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Dev Biol
2014 Jun 15;3902:231-46. doi: 10.1016/j.ydbio.2014.03.003.
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Evolutionarily conserved morphogenetic movements at the vertebrate head-trunk interface coordinate the transport and assembly of hypopharyngeal structures.
Lours-Calet C
,
Alvares LE
,
El-Hanfy AS
,
Gandesha S
,
Walters EH
,
Sobreira DR
,
Wotton KR
,
Jorge EC
,
Lawson JA
,
Kelsey Lewis A
,
Tada M
,
Sharpe C
,
Kardon G
,
Dietrich S
.
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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 lateralmesoderm 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 lateralmesoderm and ectoderm. Thus, we have discovered evolutionarily conserved morphogenetic movements, driven by the occipital lateralmesoderm and ectoderm, that ensure cell transport and organ assembly at the head-trunk interface.
Fig. 8.
DiI labelling of the Xenopus occipital lateralmesoderm. (A, B) Lateral views of Xenopus laevis transgenic cardiac actin:GFP embryos, rostral to the left, dorsal to the top. (Bi) Section of the embryo shown in (B) along the plane indicated in (B), dorsal to the right, medial to the top. (A) DiI-labelling (arrowhead) of the occipital lateralmesoderm next to the 1st somite (as identified by its green fluorescence) at st 20. (B, Bi) Three days later, the labelled lateralmesoderm has expanded in a ventral–rostral direction, surrounding the pharyngeal arches and heading towards the floor of the arches (arrowheads) as previously seen for the chicken. Abbreviations: ect, surface ectoderm; end, endoderm; ht, heart; and lm, lateralmesoderm.
Suppl. Material 3. Rostral extension of occipital gene expression domains is conserved in osteichthyans. Headâ€trunk interface of (Aâ€C) chicken embryos at HH20, (D,E) mouse embryos at E10.5 pc, (F,G) Xenopus
laevis embryos at st36 and (H,I) zebrafish embryos at 48 hpf; lateral views, rostral to the top (Aâ€E) or the
right (Fâ€I); the molecular markers used are indicated. The hypobranchial/hypoglossal muscle precursors
(HMP) express Lbx1 (A,D,F, arrows) or in the zebrafish, the paralogous gene lbx2 (H, arrows). The paired
type homeobox genes Alx4 and Prrx1 are expressed in the lateralmesoderm, with expression domains
anticipating the path of the HMP (B,C,E,G,I arrows).
alx4 (ALX homeobox 4 ) gene expression in Xenopus laevis embryo, assayed via in situ hybridization, NF stage 36, lateral view, anteriorright, dorsal up.
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