TRIM32 Regulates Skeletal Muscle Stem Cell Differentiation and Is Necessary for Normal Adult Muscle Regeneration
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{"title"=>"TRIM32 regulates skeletal muscle stem cell differentiation and is necessary for normal adult muscle regeneration", "type"=>"journal", "authors"=>[{"first_name"=>"Sarah", "last_name"=>"Nicklas", "scopus_author_id"=>"55267254400"}, {"first_name"=>"Anthony", "last_name"=>"Otto", "scopus_author_id"=>"12780035500"}, {"first_name"=>"Xiaoli", "last_name"=>"Wu", "scopus_author_id"=>"55714928300"}, {"first_name"=>"Pamela", "last_name"=>"Miller", "scopus_author_id"=>"55267909900"}, {"first_name"=>"Sandra", "last_name"=>"Stelzer", "scopus_author_id"=>"35744056300"}, {"first_name"=>"Yefei", "last_name"=>"Wen", "scopus_author_id"=>"36998113900"}, {"first_name"=>"Shihuan", "last_name"=>"Kuang", "scopus_author_id"=>"55680946000"}, {"first_name"=>"Klaus", "last_name"=>"Wrogemann", "scopus_author_id"=>"7005919682"}, {"first_name"=>"Ketan", "last_name"=>"Patel", "scopus_author_id"=>"7402235263"}, {"first_name"=>"Hao", "last_name"=>"Ding", "scopus_author_id"=>"7402286459"}, {"first_name"=>"Jens C.", "last_name"=>"Schwamborn", "scopus_author_id"=>"6603410568"}], "year"=>2012, "source"=>"PLoS ONE", "identifiers"=>{"sgr"=>"84863050417", "doi"=>"10.1371/journal.pone.0030445", "pui"=>"364167994", "pmid"=>"22299041", "scopus"=>"2-s2.0-84863050417", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)"}, "id"=>"a10d8b01-99fc-3424-ac0b-3f248dd7208a", "abstract"=>"Limb girdle muscular dystrophy type 2H (LGMD2H) is an inherited autosomal recessive disease of skeletal muscle caused by a mutation in the TRIM32 gene. Currently its pathogenesis is entirely unclear. Typically the regeneration process of adult skeletal muscle during growth or following injury is controlled by a tissue specific stem cell population termed satellite cells. Given that TRIM32 regulates the fate of mammalian neural progenitor cells through controlling their differentiation, we asked whether TRIM32 could also be essential for the regulation of myogenic stem cells. Here we demonstrate for the first time that TRIM32 is expressed in the skeletal muscle stem cell lineage of adult mice, and that in the absence of TRIM32, myogenic differentiation is disrupted. Moreover, we show that the ubiquitin ligase TRIM32 controls this process through the regulation of c-Myc, a similar mechanism to that previously observed in neural progenitors. Importantly we show that loss of TRIM32 function induces a LGMD2H-like phenotype and strongly affects muscle regeneration in vivo. Our studies implicate that the loss of TRIM32 results in dysfunctional muscle stem cells which could contribute to the development of LGMD2H.", "link"=>"http://www.mendeley.com/research/trim32-regulates-skeletal-muscle-stem-cell-differentiation-necessary-normal-adult-muscle-regeneratio-1", "reader_count"=>26, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>1, "Professor"=>1}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>1, "Librarian"=>1, "Researcher"=>4, "Student > Ph. D. Student"=>10, "Student > Postgraduate"=>1, "Student > Master"=>6, "Other"=>1, "Professor"=>1}, "reader_count_by_subject_area"=>{"Unspecified"=>3, "Biochemistry, Genetics and Molecular Biology"=>3, "Agricultural and Biological Sciences"=>15, "Medicine and Dentistry"=>4, "Pharmacology, Toxicology and Pharmaceutical Science"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>4}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>15}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>3}, "Unspecified"=>{"Unspecified"=>3}, "Pharmacology, Toxicology and Pharmaceutical Science"=>{"Pharmacology, Toxicology and Pharmaceutical Science"=>1}}, "reader_count_by_country"=>{"Brazil"=>1, "Portugal"=>1}, "group_count"=>1}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/687408"], "description"=>"<p>(a) Myoblast C2C12 cells were transfected with the indicated constructs (left grey boxes) and cultivated for three days in 2.5% HS. Immunostainings of the cells labelled with the indicated markers (upper grey boxes) are shown. (b) Diagram showing the fraction of transfected cells that undergo muscular differentiation (Myosin positive). (mean ± std; *P<0.001 compared to EGFP).</p>", "links"=>[], "tags"=>["induce", "muscular"], "article_id"=>357889, "categories"=>["Physiology", "Biological Sciences", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Sarah Nicklas", "Anthony Otto", "Xiaoli Wu", "Pamela Miller", "Sandra Stelzer", "Yefei Wen", "Shihuan Kuang", "Klaus Wrogemann", "Ketan Patel", "Hao Ding", "Jens C. Schwamborn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030445.g004", "stats"=>{"downloads"=>0, "page_views"=>0, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TRIM32_is_necessary_and_sufficient_to_induce_muscular_differentiation_/357889", "title"=>"TRIM32 is necessary and sufficient to induce muscular differentiation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-27 02:11:29"}
  • {"files"=>["https://ndownloader.figshare.com/files/687512"], "description"=>"<p>(a) C2C12 cells were transfected with the indicated constructs (left grey boxes) and cultivated for three days in 2.5% HS. Immunostainings of the cells labelled with the indicated markers (upper grey boxes) are shown. (b) Diagram showing the fraction of transfected cells that undergo muscular differentiation (Myosin positive). (mean ± std; *P<0.001 compared to EGFP).</p>", "links"=>[], "tags"=>["c-myc", "trim32", "induced"], "article_id"=>357986, "categories"=>["Physiology", "Biological Sciences", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Sarah Nicklas", "Anthony Otto", "Xiaoli Wu", "Pamela Miller", "Sandra Stelzer", "Yefei Wen", "Shihuan Kuang", "Klaus Wrogemann", "Ketan Patel", "Hao Ding", "Jens C. Schwamborn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030445.g005", "stats"=>{"downloads"=>4, "page_views"=>9, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Degradation_of_c_Myc_is_critical_for_TRIM32_induced_differentiation_/357986", "title"=>"Degradation of c-Myc is critical for TRIM32 induced differentiation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-27 02:13:06"}
  • {"files"=>["https://ndownloader.figshare.com/files/687096"], "description"=>"<p>(a) and (c) Hematoxylin and Eosin (H&E) staining of regenerating TA muscle from wild type mice 3 days post cardiotoxin (CTX) injection. Arrows in (a) indicate the regions of CTX-induced muscle regeneration. (c) shows enlarged region of the boxed area in (a). (b) and (d) RNA in situ hybridization showing <i>TRIM32</i> expression (blue) in wild type mouse TA muscle 3 days post CTX injection. (d) shows enlarged regions of the boxed area in (b). (e) H&E staining of regenerating TA muscle from wild type mice 7 days post CTX injection. (f) RNA in situ hybridization showing <i>TRIM32</i> expression (blue) in wild type mouse TA muscle 7 days post CTX injection.</p>", "links"=>[], "tags"=>["induced", "regeneration"], "article_id"=>357574, "categories"=>["Physiology", "Biological Sciences", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Sarah Nicklas", "Anthony Otto", "Xiaoli Wu", "Pamela Miller", "Sandra Stelzer", "Yefei Wen", "Shihuan Kuang", "Klaus Wrogemann", "Ketan Patel", "Hao Ding", "Jens C. Schwamborn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030445.g002", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TRIM32_is_induced_during_muscle_regeneration_in_vivo_/357574", "title"=>"TRIM32 is induced during muscle regeneration <i>in vivo</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-27 02:06:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/686907"], "description"=>"<p>(a) Immunostainings of satellite cells on myofibers from wild type mice cultured for the indicated time (left grey boxes) and labelled with the indicated markers (upper grey boxes). The right panels show single nuclei in higher magnification. Note that here the anti-TRIM32 antibody 1137 (see methods) has been used. (b) Diagram showing the fraction of cells at each culture time point that were double-positive for TRIM32/Pax7, TRIM32/MyoD or TRIM32/Myogenin.</p>", "links"=>[], "tags"=>["cells", "regeneration"], "article_id"=>357385, "categories"=>["Physiology", "Biological Sciences", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Sarah Nicklas", "Anthony Otto", "Xiaoli Wu", "Pamela Miller", "Sandra Stelzer", "Yefei Wen", "Shihuan Kuang", "Klaus Wrogemann", "Ketan Patel", "Hao Ding", "Jens C. Schwamborn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030445.g001", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TRIM32_is_expressed_in_satellite_cells_during_regeneration_in_vitro_/357385", "title"=>"TRIM32 is expressed in satellite cells during regeneration <i>in vitro</i>.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-27 02:03:05"}
  • {"files"=>["https://ndownloader.figshare.com/files/687640"], "description"=>"<p>(a) Immunostainings with antibodies against different MHC isoforms shows no changes in TA muscle morphology and fiber composition between one month-old wild type (+/+) and <i>TRIM32</i> deficient mice (−/−). (b–e) Immunostainings of muscle satellite cells in TA muscle sections from one month-old wild type (+/+) and <i>TRIM32−/−</i> (−/−) mice labelled for the indicated markers. Arrows in (d) indicate two satellite cells located beneath the basal lamina and the arrow in (e) indicates one satellite cell located outside the basal lamina.</p>", "links"=>[], "tags"=>["trim32", "causes", "cells"], "article_id"=>358122, "categories"=>["Physiology", "Biological Sciences", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Sarah Nicklas", "Anthony Otto", "Xiaoli Wu", "Pamela Miller", "Sandra Stelzer", "Yefei Wen", "Shihuan Kuang", "Klaus Wrogemann", "Ketan Patel", "Hao Ding", "Jens C. Schwamborn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030445.g006", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Loss_of_TRIM32_function_causes_an_increase_in_muscle_satellite_cells_and_their_mislocalization_/358122", "title"=>"Loss of TRIM32 function causes an increase in muscle satellite cells and their mislocalization.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-27 02:15:22"}
  • {"files"=>["https://ndownloader.figshare.com/files/351177", "https://ndownloader.figshare.com/files/351247", "https://ndownloader.figshare.com/files/351293", "https://ndownloader.figshare.com/files/351333", "https://ndownloader.figshare.com/files/351378", "https://ndownloader.figshare.com/files/351436", "https://ndownloader.figshare.com/files/351487"], "description"=>"<div><p>Limb girdle muscular dystrophy type 2H (LGMD2H) is an inherited autosomal recessive disease of skeletal muscle caused by a mutation in the <em>TRIM32</em> gene. Currently its pathogenesis is entirely unclear. Typically the regeneration process of adult skeletal muscle during growth or following injury is controlled by a tissue specific stem cell population termed satellite cells. Given that TRIM32 regulates the fate of mammalian neural progenitor cells through controlling their differentiation, we asked whether TRIM32 could also be essential for the regulation of myogenic stem cells. Here we demonstrate for the first time that TRIM32 is expressed in the skeletal muscle stem cell lineage of adult mice, and that in the absence of TRIM32, myogenic differentiation is disrupted. Moreover, we show that the ubiquitin ligase TRIM32 controls this process through the regulation of c-Myc, a similar mechanism to that previously observed in neural progenitors. Importantly we show that loss of TRIM32 function induces a LGMD2H-like phenotype and strongly affects muscle regeneration <em>in vivo</em>. Our studies implicate that the loss of TRIM32 results in dysfunctional muscle stem cells which could contribute to the development of LGMD2H.</p> </div>", "links"=>[], "tags"=>["trim32", "regulates", "skeletal", "differentiation", "regeneration"], "article_id"=>129421, "categories"=>["Physiology", "Biological Sciences", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Sarah Nicklas", "Anthony Otto", "Xiaoli Wu", "Pamela Miller", "Sandra Stelzer", "Yefei Wen", "Shihuan Kuang", "Klaus Wrogemann", "Ketan Patel", "Hao Ding", "Jens C. Schwamborn"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0030445.s001", "https://dx.doi.org/10.1371/journal.pone.0030445.s002", "https://dx.doi.org/10.1371/journal.pone.0030445.s003", "https://dx.doi.org/10.1371/journal.pone.0030445.s004", "https://dx.doi.org/10.1371/journal.pone.0030445.s005", "https://dx.doi.org/10.1371/journal.pone.0030445.s006", "https://dx.doi.org/10.1371/journal.pone.0030445.s007"], "stats"=>{"downloads"=>10, "page_views"=>13, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/TRIM32_Regulates_Skeletal_Muscle_Stem_Cell_Differentiation_and_Is_Necessary_for_Normal_Adult_Muscle_Regeneration/129421", "title"=>"TRIM32 Regulates Skeletal Muscle Stem Cell Differentiation and Is Necessary for Normal Adult Muscle Regeneration", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2012-01-27 02:37:01"}
  • {"files"=>["https://ndownloader.figshare.com/files/687275"], "description"=>"<p>(a), (c) and (e) Immunostainings of satellite cells on freshly isolated myofibers from wild type (+/+) and <i>TRIM32−/−</i> (−/−) mice cultured for 24 h (a), 48 h (c) and 72 h (e) and labelled with the indicated markers (upper grey boxes). (b), (d) and (f) Diagrams showing the relative frequency of Pax7<sup>+</sup>/MyoD<sup>−</sup> cells on fibers cultured for 24 h (b), Pax7<sup>+</sup>/Myogenin<sup>−</sup> cells on fibers cultured for 48 h (d) and Pax7<sup>−</sup>/Myogenin<sup>+</sup> cells on fibers cultured for 72 h (f). In all cases cells on myofibers from wild type mice and <i>TRIM32−/−</i> mice are compared. (mean ± std; *P<0.001 compared to wild type).</p>", "links"=>[], "tags"=>["reduced", "progeny"], "article_id"=>357753, "categories"=>["Physiology", "Biological Sciences", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Sarah Nicklas", "Anthony Otto", "Xiaoli Wu", "Pamela Miller", "Sandra Stelzer", "Yefei Wen", "Shihuan Kuang", "Klaus Wrogemann", "Ketan Patel", "Hao Ding", "Jens C. Schwamborn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030445.g003", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Differentiation_is_strongly_reduced_in_satellite_cell_progeny_on_TRIM32_8722_8722_myofibers_/357753", "title"=>"Differentiation is strongly reduced in satellite cell progeny on <i>TRIM32−/−</i> myofibers.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-27 02:09:13"}
  • {"files"=>["https://ndownloader.figshare.com/files/687834"], "description"=>"<p>(a)–(d) H&E staining of transverse cross sections through CTX-injured TA muscles 5 days post injection from wild type (a) and (c) and <i>TRIM32−/−</i> (b) and (d) mice. (c) and (d) show enlarged regions of the boxed areas in (a) and (b), respectively. (e)–(h). H&E staining of transverse cross sections through CTX-injured TA muscles 16 days post injection from wild type (e) and (g) and <i>TRIM32−/−</i> (f) and (h) mice. (g) and (h) show enlarged regions of (e) and (f), respectively. Arrow in (g) indicates centrally nucleated myofiber characteristic of efficient muscle regeneration in wild type TA. In contrast, some regions of injured <i>TRIM32−/−</i> TA display small centrally nucleated myofibers (h, arrowhead), adipocyte-like cells (f, arrow) or fibrosis (h, arrow).</p>", "links"=>[], "tags"=>["mice", "delayed", "impaired", "skeletal"], "article_id"=>358314, "categories"=>["Physiology", "Biological Sciences", "Cell Biology", "Genetics", "Developmental Biology"], "users"=>["Sarah Nicklas", "Anthony Otto", "Xiaoli Wu", "Pamela Miller", "Sandra Stelzer", "Yefei Wen", "Shihuan Kuang", "Klaus Wrogemann", "Ketan Patel", "Hao Ding", "Jens C. Schwamborn"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0030445.g007", "stats"=>{"downloads"=>0, "page_views"=>1, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_TRIM32_8722_8722_mice_show_delayed_and_impaired_skeletal_muscle_regeneration_/358314", "title"=>"<i>TRIM32−/−</i> mice show delayed and impaired skeletal muscle regeneration.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2012-01-27 02:18:34"}

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Relative Metric

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