Hedgehog signaling patterns mesoderm in the sea urchin

Abstract

The Hedgehog (Hh) signaling pathway is essential for patterning many structures in vertebrates including the nervous system, chordamesoderm, limb and endodermal organs. In the sea urchin, a basal deuterostome, Hh signaling is shown to participate in organizing the mesoderm. At gastrulation the Hh ligand is expressed by the endoderm downstream of the Brachyury and FoxA transcription factors in the endomesoderm gene regulatory network. The co-receptors Patched (Ptc) and Smoothened (Smo) are expressed by the neighboring skeletogenic and non-skeletogenic mesoderm. Perturbations of Hh, Ptc and Smo cause embryos to develop with skeletal defects and inappropriate non-skeletogenic mesoderm patterning, although initial specification of mesoderm occurs without detectable abnormalities. Perturbations of the pathway caused late defects in skeletogenesis and in the non-skeletogenic mesoderm, including altered numbers of pigment and blastocoelar cells, randomized left-right asymmetry of coelomic pouches, and disorganized circumesophageal muscle causing an inability to swallow. Together the data support the requirement of Hh signaling in patterning each of the mesoderm subtypes in the sea urchin embryo.

Late Alk4/5/7 signaling is required for anterior skeletal patterning in sea urchin embryos

“…The LvUnivin MO (Gene Tools) sequence is 5′-AGATCAAGACTTTCCAGACATCCAT-3′. For feeding assays, pluteus stage larvae were incubated with fluoresceinconjugated beads (10 µm diameter; Polysciences) for 30 min, then imaged, as previously described (Walton et al, 2009). Differential interference contrast (DIC) imaging, plane-polarized light imaging and epifluorescence imaging were carried out using a Zeiss Axioplan microscope at 200× magnification.…”

Notch and Nodal control forkhead factor expression in the specification of multipotent progenitors in sea urchin

“…1A), concurrent with expression of its downstream effector gli1 (Walton et al, 2006). The receptors ptc and smo are present throughout embryogenesis and are expressed prominently at the tip of the archenteron and in the coelomic pouches (Walton et al, 2006;Walton et al, 2009). Experimental activation of Hh signaling has been shown to randomize laterality and cause defects in muscle patterning (Walton et al, 2009), but the function of the endogenous Hh signal with regard to coelomic pouch development has not been studied systematically.…”

“…Laterality defects in mice caused by loss of Hh signaling can be rescued by expression of a constitutively active Smo receptor in lateral plate mesoderm resulting in unilateral expression of nodal (Tsiairis and McMahon, 2009). In sea urchins, overexpression of a constitutively active Smo receptor randomizes the position of the adult rudiment (Walton et al, 2009). It has recently been shown that unilateral expression of Nodal at the archenteron tip, and thus in close proximity to the Hh source, determines the sidedness of Nodal expression in the ectoderm (Bessodes et al, 2012).…”

“…During archenteron formation, the CPC progenitors are located at the tip but then split into two groups that relocate laterally to either side of the foregut. Although little is known about the regulation of this morphogenetic process, the expression of Hedgehog (Hh) in the adjoining endoderm and of its receptors in CPC progenitors (Walton et al, 2009) suggests the possible involvement of this signal. The small micromeres (SMMs) are also located at the tip of the archenteron and are distributed to either coelomic pouch at the pluteus stage (Pehrson and Cohen, 1986).…”

Evolutionary crossroads in developmental biology: sea urchins

“…Nodal later provides a signaling input that is important for specifying left-right asymmetries (Duboc et al, 2005), although, surprisingly, Nodal operates on the right side (compared with the situation in vertebrates where it operates on the left). In addition, Hedgehog signaling contributes to leftright patterning in the sea urchin (Walton et al, 2009), a property that is also shared with left-right specification in vertebrates (Levin et al, 1995).…”