>) HEK293 cells overexpressing GFP or GFP-miR-218 vectors were treated with O/A for 2 h and subjected to mitochondria purification. (<bold>b</bold>) The graph shows the mitochondrial PRKN normalized on the mitochondrial loading control. (<bold>c</bold>) Representative image of HEK293 cells transfected with GFP or GFP-miR-218 constructs and treated with O/A for 2 h in order to analyze total ubiquitin amount in mitochondria. (<bold>d</bold>) The graph shows total Ub (Ubiquitin) normalized on the mitochondrial protein HSP60 (Heat Shock Protein 60). All data represent the mean of three experiments (±s.e.m.). * <italic>p</italic> < 0.05. Statistical analysis was performed using Student t-test with Welch’s correction. Mr(K) = relative molecular mass expressed in Kilo Dalton.</p></caption><graphic xlink:href="ijms-21-00355-g003"></graphic></fig><fig id="ijms-21-00355-f004" orientation="portrait" position="float"><label>Figure 4</label><caption><p>(<bold>a</bold>,<bold>b</bold>) Representative immunofluorescence image and related graph of HEK293 cells transfected with GFP or GFP-miR-218 vectors were treated with O/A for 5 h and immunostained with an anti-MAP1LC3A antibody (red) and an anti-TOMM20 (cyan) to detect mitochondria. Scale bar, 7 μm. The right panels report the magnifications (4X) of the images that are in the white dotted frames. Data represent the mean of three different samples (±s.e.m.) and are representative of experimental triplicate. * <italic>p</italic> < 0.05, n.s. (not significant). Statistical analysis was performed using One-Way ANOVA with Sidak’s correction. (<bold>c</bold>) Representative image of HEK293 cells transfected as in (<bold>a</bold>) and treated with O/A for 8 h in combination or not with the autophagosome-lysosome fusion inhibitor chloroquine (CQ), were immunoblotted for the indicated antibodies.</p></caption><graphic xlink:href="ijms-21-00355-g004"></graphic></fig></floats-group></pmc><affiliations><list><country><li>Italie</li></country><region><li>Latium</li></region><settlement><li>Rome</li></settlement></list><tree><noCountry><name sortKey="Maiorino, Teresa" sort="Maiorino, Teresa" uniqKey="Maiorino T" first="Teresa" last="Maiorino">Teresa Maiorino</name><name sortKey="Strappazzon, Flavie" sort="Strappazzon, Flavie" uniqKey="Strappazzon F" first="Flavie" last="Strappazzon">Flavie Strappazzon</name></noCountry><country name="Italie"><region name="Latium"><name sortKey="Di Rita, Anthea" sort="Di Rita, Anthea" uniqKey="Di Rita A" first="Anthea" last="Di Rita">Anthea Di Rita</name></region><name sortKey="Bellenchi, Gian Carlo" sort="Bellenchi, Gian Carlo" uniqKey="Bellenchi G" first="Gian Carlo" last="Bellenchi">Gian Carlo Bellenchi</name><name sortKey="Bruqi, Krenare" sort="Bruqi, Krenare" uniqKey="Bruqi K" first="Krenare" last="Bruqi">Krenare Bruqi</name><name sortKey="Volpicelli, Floriana" sort="Volpicelli, Floriana" uniqKey="Volpicelli F" first="Floriana" last="Volpicelli">Floriana Volpicelli</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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