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Clonal Analysis Reveals a Common Origin Between Nonsomite-Derived Neck Muscles and Heart Myocardium

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Clonal Analysis Reveals a Common Origin Between Nonsomite-Derived Neck Muscles and Heart Myocardium Clonal analysis reveals a common origin between nonsomite-derived neck muscles and heart myocardium Fabienne Lescroarta,1, Wissam Hamoua, Alexandre Francoub, Magali Théveniau-Ruissyb, Robert G. Kellyb, and Margaret Buckinghama,2 aUnité de Génétique Moléculaire du Développement, CNRS Unité de Recherche Associée 2578, Institut Pasteur, 75015 Paris, France; and bAix-Marseille Université, Institut de Biologie du Développement de Marseille, CNRS Unité Mixte de Recherche 7288, 13288 Marseille, France Contributed by Margaret Buckingham, December 23, 2014 (sent for review November 10, 2014; reviewed by Michael Levine and Drew Noden) Neck muscles constitute a transition zone between somite-derived Masticatory and facial expression muscles derive from the skeletal muscles of the trunk and limbs, and muscles of the head, mesodermal core that extends into the first and second branchial which derive from cranial mesoderm. The trapezius and sterno- (or pharyngeal) arches, respectively (11). These arches also con- cleidomastoid neck muscles are formed from progenitor cells that tain SHF cardiac progenitors (12). Cells with divergent cardiac have expressed markers of cranial pharyngeal mesoderm, whereas and skeletal muscle fates in this cardiopharyngeal mesoderm are other muscles in the neck arise from Pax3-expressing cells in the similarly labeled by genetic tracing (13). Furthermore, retrospec- somites. Mef2c-AHF-Cre genetic tracing experiments and Tbx1 mu- tive clonal analysis in the mouse embryo has shown that masti- tant analysis show that nonsomitic neck muscles share a gene catory muscles of the head and right ventricular myocardium regulatory network with cardiac progenitor cells in pharyngeal me- originate from common progenitor cells, whereas facial expres- soderm of the second heart field (SHF) and branchial arch-derived sion muscles share a common clonal origin with the arterial pole head muscles. Retrospective clonal analysis shows that this group of the heart, such that myocardium at the base of the pulmonary of neck muscles includes laryngeal muscles and a component of the trunk or the aorta is clonally related to left or right facial ex- splenius muscle, of mixed somitic and nonsomitic origin. We dem- pression muscles, respectively (14). Cardiopharyngeal mesoderm onstrate that the trapezius muscle group is clonally related to myo- cells that give rise to both cardiac and skeletal muscle derivatives cardium at the venous pole of the heart, which derives from the are already present in urochordates, such as the ascidian Ciona posterior SHF. The left clonal sublineage includes myocardium of intestinalis, where the equivalent of an SHF can be distinguished the pulmonary trunk at the arterial pole of the heart. Although (15). A number of genes, including homologs of vertebrate Islet1 muscles derived from the first and second branchial arches also and Tbx1, are expressed in ascidian cardiopharyngeal mesoderm share a clonal relationship with different SHF-derived parts of the and form a gene regulatory network that governs both heart and heart, neck muscles are clonally distinct from these muscles and pharyngeal muscle formation (16, 17). define a third clonal population of common skeletal and cardiac Muscles of the neck play an essential role in coordination of muscle progenitor cells within cardiopharyngeal mesoderm. By link- movement between the head and trunk. In this transition zone, ing neck muscle and heart development, our findings highlight the muscles of both branchial and somitic origin are found. Myo- importance of cardiopharyngeal mesoderm in the evolution of the blasts in the more caudal branchial arches (3rd, 4th, and 6th) are vertebrate heart and neck and in the pathophysiology of human thought to give rise to neck muscles such as the cucullaris muscle, congenital disease. neck muscles | myocardium | retrospective clonal analysis | mouse embryo | Tbx1 Significance n mammals, all skeletal muscles are not equivalent. Entry into Head muscles, derived from the first and second pharyngeal Ithe skeletal muscle program and subsequent differentiation arches, share common progenitors with myocardial cells of the depend on transcription factors of the MyoD (myogenic differ- heart. This is in contrast to somite-derived skeletal muscles of the trunk and limbs. Neck muscles, located in the transition zone entiation 1) family. However, upstream regulators of the myo- between head and trunk, have both a somitic and nonsomitic genic program differ in different parts of the body. Skeletal origin. We now demonstrate a clonal relationship between muscles of the trunk and limbs derive from the somites and thus nonsomitic neck muscles and myocardial cells located in the are descendants of progenitors expressing Pax3, a paired box atria, inflow and outflow regions of the heart. This is distinct transcription factor that plays a major role in the control of −/− −/− from that of the two head muscle lineages. Formation of these myogenesis (1, 2). In Pax3 ;Myf5 double mutants most neck muscles, like those in the head, depends on a gene regu- skeletal muscles are lost. However, muscles in the cranial part of latory network shared with myocardial progenitors. We thus the embryo are not affected in these mutant mice (3), showing identify a third clonal group within cardiopharyngeal meso- that myogenesis in head skeletal muscles is controlled by a dif- derm, with implications for human malformations. ferent upstream genetic network (2). Indeed, head muscles are − + formed from cranial mesoderm, derived from Pax3 ;Mesp1 Author contributions: F.L. and M.B. designed research; F.L., W.H., A.F., and M.T.-R. per- (mesoderm posterior homolog transcription factor 1) cells (4, 5). formed research; F.L., R.G.K., and M.B. analyzed data; and F.L., R.G.K., and M.B. wrote the paper. Many of these myogenic progenitors express genes, including Islet1 (Isl1 transcription factor), Nkx2-5,orTbx1 (T-box tran- Reviewers: M.L., University of California Berkeley; and D.N., Cornell University. scription factor 1), that are also expressed in cardiac progenitor The authors declare no conflict of interest. 1 cells of the second heart field (SHF) within pharyngeal meso- Present address: Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire, Université Libre de Bruxelles, B61070, Belgium. derm populations that form myocardium at the poles of the heart 2To whom correspondence should be addressed. Email: margaret.buckingham@ (6, 7). Among these regulators, Tbx1 is required for development pasteur.fr. of both the arterial pole of the heart and head muscle specifi- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. cation (8–10). 1073/pnas.1424538112/-/DCSupplemental. 1446–1451 | PNAS | February 3, 2015 | vol. 112 | no. 5 www.pnas.org/cgi/doi/10.1073/pnas.1424538112 Downloaded by guest on September 27, 2021 or its mammalian derivatives the trapezius and sternocleido- some neck muscles, including the trapezius and sternocleido- mastoidius, which, in keeping with a branchial origin, are in- mastoid muscles, are labeled (Fig. 1 C and D). The Mef2c nervated by a cranial nerve (18). Recent analysis of gene (myocyte enhancer factor 2c) enhancer is activated in the ante- expression and genetic tracing supports this view. The cucullaris rior SHF (21), and when Mef2c-Cre transgenic mice are crossed R-nlacZ/+ muscle in birds and turtles derives from cells in adjacent lateral with the Rosa26 reporter line, labeling is seen in head mesoderm that do not express Pax3 but express Tbx1 (19). De- muscles, notably those derived from the first branchial arch (14), spite evolutionary changes in cranial somites, this is also the case as well as in myocardium of the pulmonary trunk, aorta, and right for the progenitors of the trapezius and sternocleidomastoid ventricle. The trapezius and sternocleidomastoid muscles are also muscles in the mouse (19), where progenitors were also shown to labeled using this Cre line, as shown for the trapezius muscles on have expressed Islet1. Furthermore the trapezius muscle is missing whole-mount X-gal–stained embryos at embryonic day (E)14.5 in Tbx1 mutants (10, 19), consistent with an origin in cranial me- and E12.5 (Fig. 1 E and F). At E10.5 (Fig. 1G), labeling can be soderm rather than somites, in the mouse embryo. observed in the posterior pharyngeal region, where trapezius Here we address the question of a link between nonsomite- progenitors are potentially present. In keeping with this, these derived neck muscles and the myocardium. Using genetic tracing cells also express MyoD, indicating commitment to the skeletal in WT and Tbx1 mutant embryos and retrospective clonal anal- muscle lineage (1) (Fig. 1H). These results show that progenitors ysis, we characterize such muscles and show that neck muscle of nonsomitic neck muscles express common markers with, and progenitor cells share a common clonal origin with the venous originate in close proximity to, cardiac progenitors. pole of the heart. Our results identify a third common skeletal and cardiac progenitor population in cardiopharyngeal meso- No Clonal Relation with Head or Somite-Derived Muscles. To inves- derm, and we discuss the importance of this tissue in the evo- tigate a potential clonal relationship between these neck muscles, lution of the vertebrate heart and head/neck and the implications muscles derived from the first and second branchial arches, and for human pathology. somite-derived muscles of the neck and body, we performed
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