Developmental fates of shark head cavities reveal mesodermal contributions to tendon progenitor cells in extraocular muscles

Shunya Kuroda,Rie Kusakabe,Noritaka Adachi,Shigeru Kuratani

doi:10.1186/s40851-021-00170-2

Shunya Kuroda, Rie Kusakabe + Show 2 more

Open Access

https://doi.org/10.1186/s40851-021-00170-2

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Abstract

Vertebrate extraocular muscles (EOMs) function in eye movements. The EOMs of modern jawed vertebrates consist primarily of four recti and two oblique muscles innervated by three cranial nerves. The developmental mechanisms underlying the establishment of this complex and the evolutionarily conserved pattern of EOMs are unknown. Chondrichthyan early embryos develop three pairs of overt epithelial coeloms called head cavities (HCs) in the head mesoderm, and each HC is believed to differentiate into a discrete subset of EOMs. However, no direct evidence of these cell fates has been provided due to the technical difficulty of lineage tracing experiments in chondrichthyans. Here, we set up an in ovo manipulation system for embryos of the cloudy catshark Scyliorhinus torazame and labeled the epithelial cells of each HC with lipophilic fluorescent dyes. This experimental system allowed us to trace the cell lineage of EOMs with the highest degree of detail and reproducibility to date. We confirmed that the HCs are indeed primordia of EOMs but showed that the morphological pattern of shark EOMs is not solely dependent on the early pattern of the head mesoderm, which transiently appears as tripartite HCs along the simple anteroposterior axis. Moreover, we found that one of the HCs gives rise to tendon progenitor cells of the EOMs, which is an exceptional condition in our previous understanding of head muscles; the tendons associated with head muscles have generally been supposed to be derived from cranial neural crest (CNC) cells, another source of vertebrate head mesenchyme. Based on interspecies comparisons, the developmental environment is suggested to be significantly different between the two ends of the rectus muscles, and this difference is suggested to be evolutionarily conserved in jawed vertebrates. We propose that the mesenchymal interface (head mesoderm vs CNC) in the environment of developing EOM is required to determine the processes of the proximodistal axis of rectus components of EOMs.

Highlights

The extraocular muscles (EOMs) connect the surface of the eye and cranial wall and function in eyeball movements
Our results provide the first evidence that head cavities (HCs), which belong to the head mesoderm, give rise to dense connective tissues of the head muscles in shark; the mnc gives rise to tendon progenitor cells at the origin of the rectus muscles and at the insertion of lateral rectus muscles (Fig. 6d and e)
In our lineage tracing analysis in shark HCs, we confirmed the classical view of the developmental origin of EOMs; each HC gives rise to different subsets of EOMs innervated by each cranial motor nerve

Summary

Introduction

The extraocular muscles (EOMs) connect the surface of the eye and cranial wall and function in eyeball movements. The mandibular head cavity (mnc) and hyoid head cavity (hyc), on the other hand, are derived from the head paraxial mesoderm (Fig. 1b-d) [12]. Both HCs arise as schizocoels between the neurula and early pharyngula stages [12]. The morphology of HCs has long been believed to serve as a prepattern for EOM morphology [11, 15,16,17] This predicted lineage of HCs has only been roughly illustrated by histological observations of developmental series of elasmobranch embryos (sharks, skates, and rays) [10, 14]. The developmental contributions of HCs to nonmuscular tissues remain to be investigated [11, 12, 18,19,20]

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