Myogenesis in the sea urchin embryo: the molecular fingerprint of the myoblast precursors

Abstract

BackgroundIn sea urchin larvae the circumesophageal fibers form a prominent muscle system of mesodermal origin. Although the morphology and later development of this muscle system has been well-described, little is known about the molecular signature of these cells or their precise origin in the early embryo. As an invertebrate deuterostome that is more closely related to the vertebrates than other commonly used model systems in myogenesis, the sea urchin fills an important phylogenetic gap and provides a unique perspective on the evolution of muscle cell development.ResultsHere, we present a comprehensive description of the development of the sea urchin larval circumesophageal muscle lineage beginning with its mesodermal origin using high-resolution localization of the expression of several myogenic transcriptional regulators and differentiation genes. A few myoblasts are bilaterally distributed at the oral vegetal side of the tip of the archenteron and first appear at the late gastrula stage. The expression of the differentiation genes Myosin Heavy Chain, Tropomyosin I and II, as well as the regulatory genes MyoD2, FoxF, FoxC, FoxL1, Myocardin, Twist, and Tbx6 uniquely identify these cells. Interestingly, evolutionarily conserved myogenic factors such as Mef2, MyoR and Six1/2 are not expressed in sea urchin myoblasts but are found in other mesodermal domains of the tip of the archenteron. The regulatory states of these domains were characterized in detail. Moreover, using a combinatorial analysis of gene expression we followed the development of the FoxF/FoxC positive cells from the onset of expression to the end of gastrulation. Our data allowed us to build a complete map of the Non-Skeletogenic Mesoderm at the very early gastrula stage, in which specific molecular signatures identify the precursors of different cell types. Among them, a small group of cells within the FoxY domain, which also express FoxC and SoxE, have been identified as plausible myoblast precursors. Together, these data support a very early gastrula stage segregation of the myogenic lineage.ConclusionsFrom this analysis, we are able to precisely define the regulatory and differentiation signatures of the circumesophageal muscle in the sea urchin embryo. Our findings have important implications in understanding the evolution of development of the muscle cell lineage at the molecular level. The data presented here suggest a high level of conservation of the myogenic specification mechanisms across wide phylogenetic distances, but also reveal clear cases of gene cooption.

Echinodermata

“…When it comes to the muscle cell progenitors, a less clear distribution is observed, mostly due to the failure of scoring myoblasts independently from nearby foregut cells (Ruffi ns and Ettensohn 1996 ). Recent studies suggest that myoblast precursors are indeed specifi ed later on, soon after having undergone epithelial mesenchyme transition at the very early gastrula stage (Andrikou et al 2013 ).…”

“…As the archenteron elongates, secondary mesenchyme cells delaminate from its tip and disperse within the blastocoel, where they proliferate to form four types of non-skeletogenic mesoderm (NSM) cells (Ettensohn and Ruffi ns 1993 ): pigment cells (Gibson andBurke 1985 , 1987 ), blastocoelar cells (Tamboline and Burke 1992 ), coelomic pouch cells, and circumesophageal muscle cells (Ishimoda-Takagi et al 1984 ;Burke and Alvarez 1988 ;Andrikou et al 2013 ). These cell types are specifi ed long before delaminating from the tip of the archenteron where they are arranged spatially to occupy different positions along the animal/ vegetal and oral/aboral axis (see different color cells in Fig.…”

“…These cell types are specifi ed long before delaminating from the tip of the archenteron where they are arranged spatially to occupy different positions along the animal/ vegetal and oral/aboral axis (see different color cells in Fig. 1.6D, E ; for the specifi cation state of these NSM cells at the tip of the archenteron see Luo andAndrikou et al 2013 ).…”

Mechanisms of the epithelial-to-mesenchymal transition in sea urchin embryos

“…The myoblasts surround the esophagus by the early pluteus stage in S. purpuratus. 137 The myoblasts and coelomic pouch cells depart the archenteron as epithelial sheets during the prism stage, and they seem to transcribe snail. 94 The myoblasts extend filopodia toward the esophagus and form the ring of muscle in H. pulcherrimus.…”

A dynamic regulatory network explains ParaHox gene control of gut patterning in the sea urchin

“…compare confocal images in Fig. 4G,H), the cells of which express the muscle-specific terminal differentiation gene, Myosin heavy chain (SpMHC) (Andrikou et al, 2013;Venuti et al, 1993). In control larvae, MHC is expressed in the four muscular structures of the gut, the esophageal muscles and the cardiac, pyloric and anal sphincters.…”