title: Evolutionarily conserved morphogenetic movements at the vertebrate head-trunk interface coordinate the transport and assembly of hypopharyngeal structures.
abstract: The vertebrate head-trunk interface (occipital region) has been heavily remodelled during evolution, and its development is still poorly understood. In extant jawed vertebrates, this region provides muscle precursors for the throat and tongue (hypopharyngeal/hypobranchial/hypoglossal muscle precursors, HMP) that take a stereotype path rostrally along the pharynx and are thought to reach their target sites via active migration. Yet, this projection pattern emerged in jawless vertebrates before the evolution of migratory muscle precursors. This suggests that a so far elusive, more basic transport mechanism must have existed and may still be traceable today. Here we show for the first time that all occipital tissues participate in well-conserved cell movements. These cell movements are spearheaded by the occipital lateral mesoderm and ectoderm that split into two streams. The rostrally directed stream projects along the floor of the pharynx and reaches as far rostrally as the floor of the mandibular arch and outflow tract of the heart. Notably, this stream leads and engulfs the later emerging HMP, neural crest cells and hypoglossal nerve. When we (i) attempted to redirect hypobranchial/hypoglossal muscle precursors towards various attractants, (ii) placed non-migratory muscle precursors into the occipital environment or (iii) molecularly or (iv) genetically rendered muscle precursors non-migratory, they still followed the trajectory set by the occipital lateral mesoderm and ectoderm. Thus, we have discovered evolutionarily conserved morphogenetic movements, driven by the occipital lateral mesoderm and ectoderm, that ensure cell transport and organ assembly at the head-trunk interface.
authors.affiliation: School of Biomedical & Health Sciences, King׳s College London, Hodgkin Building G43S/44S, Guy׳s Campus, London SE1 1UL, UK; GReD - Génétique Reproduction et Développement, UMR CNRS 6247, INSERM U931, Clermont Université, 24, Avenue des Landais, BP 80026, 63171 Aubiere Cedex, France.
authors.forename: Corinne
authors.initials: C
authors.lastname: Lours-Calet
authors.affiliation: School of Biomedical & Health Sciences, King׳s College London, Hodgkin Building G43S/44S, Guy׳s Campus, London SE1 1UL, UK; Department of Histology and Embryology, University of Campinas (UNICAMP), Rua Charles Darwin s/n, Cx. Postal 6109, CEP 13083-863 Campinas, São Paulo, Brazil.
authors.forename: Lucia E
authors.initials: LE
authors.lastname: Alvares
authors.affiliation: School of Biomedical & Health Sciences, King׳s College London, Hodgkin Building G43S/44S, Guy׳s Campus, London SE1 1UL, UK.
authors.forename: Amira S
authors.initials: AS
authors.lastname: El-Hanfy
authors.affiliation: School of Biomedical & Health Sciences, King׳s College London, Hodgkin Building G43S/44S, Guy׳s Campus, London SE1 1UL, UK; College Road Dental Practice, 2 College Road, Bromsgrove, B60 2NE.
authors.forename: Saniel
authors.initials: S
authors.lastname: Gandesha
authors.affiliation: School of Biomedical & Health Sciences, King׳s College London, Hodgkin Building G43S/44S, Guy׳s Campus, London SE1 1UL, UK.
authors.forename: Esther H
authors.initials: EH
authors.lastname: Walters
authors.affiliation: Department of Histology and Embryology, University of Campinas (UNICAMP), Rua Charles Darwin s/n, Cx. Postal 6109, CEP 13083-863 Campinas, São Paulo, Brazil; Institute for Biomedical and Biomolecular Science (IBBS), School of Pharmacy and Biomedical Sciences, University of Portsmouth, St. Michael׳s Building, White Swan Road, Portsmouth PO1 2DT, UK.
authors.forename: Débora Rodrigues
authors.initials: DR
authors.lastname: Sobreira
authors.affiliation: School of Biomedical & Health Sciences, King׳s College London, Hodgkin Building G43S/44S, Guy׳s Campus, London SE1 1UL, UK; EMBL/CRG Systems Biology Research Unit, Centre for Genomic Regulation (CRG) and UPF, Dr. Aiguader 88, 08003 Barcelona, Spain.
authors.forename: Karl R
authors.initials: KR
authors.lastname: Wotton
authors.affiliation: School of Biomedical & Health Sciences, King׳s College London, Hodgkin Building G43S/44S, Guy׳s Campus, London SE1 1UL, UK; Departamento de Morfologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Minas Gerais, Brazil.
authors.forename: Erika C
authors.initials: EC
authors.lastname: Jorge
authors.affiliation: Department of Human Genetics, University of Utah, 15 North 2030 East, Salt Lake City, UT 84112, USA.
authors.forename: Jennifer A
authors.initials: JA
authors.lastname: Lawson
authors.affiliation: Department of Human Genetics, University of Utah, 15 North 2030 East, Salt Lake City, UT 84112, USA.
authors.forename: A
authors.initials: A
authors.lastname: Kelsey Lewis
authors.affiliation: Department of Cell & Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK.
authors.forename: Masazumi
authors.initials: M
authors.lastname: Tada
authors.affiliation: Institute for Biomedical and Biomolecular Science (IBBS), School of Biology, University of Portsmouth, St. Michael׳s Building, White Swan Road, Portsmouth PO1 2DT, UK.
authors.forename: Colin
authors.initials: C
authors.lastname: Sharpe
authors.affiliation: Department of Human Genetics, University of Utah, 15 North 2030 East, Salt Lake City, UT 84112, USA.
authors.forename: Gabrielle
authors.initials: G
authors.lastname: Kardon
authors.affiliation: School of Biomedical & Health Sciences, King׳s College London, Hodgkin Building G43S/44S, Guy׳s Campus, London SE1 1UL, UK; Institute for Biomedical and Biomolecular Science (IBBS), School of Pharmacy and Biomedical Sciences, University of Portsmouth, St. Michael׳s Building, White Swan Road, Portsmouth PO1 2DT, UK. Electronic address: susanne.dietrich@port.ac.uk.
authors.forename: Susanne
authors.initials: S
authors.lastname: Dietrich
mesh_terms: D000818:Animals; D005075:Biological Evolution; D002465:Cell Movement / Q000502:physiology*; D004475:Ectoderm / Q000502:physiology*; D018274:Electroporation; D006257:Head / Q000033:anatomy & histology / Q000196:embryology; D007013:Hypopharynx / Q000196:embryology*; D007150:Immunohistochemistry; D017403:In Situ Hybridization; D008648:Mesoderm / Q000502:physiology*; D008866:Microsurgery; D009024:Morphogenesis / Q000502:physiology*; D009432:Neural Crest / Q000502:physiology; D013045:Species Specificity; D060726:Torso / Q000033:anatomy & histology / Q000196:embryology; D014714:Vertebrates / Q000196:embryology*
keywords: Chicken; Circumpharyngeal route; Evolution of vertebrate developmental mechanisms; Floor of pharynx; Head–trunk interface; Hypobranchial/hypoglossal muscle; Migratory muscle precursors; Morphogenetic movements; Mouse; Occipital ectoderm; Occipital lateral mesoderm; Occipital neural crest; Occipital somites; Pharyngeal arches; Xenopus; Zebrafish