MIR376A Is a Regulator of Starvation-Induced Autophagy
Publication Date
December 16, 2013
Journal
PLOS ONE
Authors
Gozde Korkmaz, Kumsal Ayse Tekirdag, Deniz Gulfem Ozturk, Ali Kosar, et al
Volume
8
Issue
12
Pages
e82556
DOI
https://dx.plos.org/10.1371/journal.pone.0082556
Publisher URL
http://journals.plos.org/plosone/article?id=10.1371%2Fjournal.pone.0082556
PubMed
http://www.ncbi.nlm.nih.gov/pubmed/24358205
PubMed Central
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3864973
Europe PMC
http://europepmc.org/abstract/MED/24358205
Web of Science
000328735700081
Scopus
84892752232
Mendeley
http://www.mendeley.com/research/mir376a-regulator-starvationinduced-autophagy
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Mendeley | Further Information

{"title"=>"MIR376A is a regulator of starvation-induced autophagy", "type"=>"journal", "authors"=>[{"first_name"=>"Gozde", "last_name"=>"Korkmaz", "scopus_author_id"=>"55015217900"}, {"first_name"=>"Kumsal", "last_name"=>"Ayse Tekirdag", "scopus_author_id"=>"56010709000"}, {"first_name"=>"Deniz", "last_name"=>"Gulfem Ozturk", "scopus_author_id"=>"56009018800"}, {"first_name"=>"Ali", "last_name"=>"Kosar", "scopus_author_id"=>"36941876500"}, {"first_name"=>"Osman", "last_name"=>"Ugur Sezerman", "scopus_author_id"=>"36125855600"}, {"first_name"=>"Devrim", "last_name"=>"Gozuacik", "scopus_author_id"=>"6507315780"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84892752232", "doi"=>"10.1371/journal.pone.0082556", "pui"=>"372169962", "pmid"=>"24358205", "scopus"=>"2-s2.0-84892752232", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"6146b48f-5032-37b8-9db1-5d690f4fc13c", "abstract"=>"BACKGROUND: Autophagy is a vesicular trafficking process responsible for the degradation of long-lived, misfolded or abnormal proteins, as well as damaged or surplus organelles. Abnormalities of the autophagic activity may result in the accumulation of protein aggregates, organelle dysfunction, and autophagy disorders were associated with various diseases. Hence, mechanisms of autophagy regulation are under exploration.\\n\\nMETHODS: Over-expression of hsa-miR-376a1 (shortly MIR376A) was performed to evaluate its effects on autophagy. Autophagy-related targets of the miRNA were predicted using Microcosm Targets and MIRanda bioinformatics tools and experimentally validated. Endogenous miRNA was blocked using antagomirs and the effects on target expression and autophagy were analyzed. Luciferase tests were performed to confirm that 3' UTR sequences in target genes were functional. Differential expression of MIR376A and the related MIR376B was compared using TaqMan quantitative PCR.\\n\\nRESULTS: Here, we demonstrated that, a microRNA (miRNA) from the DLK1/GTL2 gene cluster, MIR376A, played an important role in autophagy regulation. We showed that, amino acid and serum starvation-induced autophagy was blocked by MIR376A overexpression in MCF-7 and Huh7 cells. MIR376A shared the same seed sequence and had overlapping targets with MIR376B, and similarly blocked the expression of key autophagy proteins ATG4C and BECN1 (Beclin 1). Indeed, 3' UTR sequences in the mRNA of these autophagy proteins were responsive to MIR376A in luciferase assays. Antagomir tests showed that, endogenous MIR376A was participating to the control of ATG4C and BECN1 transcript and protein levels. Moreover, blockage of endogenous MIR376A accelerated starvation-induced autophagic activity. Interestingly, MIR376A and MIR376B levels were increased with different kinetics in response to starvation stress and tissue-specific level differences were also observed, pointing out to an overlapping but miRNA-specific biological role.\\n\\nCONCLUSIONS: Our findings underline the importance of miRNAs encoded by the DLK1/GTL2 gene cluster in stress-response control mechanisms, and introduce MIR376A as a new regulator of autophagy.", "link"=>"http://www.mendeley.com/research/mir376a-regulator-starvationinduced-autophagy", "reader_count"=>28, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Researcher"=>9, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>4, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Researcher"=>9, "Student > Ph. D. Student"=>8, "Student > Postgraduate"=>1, "Student > Master"=>3, "Other"=>1, "Student > Bachelor"=>4, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>4, "Agricultural and Biological Sciences"=>17, "Medicine and Dentistry"=>2, "Neuroscience"=>1, "Computer Science"=>2}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Neuroscience"=>{"Neuroscience"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>17}, "Computer Science"=>{"Computer Science"=>2}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Unspecified"=>{"Unspecified"=>2}}, "reader_count_by_country"=>{"France"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1316904"], "description"=>"<p>(A) Individual miRNA genes were indicated. Sizes of spacer sequences between miRNA genes were marked as nucleotides (nt). (B) Comparison of mature miRNA sequences with identical “seed sequences” (bold, underlined). Identical nucleotides were indicated by asterix (*). ClustalW tool was used for the analysis. (C) ClustalW comparison of the stem-loop sequences of <i>MIR376A</i> and <i>MIR376B</i>. Seed sequences were marked as bold and underlined.</p>", "links"=>[], "tags"=>["mirnas"], "article_id"=>879325, "categories"=>["Biological Sciences"], "users"=>["Gozde Korkmaz", "Kumsal Ayse Tekirdag", "Deniz Gulfem Ozturk", "Ali Kosar", "Osman Ugur Sezerman", "Devrim Gozuacik"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0082556.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MIR376_family_miRNAs_in_the_DLKI_GTL2_gene_cluster_/879325", "title"=>"<i>MIR376</i> family miRNAs in the <i>DLKI/GTL2</i> gene cluster.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-16 03:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1316905"], "description"=>"<p>(A) MCF-7 cells were co-transfected with either <i>MIR-CNT</i> (control plasmid) or <i>MIR376A</i> and GFP-LC3 plasmid, and GFP-LC3 dot formation was analyzed. White arrows indicate clusters of the GFP-LC3 dots in cells. (B) Quantification of the experiments in A. <i>MIR376A</i> overexpression, but not <i>MIR-CNT</i> expression, blocked starvation (STV)-induced autophagy (mean ± S.D. of independent experiments, n = 4, ***p<0,01). NON STV, non-starved (C) Overexpression of <i>MIR376A</i> resulted in a decrease in the autophagic activity of MCF-7 cells. Starvation-induced conversion of LC3-I to LC3-II in MCF-7 cells was analyzed. Tests were performed in the presence or absence of E64d (10 µg/ml) and Pepstatin A (10 µg/ml) (E+P). LC3-II/LC3-I densitometric ratios were marked. ACTB was used as a loading control. (D) <i>MIR376A</i> blocked starvation induced SQSTM1 degradation in MCF-7 cells. ACTB was used as a loading control. SQSTM1/ACTIN densitometric ratios were marked.</p>", "links"=>[], "tags"=>["overexpression"], "article_id"=>879326, "categories"=>["Biological Sciences"], "users"=>["Gozde Korkmaz", "Kumsal Ayse Tekirdag", "Deniz Gulfem Ozturk", "Ali Kosar", "Osman Ugur Sezerman", "Devrim Gozuacik"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0082556.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_MIR376A_overexpression_on_autophagy_/879326", "title"=>"Effect of <i>MIR376A</i> overexpression on autophagy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-16 03:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1316906"], "description"=>"<p>(A) <i>MIR376A</i> blocked GFP-LC3 dot formation under starvation condition. (B) Quantitative analysis of experiments in A (mean ± S.D. of independent experiments, n = 3, ***p<0,01). (C) Overexpression of <i>MIR376A</i> resulted in decreased autophagic flux in Huh-7 cells. Starvation-induced conversion of LC3-I to LC3-II was analyzed. Tests were performed in the presence or absence of E64d (10 µg/ml) and Pepstatin A (10 µg/ml) (E+P). LC3-II/LC3-I densitometric ratios were marked. ACTB was used as a loading control.</p>", "links"=>[], "tags"=>["overexpression", "blocked", "autophagy", "huh-7"], "article_id"=>879327, "categories"=>["Biological Sciences"], "users"=>["Gozde Korkmaz", "Kumsal Ayse Tekirdag", "Deniz Gulfem Ozturk", "Ali Kosar", "Osman Ugur Sezerman", "Devrim Gozuacik"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0082556.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MIR376A_overexpression_blocked_autophagy_in_Huh_7_cells_/879327", "title"=>"<i>MIR376A</i> overexpression blocked autophagy in Huh-7 cells.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-16 03:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1316908"], "description"=>"<p>(A and B) <i>MIR376A</i> mature miRNA sequence and <i>MIR376A</i> binding target sequences in the 3' UTR of <i>ATG4C</i> (A) and <i>BECN1</i>(B) mRNAs were depicted. <i>MIR376A</i> seed sequence was shown in bold letters and and complemetary sequences were indicated. (C and D) qPCR analysis of <i>ATG4C</i> and <i>BECN1</i> mRNA expression in control miRNA (<i>MIR-CONT</i>) or <i>MIR376A</i> overexpressing cells under non-starved (NON STV) or starved (STV) condition (mean ± S.D. of independent experiments, n = 3, *p<0,05). (E and F) Immunoblots showing ATG4C and BECN1 protein levels following control miRNA (<i>MIR-CONT</i>) or <i>MIR376A</i> overexpression. ACTB was used as a loading control. ATG4C/ACTB or BECN1/ACTB densitometric ratios were marked.</p>", "links"=>[], "tags"=>["becn1", "targets"], "article_id"=>879329, "categories"=>["Biological Sciences"], "users"=>["Gozde Korkmaz", "Kumsal Ayse Tekirdag", "Deniz Gulfem Ozturk", "Ali Kosar", "Osman Ugur Sezerman", "Devrim Gozuacik"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0082556.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_ATG4C_and_BECN1_were_targets_of_MIR376A_/879329", "title"=>"ATG4C and BECN1 were targets of <i>MIR376A</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-16 03:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1316909"], "description"=>"<p>(A and B) qPCR analysis of <i>ATG4C</i> and <i>BECN1</i> mRNA levels in MCF-7 cells transfected with control antagomirs (CNT-Ant) or antagomir-376a (Ant-376a) (mean ± S.D. of independent experiments, n = 3, **p<0,03 for <i>ATG4C</i>, and n = 3, **p<0,03 for <i>BECN1</i>). Results were expressed as fold changes against <i>GAPDH</i> mRNA levels. (C and D) ATG4C and BECN1 protein levels were increased following antagomir-376a (Ant-376a) transfection. ATG4C/ACTB or BECN1/ACTB densitometric ratios were marked.</p>", "links"=>[], "tags"=>["antagomirs"], "article_id"=>879330, "categories"=>["Biological Sciences"], "users"=>["Gozde Korkmaz", "Kumsal Ayse Tekirdag", "Deniz Gulfem Ozturk", "Ali Kosar", "Osman Ugur Sezerman", "Devrim Gozuacik"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0082556.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effect_of_antagomirs_on_MIR376A_target_expression_/879330", "title"=>"Effect of antagomirs on <i>MIR376A</i> target expression.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-16 03:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1316910"], "description"=>"<p>Schemes showing <i>ATG4C</i> (A) and (B) <i>BECN1</i> MRE (top), or their mutated versions (bottom) placed in the 3' UTR of the luciferase gene in the pGL3 vector. Mutated residues were <i>italicized</i>. <i>MIR376A</i> seed target sequence was underlined. (C and D) Normalized luciferase activity measuremets of lysates from 293T cells that were co-transfected with either <i>MIR-CNT</i> or <i>MIR376A</i> plasmids together with the wild-type or mutant luciferase constructs (mean ± S.D. of independent experiments, n = 3 for <i>ATG4C</i> tests, *p<0,05 and n = 5 for <i>BECN1</i> tests, ***p<0,01).</p>", "links"=>[], "tags"=>["controlled", "mirna-response", "elements", "mrna"], "article_id"=>879331, "categories"=>["Biological Sciences"], "users"=>["Gozde Korkmaz", "Kumsal Ayse Tekirdag", "Deniz Gulfem Ozturk", "Ali Kosar", "Osman Ugur Sezerman", "Devrim Gozuacik"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0082556.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MIR376A_controlled_miRNA_response_elements_MREs_in_ATG4C_and_BECN1_mRNA_3_UTRs_/879331", "title"=>"<i>MIR376A</i> controlled miRNA-response elements (MREs) in <i>ATG4C</i> and <i>BECN1</i> mRNA 3′ UTRs.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-16 03:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1316911"], "description"=>"<p>(A) Blockage of endogenous <i>MIR376A</i> by Ant-376a, but not CNT-Ant further stimulated starvation (STV)-activated LC3-I to LC3-II conversion in MCF-7 cells. ACTB was used as a loading control. LC3-II/LC3-I densitometric ratios were marked. (B) Ant-376a, but not CNT-Ant resulted in further activation of SQSTM1 protein degradation following starvation in MCF-7 cells. SQSTM1/ACTB ratios were marked.</p>", "links"=>[], "tags"=>["limits", "starvation-induced"], "article_id"=>879332, "categories"=>["Biological Sciences"], "users"=>["Gozde Korkmaz", "Kumsal Ayse Tekirdag", "Deniz Gulfem Ozturk", "Ali Kosar", "Osman Ugur Sezerman", "Devrim Gozuacik"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0082556.g007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Endogenous_MIR376A_limits_starvation_induced_autophagy_/879332", "title"=>"Endogenous <i>MIR376A</i> limits starvation-induced autophagy.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-16 03:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1316913"], "description"=>"<p>(A and B) TaqMan quantitative PCR (qPCR) analysis of endogenous <i>MIR376A</i> (A) and <i>MIR376B</i> (B) levels under control (CNT, no starvation) or starvation (STV, 1 to 8 hours) conditions. TaqMan qPCR data was normalized using <i>U6 small nuclear 1 (RNU6-1)</i> (U6) mRNA levels (mean ± S.D. of independent experiments, n = 5 for both A and B, ***p<0,01).</p>", "links"=>[], "tags"=>["starvation"], "article_id"=>879334, "categories"=>["Biological Sciences"], "users"=>["Gozde Korkmaz", "Kumsal Ayse Tekirdag", "Deniz Gulfem Ozturk", "Ali Kosar", "Osman Ugur Sezerman", "Devrim Gozuacik"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0082556.g008"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MIR376A_and_MIR376B_level_changes_in_response_to_starvation_stress_/879334", "title"=>"<i>MIR376A</i> and <i>MIR376B</i> level changes in response to starvation stress.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-16 03:49:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1316914"], "description"=>"<div><p>Background</p><p>Autophagy is a vesicular trafficking process responsible for the degradation of long-lived, misfolded or abnormal proteins, as well as damaged or surplus organelles. Abnormalities of the autophagic activity may result in the accumulation of protein aggregates, organelle dysfunction, and autophagy disorders were associated with various diseases. Hence, mechanisms of autophagy regulation are under exploration.</p><p>Methods</p><p>Over-expression of hsa-miR-376a1 (shortly <i>MIR376A</i>) was performed to evaluate its effects on autophagy. Autophagy-related targets of the miRNA were predicted using Microcosm Targets and MIRanda bioinformatics tools and experimentally validated. Endogenous miRNA was blocked using antagomirs and the effects on target expression and autophagy were analyzed. Luciferase tests were performed to confirm that 3′ UTR sequences in target genes were functional. Differential expression of <i>MIR376A</i> and the related <i>MIR376B</i> was compared using TaqMan quantitative PCR.</p><p>Results</p><p>Here, we demonstrated that, a microRNA (miRNA) from the <i>DLK1/GTL2</i> gene cluster, <i>MIR376A</i>, played an important role in autophagy regulation. We showed that, amino acid and serum starvation-induced autophagy was blocked by <i>MIR376A</i> overexpression in MCF-7 and Huh7 cells. <i>MIR376A</i> shared the same seed sequence and had overlapping targets with <i>MIR376B</i>, and similarly blocked the expression of key autophagy proteins ATG4C and BECN1 (Beclin 1). Indeed, 3′ UTR sequences in the mRNA of these autophagy proteins were responsive to <i>MIR376A</i> in luciferase assays. Antagomir tests showed that, endogenous <i>MIR376A</i> was participating to the control of <i>ATG4C</i> and <i>BECN1</i> transcript and protein levels. Moreover, blockage of endogenous <i>MIR376A</i> accelerated starvation-induced autophagic activity. Interestingly, <i>MIR376A</i> and <i>MIR376B</i> levels were increased with different kinetics in response to starvation stress and tissue-specific level differences were also observed, pointing out to an overlapping but miRNA-specific biological role.</p><p>Conclusions</p><p>Our findings underline the importance of miRNAs encoded by the <i>DLK1/GTL2</i> gene cluster in stress-response control mechanisms, and introduce <i>MIR376A</i> as a new regulator of autophagy.</p></div>", "links"=>[], "tags"=>["starvation-induced", "autophagy"], "article_id"=>879335, "categories"=>["Biological Sciences"], "users"=>["Gozde Korkmaz", "Kumsal Ayse Tekirdag", "Deniz Gulfem Ozturk", "Ali Kosar", "Osman Ugur Sezerman", "Devrim Gozuacik"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0082556"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_MIR376A_Is_a_Regulator_of_Starvation_Induced_Autophagy/879335", "title"=>"<i>MIR376A</i> Is a Regulator of Starvation-Induced Autophagy", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-12-16 03:49:18"}

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Relative Metric

{"start_date"=>"2013-01-01T00:00:00Z", "end_date"=>"2013-12-31T00:00:00Z", "subject_areas"=>[{"subject_area"=>"/Biology and life sciences/Biochemistry", "average_usage"=>[266, 468, 593, 703, 804, 903, 993, 1084, 1171, 1256, 1339, 1422, 1492]}, {"subject_area"=>"/Biology and life sciences/Cell biology", "average_usage"=>[272, 472, 600, 713, 815, 911, 1004, 1094, 1185, 1273, 1358, 1441]}, {"subject_area"=>"/Biology and life sciences/Molecular biology", "average_usage"=>[272, 466, 589, 702, 806, 903, 995, 1086, 1176, 1258, 1347, 1422, 1493]}]}
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