Involvement of Delta and Nodal signals in the specification process of five types of secondary mesenchyme cells in embryo of the sea urchin, Hemicentrotus pulcherrimus

Abstract

Secondary mesenchyme cells (SMCs) of the sea urchin embryo are composed of pigment cells, blastocoelar cells, spicule tip cells, coelomic pouch cells and muscle cells. To learn how and when these five types of SMCs are specified in the veg2 descendants, Notch or Nodal signaling was blocked with γ‐secretase inhibitor or Nodal receptor inhibitor, respectively. All types of SMCs were decreased with DAPT, while sensitivity to this inhibitor varied among them. Pulse‐treatment revealed that five types of SMCs are divided into “early” (pigment cells and blastocoelar cells) and “late” (spicule tip cells, coelomic pouch cells and muscle cells) groups; the “early” group was sensitive to DAPT up to the hatching, and the “late” group was sensitive until the mesenchyme blastula stage. Judging from timing of the shift of Delta‐expressing regions, it was suggested that the “early” group and “late” groups are derived from the lower and the middle tier of veg2 descendants, respectively. Interestingly, numbers of SMCs were also altered with SB431542; blastocoelar cells, coelomic pouch cells and circum‐esophageal muscles decreased, whereas pigment cells and spicule tip cells increased in number. Pulse‐treatment showed that the “early” group was sensitive up to the mesenchyme blastula stage, while the “late” group up to the onset of gastrulation. Thus, it became clear that precursor cells of the “early” and “late” groups, which are located in different regions in the vegetal plate, receive Delta and Nodal signals at different timings, resulting in the diversification of SMCs. Based on the obtained results, the specification processes of five types of SMCs are diagrammatically presented.

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

“…134 In H. pulcherrimus, the aboral field-derived pigment cells and the oral field-derived blastocoelar cells begin to migrate away from the vegetal plate into the blastocoel at the 12-hpf mesenchyme blastula stage. 135 After the EMT, the pigment cells leave the tip of the archenteron during gastrulation and enter the animal plate. Then, they migrate toward the vegetal pole through the aboral ectoderm and are distributed randomly in the aboral ectoderm by the prism larva stage.…”

“…9). 135 The myoblasts transcribe the myosin heavy chain gene and other related genes including tropomyosin I and II and the regulatory genes myoD2, foxF, foxC, foxL1, myocardin, twist, and tbx6, which are transcribed in both the left and right coelomic pouches from the late gastrula stage to the prism stage. Evolutionarily conserved myogenic factors such as mef2, myoR and mix1/2 are not expressed among the myoblasts but are found in other mesodermal domains at the tip of the archenteron.…”

Evolution, divergence and loss of the Nodal signalling pathway: new data and a synthesis across the Bilateria

“…However, unlike vertebrate nodal, which is expressed in the endomesoderm and is involved in its induction, non-vertebrate deuterostome nodal is expressed in different germ layer precursors depending on the group, and does not play a broad role in endoderm and mesoderm specification in all groups. Especially intriguing are results in echinoderms, since nodal and Pitx are expressed in the ectoderm and endoderm (Duboc et al, 2010;Ohguro et al, 2011;Bessodes et al, 2012), and mesoderm cells are specified even when the pathway is blocked (Duboc et al, 2005). In addition, as mentioned above, asymmetric expression and the actions of the Nodal pathway are conserved features of deuterostomes.…”

“…In addition, after gastrulation, nodal expression occurs in different germ layers depending on the group considered: the ectoderm in snails (Grande and Patel 2009), the ectoderm and endoderm in echinoderms (Duboc et al, 2010;Ohguro et al, 2011;Bessodes et al, 2012), all three germ layers in cephalochordates, urochordates, and hemichordates, and the endomesoderm in vertebrates (Hamada et al, 2002;Morokuma et al, 2002;Yu et al, 2002;Duboc et al, 2005;Wlizla 2011). Here we have shown that in brachiopods nodal is restricted to the mesoderm.…”

Symmetry Breaking and Establishment of Dorsal/Ventral Polarity in the Early Sea Urchin Embryo

“…Afterwards, nodal expression is rapidly downregulated in the presumptive dorsal blastomeres, exclusively marking the prospective ventral ectoderm of the early blastula [17,18,40]. Not only nodal expression is required for specification of the latter territory, but the small group of cells that specifically express nodal at the early blastula stage, thereupon behaves as an organizing centre imposing DV polarity in all three germ layers of the embryo [17,18,[41][42][43].…”