Evolutionarily conserved morphogenetic movements at the vertebrate head-trunk interface coordinate the transport and assembly of hypopharyngeal structures

Corinne Lours-Calet, Lucia Elvira Alvares, Amira S. El-Hanfy, Saniel Gandesha, Esther H. Walters, Debora R. Sobreira, Karl R. Wotton, Erika C. Jorge, Jennifer A. Lawson, A. Kelsey Lewis, Masazumi Tada, Colin Sharpe, Gabrielle Kardon, Susanne Dietrich

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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.
Original languageEnglish
Pages (from-to)231-246
Number of pages16
JournalDevelopmental Biology
Volume390
Issue number2
Early online date21 Mar 2014
DOIs
Publication statusPublished - 15 Jun 2014

Keywords

  • evolution of vertebrate developmental mechanisms, head - trunk interface, morphogenetic movements, occipital lateral mesoderm, occipital somites, occipital ectoderm, occipital neural crest, hypobranchial/ hypoglossal muscle, migratory muscle precursors, floor of pharynx, pharyngeal arches, circumpharyngeal route, zebrafish, Xenopus, chicken, mouse
  • RCUK
  • BBSRC
  • 29/G13556

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