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      The zebrafish HGF receptor met controls migration of myogenic progenitor cells in appendicular development

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          Abstract

          The hepatocyte growth factor receptor C-met plays an important role in cellular migration, which is crucial for many developmental processes as well as for cancer cell metastasis. C-met has been linked to the development of mammalian appendicular muscle, which are derived from migrating muscle progenitor cells (MMPs) from within the somite. Mammalian limbs are homologous to the teleost pectoral and pelvic fins. In this study we used Crispr/Cas9 to mutate the zebrafish met gene and found that the MMP derived musculature of the paired appendages was severely affected. The mutation resulted in a reduced muscle fibre number, in particular in the pectoral abductor, and in a disturbed pectoral fin function. Other MMP derived muscles, such as the sternohyoid muscle and posterior hypaxial muscle were also affected in met mutants. This indicates that the role of met in MMP function and appendicular myogenesis is conserved within vertebrates.

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          Most cited references44

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          Gene regulatory networks and transcriptional mechanisms that control myogenesis.

          We discuss the upstream regulators of myogenesis that lead to the activation of myogenic determination genes and subsequent differentiation, focusing on the mouse model. Key upstream genes, such as Pax3 and Pax7, Six1 and Six4, or Pitx2, participate in gene regulatory networks at different sites of skeletal muscle formation. MicroRNAs also intervene, with emerging evidence for the role of other noncoding RNAs. Myogenic determination and subsequent differentiation depend on members of the MyoD family. We discuss new insights into mechanisms underlying the transcriptional activity of these factors. Copyright © 2014 Elsevier Inc. All rights reserved.
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            Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud.

            Limb muscles develop from cells that migrate from the somites. The signal that induces migration of myogenic precursor cells to the limb emanates from the mesenchyme of the limb bud. Here we report that the c-met-encoded receptor tyrosine kinase is essential for migration of myogenic precursor cells into the limb anlage and for migration into diaphragm and tip of tongue. In c-met homozygous mutant (-/-) mouse embryos, the limb bud and diaphragm are not colonized by myogenic precursor cells and, as a consequence, skeletal muscles of the limb and diaphragm do not form. In contrast, development of the axial skeletal muscles proceeds in the absence of c-met signalling. The specific ligand of the c-met protein, the motility and growth factor scatter factor/hepatocyte growth factor, is expressed in limb mesenchyme and can thus provide the signal for migration which is received by c-met. We have therefore identified a paracrine signalling system that regulates migration of myogenic precursor cells.
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              Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos.

              Mesoderm formation is critical for the establishment of the animal body plan and in Drosophila requires the snail gene. This report concerns the cloning and expression pattern of the structurally similar gene snail1 from zebrafish. In situ hybridization shows that the quantity of snail1 RNA increases at the margin of the blastoderm in cells that involute during gastrulation. As gastrulation begins, snail1 RNA disappears from the dorsal axial mesoderm and becomes restricted to the paraxial mesoderm and the tail bud. snail1 RNA increases in cells that define the posterior border of each somite and then disappears when somitic cells differentiate. Later in development, expression appears in cephalic neural crest derivatives. Many snail1-expressing cells were missing from mutant spadetail embryos and the quantity of snail1 RNA was greatly reduced in mutant no tail embryos. The work presented here suggests that snail1 is involved in morphogenetic events during gastrulation, somitogenesis and development of the cephalic neural crest, and that no tail may act as a positive regulator of snail1.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: VisualizationRole: Writing – review & editing
                Role: Formal analysisRole: Investigation
                Role: Resources
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                9 July 2019
                2019
                : 14
                : 7
                : e0219259
                Affiliations
                [1 ] Department of Integrative Medical Biology, Umeå University, Umeå, Sweden
                [2 ] Umeå Centre for Molecular Medicine, Umeå University, Umeå, Sweden
                Stanford University School of Medicine, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-0885-6586
                http://orcid.org/0000-0001-7799-3985
                http://orcid.org/0000-0003-3730-1790
                Article
                PONE-D-19-15964
                10.1371/journal.pone.0219259
                6615617
                31287821
                88eb1c89-6c88-4350-bcf3-6ea71fb1e9b7
                © 2019 Nord et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 29 January 2019
                : 20 June 2019
                Page count
                Figures: 6, Tables: 0, Pages: 14
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100002794, Cancerfonden;
                Award ID: 170710
                Award Recipient :
                This work was supported by Cancerfonden (Sweden) grant 170710, www.cancerfonden.se (JVH). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Developmental Biology
                Embryology
                Embryos
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Model Organisms
                Zebrafish
                Research and Analysis Methods
                Model Organisms
                Zebrafish
                Research and Analysis Methods
                Animal Studies
                Experimental Organism Systems
                Animal Models
                Zebrafish
                Biology and Life Sciences
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                Eukaryota
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                Vertebrates
                Fish
                Osteichthyes
                Zebrafish
                Biology and Life Sciences
                Developmental Biology
                Organism Development
                Organogenesis
                Somites
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Body Limbs
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Body Limbs
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Muscle Fibers
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Muscle Fibers
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Muscle Fibers
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Amniotes
                Biology and Life Sciences
                Developmental Biology
                Morphogenesis
                Muscle Differentiation
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                Digestive System
                Gastrointestinal Tract
                Esophagus
                Medicine and Health Sciences
                Anatomy
                Digestive System
                Gastrointestinal Tract
                Esophagus
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                All relevant data are within the manuscript and its Supporting Information files.

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