Smaug/SAMD4A Restores Translational Activity of CUGBP1 and Suppresses CUG-Induced Myopathy
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{"title"=>"Smaug/SAMD4A Restores Translational Activity of CUGBP1 and Suppresses CUG-Induced Myopathy", "type"=>"journal", "authors"=>[{"first_name"=>"Maria", "last_name"=>"de Haro", "scopus_author_id"=>"23484747300"}, {"first_name"=>"Ismael", "last_name"=>"Al-Ramahi", "scopus_author_id"=>"14019027900"}, {"first_name"=>"Karlie R.", "last_name"=>"Jones", "scopus_author_id"=>"55268086200"}, {"first_name"=>"Jerrah K.", "last_name"=>"Holth", "scopus_author_id"=>"55566630700"}, {"first_name"=>"Lubov T.", "last_name"=>"Timchenko", "scopus_author_id"=>"7006204950"}, {"first_name"=>"Juan", "last_name"=>"Botas", "scopus_author_id"=>"7005312089"}], "year"=>2013, "source"=>"PLoS Genetics", "identifiers"=>{"issn"=>"15537390", "scopus"=>"2-s2.0-84876830225", "pui"=>"368819453", "doi"=>"10.1371/journal.pgen.1003445", "isbn"=>"1553-7404 (Electronic)\\r1553-7390 (Linking)", "sgr"=>"84876830225", "pmid"=>"23637619"}, "id"=>"f204a523-eee9-3d32-8d4b-ee9039fe9958", "abstract"=>"We report the identification and characterization of a previously unknown suppressor of myopathy caused by expansion of CUG repeats, the mutation that triggers Myotonic Dystrophy Type 1 (DM1). We screened a collection of genes encoding RNA-binding proteins as candidates to modify DM1 pathogenesis using a well established Drosophila model of the disease. The screen revealed smaug as a powerful modulator of CUG-induced toxicity. Increasing smaug levels prevents muscle wasting and restores muscle function, while reducing its function exacerbates CUG-induced phenotypes. Using human myoblasts, we show physical interactions between human Smaug (SMAUG1/SMAD4A) and CUGBP1. Increased levels of SMAUG1 correct the abnormally high nuclear accumulation of CUGBP1 in myoblasts from DM1 patients. In addition, augmenting SMAUG1 levels leads to a reduction of inactive CUGBP1-eIF2α translational complexes and to a correction of translation of MRG15, a downstream target of CUGBP1. Therefore, Smaug suppresses CUG-mediated muscle wasting at least in part via restoration of translational activity of CUGBP1.", "link"=>"http://www.mendeley.com/research/smaugsamd4a-restores-translational-activity-cugbp1-suppresses-cuginduced-myopathy", "reader_count"=>28, "reader_count_by_academic_status"=>{"Professor > Associate Professor"=>1, "Student > Doctoral Student"=>1, "Researcher"=>3, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>5, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Professor > Associate Professor"=>1, "Student > Doctoral Student"=>1, "Researcher"=>3, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>1, "Student > Master"=>5, "Student > Bachelor"=>5, "Lecturer"=>1, "Lecturer > Senior Lecturer"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>1, "Biochemistry, Genetics and Molecular Biology"=>8, "Agricultural and Biological Sciences"=>15, "Medicine and Dentistry"=>3, "Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>3}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>15}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>8}, "Unspecified"=>{"Unspecified"=>1}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"United States"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1029097"], "description"=>"<p>A–D. Scanning electron microscopy (SEM) images of <i>Drosophila</i> eyes expressing (CUG)480 and different levels of <i>smaug</i>. A. Control GMR-Gal4 eye showing characteristic organization of ommatidia and interommatidial bristles. B. Animals expressing (CUG)480 under the control of GMR-Gal4 eye driver show reduced eye size, and disorganization of ommatidia and bristles. C. Overexpression of <i>smaug</i> ameliorates the (CUG)480-induced phenotypes. Note improved eye size and ommatidial organization relative to B. D. Reduced <i>smaug</i> function enhances (CUG)480-induced toxicity. Eyes of animals expressing (CUG)480 and carrying a heterozygous loss-of-function mutation in <i>smaug</i> show more severe eye size reduction, more ommatidial disorganization and less bristles than eyes of (CUG)480 animals (compare with B). E. Eosin stained transversal paraffin sections of indirect flight muscles (IFM). Expression of (CUG)480 in the muscles causes progressive loss of tissue and vacuolization. (CUG)480 animals of the same age that overexpress <i>smaug</i> show no muscle tissue loss or vacuolization. All E panels show IFMs from 20-day-old animals grown at 25C. F. Chart showing the percentage of control and experimental animals that are able to fly at different ages. Almost 100% of control animals (blue bars) are able to fly at days 5, 10 and 20. Animal expressing (CUG)480 in the IFMs show impaired flying ability (green bars). (CUG)480 animals that also overexpress <i>smaug</i> show rescue of the flying impairment phenotype (orange bars). n = 100. G. Larval muscles from animals expressing (CUG)480. probed with Cy3-labelled 5′-CAG-3′ LNA probe to detect nuclear foci (NF, in red) and stained with anti-Smaug (in green). Note that the Smaug protein does not localize to nuclear foci (NF). Smaug protein is mainly cytoplasmic where it accumulates in granules, and it also delineates the nucleus (arrow). Scale bar: A–D: 100 µm. E: 50 µm. G: 10 µm. Genotypes: A: <i>w</i>; GMR-Gal4/+. B: <i>w</i>; GMR-Gal4/+;<i>UAS-(CUG)480-M5T</i>/+. C: <i>w</i>; GMR-Gal4/+;<i>UAS-(CUG)480-M5T</i>/<i>smg</i>EP3556. D: <i>w</i>; GMR-Gal4/+;<i>UAS-(CUG)480-M5T</i>/<i>smg</i>1. E: Control: <i>w</i>; +; MHC-Gal4/+. (CUG)480: <i>w</i>; <i>UAS-(CUG)480-M5Q</i>, <i>UAS-(CUG)480-M13D</i>/+; MHC-Gal4/+. (CUG)480/<i>smgOE</i>: <i>w</i>; <i>UAS-(CUG)480-M5Q</i>, <i>UAS-(CUG)480-M13D</i>/+; MHC-Gal4/<i>smg</i>EP3556. F: Control: <i>w</i>; +; MHC-Gal4/+. (CUG)480: <i>w</i>; <i>UAS-(CUG)480-M13D</i>/+; MHC-Gal4/+. (CUG)480/smgOE: <i>w</i>; <i>UAS-(CUG)480-M13D</i>/+; MHC-Gal4/<i>smg</i>EP3556. G: <i>w</i>; <i>UAS-(CUG)480-M5Q</i>, <i>UAS-(CUG)480-M13D</i>/+; MHC-Gal4/+.</p>", "links"=>[], "tags"=>["genetics", "Human genetics", "Autosomal dominant", "Genetic screens", "Model organisms", "Animal models", "Drosophila melanogaster", "Molecular cell biology", "overexpression", "suppresses", "expanded", "cug-induced", "toxicity"], "article_id"=>686007, "categories"=>["Biological Sciences"], "users"=>["Maria de Haro", "Ismael Al-Ramahi", "Karlie R. Jones", "Jerrah K. Holth", "Lubov T. Timchenko", "Juan Botas"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003445.g001"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_smaug_overexpression_suppresses_expanded_CUG_induced_toxicity_in_Drosophila_/686007", "title"=>"<i>smaug</i> overexpression suppresses expanded CUG-induced toxicity in <i>Drosophila</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-18 01:40:07"}
  • {"files"=>["https://ndownloader.figshare.com/files/1029100"], "description"=>"<p>A–C. SEM eye images of animals overexpressing CUGBP1 and different levels of <i>smaug</i>. A. SEM eye image showing that expression of CUGBP1 using GMR-Gal4 causes ommatidial disorganization, loss of bristles and decrease in eye size compared to control eyes (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003445#pgen-1003445-g001\" target=\"_blank\">Figure 1A</a>). This phenotype is most prominent in the central dorsal part of the eye (see close-up). B. <i>smaug</i> overexpression (OE) in animals expressing CUGBP1 rescues the ommatidial, bristle and eye size phenotypes. C. A heterozygous loss-of-function mutation in <i>smaug</i> enhances the CUGBP1-induced eye phenotype, particularly in the most affected central dorsal area of the eye (see close-up). D–F. SEM eye images of animals overexpressing MBNL1 and different levels of <i>smaug</i>. D. Expression of MBNL1 in the eye using GMR-Gal4 causes ommatidial disorganization, loss of bristles and reduction of eye size compared to control eyes (<a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003445#pgen-1003445-g001\" target=\"_blank\">Figure 1A</a>). Neither overexpression (E) nor partial loss of function (F) of <i>smaug</i> in animals expressing MBNL1 affect these phenotypes. Scale bar: A–F: 100 µm. Genotypes: A: <i>w</i>; GMR-Gal4/+; <i>UAS-CUGBP1-M2E</i>/+. B: <i>w</i>; GMR-Gal4/+; <i>UAS-CUGBP1-M2E</i>/<i>smg</i>EP3556. C: <i>w</i>; GMR-Gal4/+; <i>UAS-CUGBP1-M2E</i>/<i>smg</i>1. D: <i>w</i>; GMR-Gal4, <i>UAS-MBNL1-M6B</i>/+. E: w; GMR-Gal4, <i>UAS-MBNL1-M6B</i>/+; <i>smg</i>EP3556/+. F: <i>w</i>; GMR-Gal4, <i>UAS-MBNL1-M6B</i>/+; <i>smg</i>1/+.</p>", "links"=>[], "tags"=>["genetics", "Human genetics", "Autosomal dominant", "Genetic screens", "Model organisms", "Animal models", "Drosophila melanogaster", "Molecular cell biology", "interacts", "genetically", "cugbp1"], "article_id"=>686010, "categories"=>["Biological Sciences"], "users"=>["Maria de Haro", "Ismael Al-Ramahi", "Karlie R. Jones", "Jerrah K. Holth", "Lubov T. Timchenko", "Juan Botas"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003445.g002"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Smaug_interacts_genetically_with_CUGBP1_but_not_with_MBNL1_/686010", "title"=>"Smaug interacts genetically with CUGBP1 but not with MBNL1.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-18 01:40:10"}
  • {"files"=>["https://ndownloader.figshare.com/files/1029102"], "description"=>"<p>Immunofluorescense and in situ images of COSM6 cells. A. Expanded CUG repeat-transfected COSM6 cells show accumulation of the transcripts in nuclear foci (detected with a Cy3-labelled 5′-CAG-3′ LNA probe, white), and increased nuclear CUGBP1 signal (arrowhead) (α-CUGBP1, red). B. COSM6 cells co-transfected with CUGs and SMAUG1-ECFP show cytoplasmic signal of SMAUG1 (SMAUG1-ECFP, green) and CUG nuclear foci (CAG probe, white). These cells have decreased CUGBP1 nuclear signal (arrowhead) (α-CUGBP1, red); in addition, CUGBP1 co-localizes with SMAUG1 in cytoplasmic granules (arrow). C. Untransfected (arrowhead) and GFP-transfected (arrow) cells show similar nuclear CUGBP signal (α-CUGBP1, red). White lines in A–B delineate the nuclei. Scale bar: A–C: 10 µm.</p>", "links"=>[], "tags"=>["genetics", "Human genetics", "Autosomal dominant", "Genetic screens", "Model organisms", "Animal models", "Drosophila melanogaster", "Molecular cell biology", "accumulation", "proteins", "co-localize", "cytoplasmic"], "article_id"=>686012, "categories"=>["Biological Sciences"], "users"=>["Maria de Haro", "Ismael Al-Ramahi", "Karlie R. Jones", "Jerrah K. Holth", "Lubov T. Timchenko", "Juan Botas"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003445.g003"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SMAUG1_expression_reduces_nuclear_accumulation_of_CUGBP1_and_both_proteins_co_localize_in_cytoplasmic_granules_/686012", "title"=>"SMAUG1 expression reduces nuclear accumulation of CUGBP1, and both proteins co-localize in cytoplasmic granules.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-18 01:40:12"}
  • {"files"=>["https://ndownloader.figshare.com/files/1029105"], "description"=>"<p>A. Immunofluorescense and in situ images of DM1 myoblasts transfected with GFP. In control DM1 myoblasts transfected with GFP (green) CUGBP1 is predominantly in the nucleus (red); CUG foci are detected in the nuclei with a Cy3-labelled 5′-CAG-3′ LNA probe (CAG probe, white). B–C. Immunofluorescense and in situ images of DM1 myoblasts transfected with SMAUG1-ECFP. SMAUG1 is detected in the cytoplasm (SMAUG1-ECFP, green). Note that nuclear CUGBP1 signal (α-CUGBP1, red) is clearly diminished in DM1 myoblasts transfected with SMAUG1 (B, arrowhead). Longer exposure of CUGBP1 signal shows cytoplasmic CUGBP1 (C) and its co-localization with SMAUG1 in granules (arrows). D. Bar graph representing the intensity of CUGBP1 nuclear signal in DM1 myoblasts transfected with GFP (DM1-GFP, green bar), versus DM1 myoblasts transfected with SMAUG1 (DM1-SMAUG1, blue bar). Data was analyzed with ANOVA followed by Student's t test, p<0.0001. Black dots represent individual observations, red lines are the standard error of the mean. E. Western blot revealing co-immunoprecipitation between CUGBP1 and human SMAUG1 in extracts from SMAUG1-V5-transfected normal and DM1 human myoblasts. Pull down was carried out using anti-CUGBP1 antibody. SMAUG1 was visualized with anti-V5-HRP antibody. White lines in A–C delineate the nuclei. Scale bar: A–C: 10 µm.</p>", "links"=>[], "tags"=>["genetics", "Human genetics", "Autosomal dominant", "Genetic screens", "Model organisms", "Animal models", "Drosophila melanogaster", "Molecular cell biology", "cugbp1", "co-localize", "dm1"], "article_id"=>686015, "categories"=>["Biological Sciences"], "users"=>["Maria de Haro", "Ismael Al-Ramahi", "Karlie R. Jones", "Jerrah K. Holth", "Lubov T. Timchenko", "Juan Botas"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003445.g004"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SMAUG1_and_CUGBP1_co_localize_and_physically_interact_in_DM1_myoblasts_/686015", "title"=>"SMAUG1 and CUGBP1 co-localize and physically interact in DM1 myoblasts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-18 01:40:15"}
  • {"files"=>["https://ndownloader.figshare.com/files/1029107"], "description"=>"<p>A–B. Nuclear localization of CUGBP1 (α-CUGBP1, red) is not altered by expression of SMAUG1 (SMAUG1-ECFP, green) in control unaffected primary human myoblasts. CUGBP1 co-localizes with SMAUG1 cytoplasmic granules in control myoblasts (arrow in B). Scale bar: 10 µm.</p>", "links"=>[], "tags"=>["genetics", "Human genetics", "Autosomal dominant", "Genetic screens", "Model organisms", "Animal models", "Drosophila melanogaster", "Molecular cell biology", "smaug1", "myoblasts", "cugbp1"], "article_id"=>686017, "categories"=>["Biological Sciences"], "users"=>["Maria de Haro", "Ismael Al-Ramahi", "Karlie R. Jones", "Jerrah K. Holth", "Lubov T. Timchenko", "Juan Botas"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003445.g005"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_of_SMAUG1_in_control_human_myoblasts_does_not_affect_CUGBP1_nuclear_localization_/686017", "title"=>"Expression of SMAUG1 in control human myoblasts does not affect CUGBP1 nuclear localization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-18 01:40:17"}
  • {"files"=>["https://ndownloader.figshare.com/files/1029108"], "description"=>"<p>A–B. Protein levels of total CUGBP1 and eIF2α in control and DM1 myoblasts (A) and fibroblasts (B) were detected by Western blotting of cytoplasmic fractions (Western). β-actin serves as a loading control. CUGBP1 levels are compared in untransfected and SMAUG1-transfected normal and DM1 myoblasts. Quantification is based in two experiments in myoblasts and two experiments in fibroblasts. Material immunoprecipitated with CUGBP1 antibodies was probed with antibody to specific inactive pS51-eIF2α (CUGBP1-IP). Note that inactive pS51-eIF2α is not detected after <i>SMAUG1</i> transfection. IgGs, heavy chains of immunoglobulins detected on the same filter. IP was repeated three times in myoblasts and three times in fibroblasts (see <a href=\"http://www.plosgenetics.org/article/info:doi/10.1371/journal.pgen.1003445#pgen.1003445.s007\" target=\"_blank\">Figure S7</a>). C. SMAUG1 recuperates normal levels of MRG15 protein in DM1 myoblasts and fibroblasts. Nuclear proteins of normal and DM1 myoblasts were examined by Western blotting with antibodies to MRG15. The filter was re-probed with antibodies to β-actin. The level of MRG15 in SMAUG1-transfected myoblasts are shown compared to untransfected normal and DM1 myoblasts from two experiments. Quantifications were performed using ImageJ Gel Analyzer software.</p>", "links"=>[], "tags"=>["genetics", "Human genetics", "Autosomal dominant", "Genetic screens", "Model organisms", "Animal models", "Drosophila melanogaster", "Molecular cell biology", "inactive", "translational", "complexes", "recuperates", "mrg15", "dm1", "myoblasts"], "article_id"=>686018, "categories"=>["Biological Sciences"], "users"=>["Maria de Haro", "Ismael Al-Ramahi", "Karlie R. Jones", "Jerrah K. Holth", "Lubov T. Timchenko", "Juan Botas"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003445.g006"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_SMAUG1_reduces_inactive_CUGBP1_pS51_eIF2_945_translational_complexes_and_recuperates_normal_levels_of_MRG15_protein_in_DM1_myoblasts_and_fibroblasts_/686018", "title"=>"SMAUG1 reduces inactive CUGBP1/pS51-eIF2α translational complexes and recuperates normal levels of MRG15 protein in DM1 myoblasts and fibroblasts.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-04-18 01:40:18"}
  • {"files"=>["https://ndownloader.figshare.com/files/1029112", "https://ndownloader.figshare.com/files/1029113", "https://ndownloader.figshare.com/files/1029114", "https://ndownloader.figshare.com/files/1029115", "https://ndownloader.figshare.com/files/1029116", "https://ndownloader.figshare.com/files/1029117", "https://ndownloader.figshare.com/files/1029118"], "description"=>"<div><p>We report the identification and characterization of a previously unknown suppressor of myopathy caused by expansion of CUG repeats, the mutation that triggers Myotonic Dystrophy Type 1 (DM1). We screened a collection of genes encoding RNA–binding proteins as candidates to modify DM1 pathogenesis using a well established <i>Drosophila</i> model of the disease. The screen revealed <i>smaug</i> as a powerful modulator of CUG-induced toxicity. Increasing <i>smaug</i> levels prevents muscle wasting and restores muscle function, while reducing its function exacerbates CUG-induced phenotypes. Using human myoblasts, we show physical interactions between human Smaug (SMAUG1/SMAD4A) and CUGBP1. Increased levels of SMAUG1 correct the abnormally high nuclear accumulation of CUGBP1 in myoblasts from DM1 patients. In addition, augmenting SMAUG1 levels leads to a reduction of inactive CUGBP1-eIF2α translational complexes and to a correction of translation of MRG15, a downstream target of CUGBP1. Therefore, Smaug suppresses CUG-mediated muscle wasting at least in part via restoration of translational activity of CUGBP1.</p></div>", "links"=>[], "tags"=>["genetics", "Human genetics", "Autosomal dominant", "Genetic screens", "Model organisms", "Animal models", "Drosophila melanogaster", "Molecular cell biology", "restores", "translational", "cugbp1", "suppresses", "cug-induced"], "article_id"=>686021, "categories"=>["Biological Sciences"], "users"=>["Maria de Haro", "Ismael Al-Ramahi", "Karlie R. Jones", "Jerrah K. Holth", "Lubov T. Timchenko", "Juan Botas"], "doi"=>["https://dx.doi.org/10.1371/journal.pgen.1003445.s001", "https://dx.doi.org/10.1371/journal.pgen.1003445.s002", "https://dx.doi.org/10.1371/journal.pgen.1003445.s003", "https://dx.doi.org/10.1371/journal.pgen.1003445.s004", "https://dx.doi.org/10.1371/journal.pgen.1003445.s005", "https://dx.doi.org/10.1371/journal.pgen.1003445.s006", "https://dx.doi.org/10.1371/journal.pgen.1003445.s007"], "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Smaug_SAMD4A_Restores_Translational_Activity_of_CUGBP1_and_Suppresses_CUG_Induced_Myopathy_/686021", "title"=>"Smaug/SAMD4A Restores Translational Activity of CUGBP1 and Suppresses CUG-Induced Myopathy", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-04-18 01:40:21"}

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Relative Metric

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