Micromere‐derived signal regulates larval left‐right polarity during sea urchin development

Abstract

The micromeres (Mics) lineage functions as a morphogenetic signaling center in early embryos of sea urchins. The Mics lineage releases signals that regulate the specification of cell fates along the animal-vegetal and oral-aboral axes. We tested whether the Mics lineage might also be responsible for differentiation of the left-right (LR) axis by observing of the placement of the adult rudiment, which normally forms only on the left side of the larvae, after removal of the Mics lineage. When all of the Mics lineage were removed from embryos of the regular sea urchin Hemicentrotus pulcherrimus between the 16- and 64-cell stages, the LR placement of the rudiment became randomized. However, the immediate retransplantation of the Mics rescued the normal LR placement of the rudiment, indicating that the Mics lineage releases a signal that specifies LR polarity. Additionally, we investigated whether the specification of LR polarity of whole embryos in the indirect-developing sea urchin H. pulcherrimus is affected by LiCl exposure, which disturbs the establishment of LR asymmetry in a direct-developing sea urchin. Larvae derived from normal animal caps combined with LiCl-exposed Mics descendants were defective in normal LR placement of the rudiment, suggesting that LiCl interferes with the Mics-derived signal. In contrast, embryos of two sand dollar species (Scaphechinus mirabilis and Astriclypeus manni) were resistant to alteration of LR placement of the rudiment by either removal of the Mics lineage or LiCl exposure. These results indicate that the Mics lineage is involved in specification of LR polarity in the regular sea urchin H. pulcherrimus, and suggest that LiCl impairs the normal LR patterning by affecting Mics-derived signaling.

Reciprocal Signaling between the Ectoderm and a Mesendodermal Left-Right Organizer Directs Left-Right Determination in the Sea Urchin Embryo

“…This suggests that Notch signaling regulates nodal expression indirectly, likely through signaling between the mesoderm that is induced by Delta/Notch signaling and the endoderm that expresses nodal . This also suggests that Delta is the signal released by the micromeres that regulates positioning of the rudiment [46].…”

“…Precursors of the coelomic pouches have a double origin: part of these precursors derive from the non-skeletogenic mesoderm that is induced by Delta-Notch signaling at the vegetal pole while another contribution comes from the small micromeres [40]–[43]. Although formation of the rudiment is a textbook example of left-right asymmetry, very little was known until recently on the mechanism that control the asymmetric positioning of this organ [44]–[46]. In particular, rudiment positioning has been shown to depend on a signal released by the micromeres but the identity of this signal is unknown [46].…”

“…Although formation of the rudiment is a textbook example of left-right asymmetry, very little was known until recently on the mechanism that control the asymmetric positioning of this organ [44]–[46]. In particular, rudiment positioning has been shown to depend on a signal released by the micromeres but the identity of this signal is unknown [46].…”

Far from solved: A perspective on what we know about early mechanisms of left–right asymmetry

“…LR asymmetry is established in some animals during early developmental stages, long before cilia are present or in some cases, with no cilia present at all; these include snails (Meshcheryakov and Beloussov, 1975;Shibazaki et al, 2004), sea urchin (Kitazawa and Amemiya, 2007), Drosophila (Hozumi et al, 2006;Coutelis et al, 2008), Arabidopsis (Hashimoto, 2002;Thitamadee et al, 2002;Abe et al, 2004), and C. elegans (Priess, 1994;Hutter and Schnabel, 1995), for example. Other animals establish the LR axis later in development, when thousands of cells are present, but also without using cilia.…”

“…At the cellular level, classical data describe asymmetric, centripetal, chiral, not mirrorsymmetric counterclockwise movement of cells in avian embryos during early (prenode) gastrulation (Lepori, 1969). Functionally, it is known that sea urchin (Kitazawa and Amemiya, 2007) and mouse (Gardner, 2010) blastomeres are not equivalent with respect The three main models make distinct predictions as to the outcomes of a number of experimental questions. Most work on cilia has focused on mutations of ciliary genes, which does not distinguish between these models (since many of these same components also play important roles in intracellular polarity determination and are present in non-ciliated cells).…”