Notch Signalling Is Required for the Formation of Structurally Stable Muscle Fibres in Zebrafish
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{"title"=>"Notch Signalling Is Required for the Formation of Structurally Stable Muscle Fibres in Zebrafish", "type"=>"journal", "authors"=>[{"first_name"=>"Susana", "last_name"=>"Pascoal", "scopus_author_id"=>"8532016700"}, {"first_name"=>"Joana", "last_name"=>"Esteves de Lima", "scopus_author_id"=>"55777532700"}, {"first_name"=>"Jonathan D.", "last_name"=>"Leslie", "scopus_author_id"=>"7101696227"}, {"first_name"=>"Simon M.", "last_name"=>"Hughes", "scopus_author_id"=>"7402137440"}, {"first_name"=>"Leonor", "last_name"=>"Saúde", "scopus_author_id"=>"56050483200"}], "year"=>2013, "source"=>"PLoS ONE", "identifiers"=>{"scopus"=>"2-s2.0-84879549227", "sgr"=>"84879549227", "issn"=>"19326203", "isbn"=>"1932-6203 (Electronic)\\r1932-6203 (Linking)", "pmid"=>"23840804", "doi"=>"10.1371/journal.pone.0068021", "pui"=>"369209187"}, "id"=>"e23ec378-1d4f-3d15-80e6-3719b4b8adbc", "abstract"=>"BACKGROUND: Accurate regulation of Notch signalling is central for developmental processes in a variety of tissues, but its function in pectoral fin development in zebrafish is still unknown.\\n\\nMETHODOLOGY/PRINCIPAL FINDINGS: Here we show that core elements necessary for a functional Notch pathway are expressed in developing pectoral fins in or near prospective muscle territories. Blocking Notch signalling at different levels of the pathway consistently leads to the formation of thin, wavy, fragmented and mechanically weak muscles fibres and loss of stress fibres in endoskeletal disc cells in pectoral fins. Although the structural muscle genes encoding Desmin and Vinculin are normally transcribed in Notch-disrupted pectoral fins, their proteins levels are severely reduced, suggesting that weak mechanical forces produced by the muscle fibres are unable to stabilize/localize these proteins. Moreover, in Notch signalling disrupted pectoral fins there is a decrease in the number of Pax7-positive cells indicative of a defect in myogenesis.\\n\\nCONCLUSIONS/SIGNIFICANCE: We propose that by controlling the differentiation of myogenic progenitor cells, Notch signalling might secure the formation of structurally stable muscle fibres in the zebrafish pectoral fin.", "link"=>"http://www.mendeley.com/research/notch-signalling-required-formation-structurally-stable-muscle-fibres-zebrafish", "reader_count"=>34, "reader_count_by_academic_status"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>10, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>1, "Student > Master"=>7, "Student > Bachelor"=>2}, "reader_count_by_user_role"=>{"Unspecified"=>1, "Professor > Associate Professor"=>2, "Librarian"=>1, "Researcher"=>10, "Student > Doctoral Student"=>1, "Student > Ph. D. Student"=>9, "Student > Postgraduate"=>1, "Student > Master"=>7, "Student > Bachelor"=>2}, "reader_count_by_subject_area"=>{"Engineering"=>2, "Unspecified"=>2, "Biochemistry, Genetics and Molecular Biology"=>4, "Mathematics"=>1, "Agricultural and Biological Sciences"=>21, "Veterinary Science and Veterinary Medicine"=>2, "Social Sciences"=>1, "Immunology and Microbiology"=>1}, "reader_count_by_subdiscipline"=>{"Engineering"=>{"Engineering"=>2}, "Social Sciences"=>{"Social Sciences"=>1}, "Immunology and Microbiology"=>{"Immunology and Microbiology"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>21}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>4}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>2}, "Veterinary Science and Veterinary Medicine"=>{"Veterinary Science and Veterinary Medicine"=>2}}, "reader_count_by_country"=>{"Argentina"=>1, "Brazil"=>1, "United Kingdom"=>1, "Portugal"=>1}, "group_count"=>0}

Scopus | Further Information

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Figshare

  • {"files"=>["https://ndownloader.figshare.com/files/1106318"], "description"=>"<p>Transmission electronic microscopy was performed in 5 dpf pectoral fins of siblings (A) and <i>mib</i><sup>ta52b</sup> mutants (B) to analyse the ultrastructure of skeletal muscle fibres. The myofibrils with clear aligned sarcomeres are formed in the sibling embryo (A), while disintegrating myofibrils with poorly aligned sarcomeres are found in <i>mib</i><sup>ta52b</sup> mutants (B). Immunostaining performed in pectoral fins at 5 dpf using Desmin, Vinculin, phalloidin and DAPI to label the Z-discs of the sarcomeres, the zone where the skeletal muscle fibres insert distally, filamentous actin and the cell nuclei, respectively (C–P) demonstrate that Desmin (n = 10) (D) and Vinculin (n = 12) (F) are downregulated in <i>mib</i><sup>ta52b</sup> mutants when compared with their siblings (n = 10) (C, E). The same is observed in DAPT-treated embryos at 48 hpf and fixed at 5 dpf (n = 9) (H), when compared with the DMSO-treated embryos (n = 10) (G). In embryos treated with blebbistatin, Desmin (n = 9) and Vinculin (n = 12) are also downregulated (J, L) when compared with the DMSO-treated embryos (n = 12) (I, K). In blebbistatin-treated embryos, the endoskeletal disc cells present high levels of actin at the periphery and the skeletal muscle fibres are wavy with gaps between them (n = 15) (N). A down-regulation of Desmin and Vinculin is also observed in MS222-treated embryos (n = 14) (P) when compared with the control embryos (n = 13) (O).</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "developmental biology", "Molecular development", "signaling", "morphogenesis", "Limb development", "Cell differentiation", "Cell fate determination", "embryology", "Model organisms", "Animal models", "zebrafish", "muscles", "fibres", "produced", "notch", "signalling"], "article_id"=>735629, "categories"=>["Biological Sciences"], "users"=>["Susana Pascoal", "Joana Esteves de Lima", "Jonathan D. Leslie", "Simon M. Hughes", "Leonor Saúde"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068021.g005", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Mechanical_weak_muscles_fibres_are_produced_when_Notch_signalling_is_perturbed_/735629", "title"=>"Mechanical weak muscles fibres are produced when Notch signalling is perturbed.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:12:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106314"], "description"=>"<p>Immunostaining of 5 dpf pectoral fins (A–G”) with DAPI and phalloidin to label nuclei (blue) and filamentous actin (green), respectively. Stress fibres in the endoskeletal disc cells and intact skeletal muscle fibres are formed in the pectoral fins of siblings (n = 20) (A–A”) and in DMSO-treated embryos (n = 17) (F-F”). In the pectoral fins were Notch signalling was disrupted like in <i>mib</i><sup>ta52b</sup> (n = 22) (B–B”) and <i>mib</i><sup>m178</sup> (n = 10) (C–C”) mutants, <i>jagged2</i> (n = 11) (D–D”) and <i>Su(H)</i>1+2 (n = 10) (E–E”) morphants and in DAPT-treated embryos (n = 16) (G–G”) the endoskeletal disc cells present high levels of actin at the periphery and the skeletal muscle fibres are wavy with gaps between them.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "developmental biology", "Molecular development", "signaling", "morphogenesis", "Limb development", "Cell differentiation", "Cell fate determination", "embryology", "Model organisms", "Animal models", "zebrafish", "signalling", "skeletal", "fibres"], "article_id"=>735625, "categories"=>["Biological Sciences"], "users"=>["Susana Pascoal", "Joana Esteves de Lima", "Jonathan D. Leslie", "Simon M. Hughes", "Leonor Saúde"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068021.g004", "stats"=>{"downloads"=>0, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Notch_signalling_is_crucial_for_skeletal_muscle_integrity_and_stress_fibres_formation_/735625", "title"=>"Notch signalling is crucial for skeletal muscle integrity and stress fibres formation.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:12:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106309"], "description"=>"<p>(A–F) Live pictures of 5 dpf larvae. (A’) A pectoral fin from a sibling embryo showing the cartilaginous endoskeletal disc with individualized cells surrounded by thin matrix deposits, the fin fold and the chleitrum (n = 17) (E, E’). A similar pectoral fin was found in a DMSO-treated embryo (n = 9). Pectoral fins of Notch signalling disrupted embryos such as <i>mib</i><sup>ta52b</sup> (n = 18) (B, B’), <i>jagged2</i> (n = 10) (C, C’) and <i>Su(H)1+2</i> (n = 12) (D, D’) morphants and DAPT-treated embryos (n = 10) (F, F’) showing disorganized endoskeletal disc cells. cl, chleitrum; ed, endoskeletal disc; ff, fin fold.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "developmental biology", "Molecular development", "signaling", "morphogenesis", "Limb development", "Cell differentiation", "Cell fate determination", "embryology", "Model organisms", "Animal models", "zebrafish", "pectoral", "fins", "formed", "notch", "signalling", "disrupted"], "article_id"=>735623, "categories"=>["Biological Sciences"], "users"=>["Susana Pascoal", "Joana Esteves de Lima", "Jonathan D. Leslie", "Simon M. Hughes", "Leonor Saúde"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068021.g002", "stats"=>{"downloads"=>0, "page_views"=>12, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Abnormal_pectoral_fins_are_formed_in_Notch_signalling_disrupted_larvae_/735623", "title"=>"Abnormal pectoral fins are formed in Notch signalling disrupted larvae.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:12:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106312"], "description"=>"<p>Whole-mount in situ hybridization of 68 hpf siblings (n = 15) (A, A’), (n = 12) (C, C’), (n = 14) (E, E’) and <i>mib<sup>ta52b</sup></i> mutants (n = 12) (B, B’), (n = 15) (D, D’), (n = 11) (F, F’) using <i>sox9a</i> and <i>sox9b</i> as cartilage markers and <i>myod</i> as a muscle marker, showing a slight upregulation of these genes in <i>mib<sup>ta52b</sup></i> mutant pectoral fin. (A–F) Whole larvae. (A’–F’) Detached pectoral fins with distal to the right. Double fluorescent in situ hybridization on sections using <i>sox9b</i> (green) and <i>myod</i> (red), counterstained with DAPI to label the nuclei (blue) shows no signs of cell mixing in a sibling (n = 7) (G) and a <i>mib<sup>ta52b</sup></i> mutant pectoral fins (n = 9) (H). An upregulation of these genes is observed in <i>mib<sup>ta52b</sup></i> mutant pectoral fins when compared with the sibling.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "developmental biology", "Molecular development", "signaling", "morphogenesis", "Limb development", "Cell differentiation", "Cell fate determination", "embryology", "Model organisms", "Animal models", "zebrafish", "masses", "specified"], "article_id"=>735624, "categories"=>["Biological Sciences"], "users"=>["Susana Pascoal", "Joana Esteves de Lima", "Jonathan D. Leslie", "Simon M. Hughes", "Leonor Saúde"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068021.g003", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Cartilage_and_muscle_masses_are_specified_in_mib_ta52b_mutants_/735624", "title"=>"Cartilage and muscle masses are specified in <i>mib</i><sup>ta52b</sup> mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:12:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106306"], "description"=>"<p>Whole-mount in situ hybridization of 48 hpf embryos shows strong expression of <i>jagged2</i> (n = 20) (A), <i>notch1a</i> (n = 22) (B), <i>notch2</i> (n = 22) (C), <i>notch3</i> (n = 20) (D), <i>her6</i> (n = 25) (E), <i>her7</i> (n = 23) (F), <i>her13.2</i> (n = 23) (G), <i>mib1</i> (n = 22) (H) and <i>mib2</i> (n = 25) (I) in the pectoral fins. At this time point it is possible to detect expression of <i>jagged2</i> (A’, A”) and <i>notch3</i> (D’, D”) lining the base of the apical ectodermal fold and in the myogenic mesenchyme, <i>notch1a</i> (B’, B”), <i>her6</i> (L’, L”), <i>her13.2</i> (N’, N”), <i>mib1</i> (H’, H”) and <i>mib2</i> (I’, I”) in the myogenic mesenchyme and <i>notch2</i> (J’, J”) and <i>her7</i> (M’, M”) in the entire fin. (A’–I’) Detached pectoral fins with distal to the top. (A”-I”) Transversal sections at the level of pectoral fins. AEF, apical ectodermal fold; dmm, dorsal myogenic mesenchyme; vmm, ventral myogenic mesenchyme; cc, chondrogenic condensation.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "developmental biology", "Molecular development", "signaling", "morphogenesis", "Limb development", "Cell differentiation", "Cell fate determination", "embryology", "Model organisms", "Animal models", "zebrafish", "notch", "signalling", "pathway", "genes", "pectoral", "fin"], "article_id"=>735622, "categories"=>["Biological Sciences"], "users"=>["Susana Pascoal", "Joana Esteves de Lima", "Jonathan D. Leslie", "Simon M. Hughes", "Leonor Saúde"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068021.g001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Expression_pattern_of_Notch_signalling_pathway_genes_during_pectoral_fin_development_/735622", "title"=>"Expression pattern of Notch signalling pathway genes during pectoral fin development.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:12:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106325", "https://ndownloader.figshare.com/files/1106326"], "description"=>"<div><p>Background</p><p>Accurate regulation of Notch signalling is central for developmental processes in a variety of tissues, but its function in pectoral fin development in zebrafish is still unknown.</p><p>Methodology/Principal Findings</p><p>Here we show that core elements necessary for a functional Notch pathway are expressed in developing pectoral fins in or near prospective muscle territories. Blocking Notch signalling at different levels of the pathway consistently leads to the formation of thin, wavy, fragmented and mechanically weak muscles fibres and loss of stress fibres in endoskeletal disc cells in pectoral fins. Although the structural muscle genes encoding Desmin and Vinculin are normally transcribed in Notch-disrupted pectoral fins, their proteins levels are severely reduced, suggesting that weak mechanical forces produced by the muscle fibres are unable to stabilize/localize these proteins. Moreover, in Notch signalling disrupted pectoral fins there is a decrease in the number of Pax7-positive cells indicative of a defect in myogenesis.</p><p>Conclusions/Significance</p><p>We propose that by controlling the differentiation of myogenic progenitor cells, Notch signalling might secure the formation of structurally stable muscle fibres in the zebrafish pectoral fin.</p></div>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "developmental biology", "Molecular development", "signaling", "morphogenesis", "Limb development", "Cell differentiation", "Cell fate determination", "embryology", "Model organisms", "Animal models", "zebrafish", "signalling", "structurally", "fibres"], "article_id"=>735636, "categories"=>["Biological Sciences"], "users"=>["Susana Pascoal", "Joana Esteves de Lima", "Jonathan D. Leslie", "Simon M. Hughes", "Leonor Saúde"], "doi"=>["https://dx.doi.org/10.1371/journal.pone.0068021.s001", "https://dx.doi.org/10.1371/journal.pone.0068021.s002"], "stats"=>{"downloads"=>0, "page_views"=>11, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Notch_Signalling_Is_Required_for_the_Formation_of_Structurally_Stable_Muscle_Fibres_in_Zebrafish_/735636", "title"=>"Notch Signalling Is Required for the Formation of Structurally Stable Muscle Fibres in Zebrafish", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2013-06-28 04:12:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106321"], "description"=>"<p>(A) Number of Pax7-positive cells in siblings and <i>mib</i><sup>ta52b</sup> mutants at time points 2 dpf (sibling n = 6, <i>mib</i><sup>ta52b</sup> n = 7, t-test p = 0.004), 3 dpf (sibling n = 13, <i>mib</i><sup>ta52b</sup> n = 10, t-test p = 0.0002), 4 dpf sibling n = 7, <i>mib</i><sup>ta52b</sup> n = 14, t-test p = 0.0019) and 5 dpf (sibling n = 14, <i>mib<sup>ta52b</sup></i> n = 15, t-test p = 0.003). Error bars = SD. 5 dpf pectoral fins immunostained for Pax7 and DAPI to label muscle progenitor cells and nuclei, respectively, in (B) siblings and (C) <i>mib</i><sup>ta52b</sup> mutants.</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "developmental biology", "Molecular development", "signaling", "morphogenesis", "Limb development", "Cell differentiation", "Cell fate determination", "embryology", "Model organisms", "Animal models", "zebrafish", "progenitor", "cells", "depleted", "mutant", "pectoral"], "article_id"=>735632, "categories"=>["Biological Sciences"], "users"=>["Susana Pascoal", "Joana Esteves de Lima", "Jonathan D. Leslie", "Simon M. Hughes", "Leonor Saúde"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068021.g007", "stats"=>{"downloads"=>0, "page_views"=>10, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Pax7_muscle_progenitor_cells_are_depleted_in_mib_ta52b_mutant_pectoral_fins_/735632", "title"=>"Pax7 muscle progenitor cells are depleted in <i>mib</i><sup>ta52b</sup> mutant pectoral fins.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:12:34"}
  • {"files"=>["https://ndownloader.figshare.com/files/1106319"], "description"=>"<p>Whole-mount in situ hybridization using <i>desmin</i>, <i>vcla</i> and <i>vclb</i> as mRNA probes. At 48 hpf, <i>desmin</i> is expressed at similar levels in the myogenic mesenchyme of the pectoral fins of siblings (n = 18) (A) and <i>mib</i><sup>ta52b</sup> mutants (n = 20) (B). At 5 dpf, the expression of <i>desmin</i> becomes stronger in <i>mib</i><sup>ta52b</sup> mutants (n = 19) (D) when compared with the sibling (n = 16) (C). Blebbistatin-treated embryos (n = 12) (F) show a similar level of <i>desmin</i> expression as control DMSO-treated (n = 10) (E). <i>vcla</i> is expressed strongly in the somites and has a faint expression in the sibling pectoral fins (n = 15) (G), the same expression pattern can be observed in the <i>mib</i><sup>ta52b</sup> mutant (n = 18) (H). <i>vclb</i> is expressed in the myogenic mesenchyme at 48 hpf in both siblings (n = 18) (I), (n = 5) (J) and <i>mib</i><sup>ta52b</sup> mutants (n = 19) (K), (n = 5) (L). At 5 dpf, the expression of <i>vclb</i> is poorly detected in the sibling embryos (n = 15) (M) and is still detected in <i>mib</i><sup>ta52b</sup> mutants (n = 16) (N). Transversal sections at the level of the pectoral fin of 48 hpf embryos are shown (J, L). Blebbistatin-treated embryos (n = 10) (P) show a similar level of <i>vclb</i> expression as control DMSO-treated (n = 12) (O).</p>", "links"=>[], "tags"=>["Anatomy and physiology", "Musculoskeletal system", "developmental biology", "Molecular development", "signaling", "morphogenesis", "Limb development", "Cell differentiation", "Cell fate determination", "embryology", "Model organisms", "Animal models", "zebrafish", "transcriptionally", "downregulated"], "article_id"=>735630, "categories"=>["Biological Sciences"], "users"=>["Susana Pascoal", "Joana Esteves de Lima", "Jonathan D. Leslie", "Simon M. Hughes", "Leonor Saúde"], "doi"=>"https://dx.doi.org/10.1371/journal.pone.0068021.g006", "stats"=>{"downloads"=>2, "page_views"=>19, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_desmin_and_vinculin_are_not_transcriptionally_downregulated_in_mib_ta52b_mutants_/735630", "title"=>"<i>desmin</i> and <i>vinculin</i> are not transcriptionally downregulated in <i>mib</i><sup>ta52b</sup> mutants.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2013-06-28 04:12:34"}

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Relative Metric

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