Trunk lateral cells are neural crest-like cells in the ascidian Ciona intestinalis: Insights into the ancestry and evolution of the neural crest

Abstract

Neural crest-like cells (NCLC) that express the HNK-1 antigen and form body pigment cells were previously identified in diverse ascidian species. Here we investigate the embryonic origin, migratory activity, and neural crest related gene expression patterns of NCLC in the ascidian Ciona intestinalis. HNK-1 expression first appeared at about the time of larval hatching in dorsal cells of the posterior trunk. In swimming tadpoles, HNK-1 positive cells began to migrate, and after metamorphosis they were localized in the oral and atrial siphons, branchial gill slits, endostyle, and gut. Cleavage arrest experiments showed that NCLC are derived from the A7.6 cells, the precursors of trunk lateral cells (TLC), one of the three types of migratory mesenchymal cells in ascidian embryos. In cleavage arrested embryos, HNK-1 positive TLC were present on the lateral margins of the neural plate and later became localized adjacent to the posterior sensory vesicle, a staging zone for their migration after larval hatching. The Ciona orthologues of seven of sixteen genes that function in the vertebrate neural crest gene regulatory network are expressed in the A7.6/TLC lineage. The vertebrate counterparts of these genes function downstream of neural plate border specification in the regulatory network leading to neural crest development. The results suggest that NCLC and neural crest cells may be homologous cell types originating in the common ancestor of tunicates and vertebrates and support the possibility that a putative regulatory network governing NCLC development was co-opted to produce neural crest cells during vertebrate evolution.

A direct role for murine Cdx proteins in the trunk neural crest-gene regulatory network

“…Yet, it is noteworthy that a lack of body pigmentation has been previously reported following Cdx loss-of-function in the ascidian Halocynthia roretzi (Katsuyama et al, 1999). In this regard, it is also interesting that two sets of pigment cells of distinct origin have been described in ascidian embryos, and each has been suggested as the ancestral precursor of the NC (Abitua et al, 2012;Jeffery et al, 2008). One set is derived from the 'a' lineage and contributes to structures equivalent to the vertebrate eye and inner ear (Abitua et al, 2012;Nishida and Satoh, 1989), whereas the other is derived from the 'A' lineage and contributes to body pigmentation (Jeffery et al, 2008(Jeffery et al, , 2004.…”

“…In this regard, it is also interesting that two sets of pigment cells of distinct origin have been described in ascidian embryos, and each has been suggested as the ancestral precursor of the NC (Abitua et al, 2012;Jeffery et al, 2008). One set is derived from the 'a' lineage and contributes to structures equivalent to the vertebrate eye and inner ear (Abitua et al, 2012;Nishida and Satoh, 1989), whereas the other is derived from the 'A' lineage and contributes to body pigmentation (Jeffery et al, 2008(Jeffery et al, , 2004. We believe that the controversy concerning which set of pigment cells is the 'true' NC precursor could be resolved in accordance with the fact that the ascidian central nervous system is compartmentalized in a similar way to that of vertebrates (Imai et al, 2009), i.e.…”

“…The trunk NCC population has the unique potential to migrate either ventrally through the somites to give rise to neural derivatives (such as neurons and glia of the dorsal root and sympathetic ganglia), or dorsolaterally beneath the surface ectoderm to give rise to melanocytes of the skin (Kuo and Erickson, 2010). The melaninproducing melanocytes appear to represent the most ancient evolutionarily conserved NC-like derivative (Abitua et al, 2012;Jeffery et al, 2008).…”

Inflamed adult pharynx tissues and swimming larva of Ciona intestinalis share CiTNFα-producing cells

“…More specifically, the position of the CiTNFα-positive cells (containing transcript and protein) in the posterior part of the trunk has allowed us to identify these cells as components of the mesenchyme. In this region, Ciona larva contains four pockets (two pairs) of mesodermal cells (mesenchyme; Satou et al 2001;Nakayama et al 2002;Jeffery et al 2008). The localisation of CiTNFα-containing cells mainly in the lateral part of the mesenchyme, as observed in some histological sections, presumably can be related to distinct cell lineages.…”

An Advanced Filter-Feeder Hypothesis for Urochordate Evolution

“…Several regulatory genes (HNK-1, zic-2 and others) expressed in the trunk lateral cells that originate from A6.3 at the 32-cell stage and its daughter A7.6 cells in the ascidian, Ciona intestinalis, are also expressed in the neural crest cells of vertebrates. Based on this, Jeffery et al (2008) have suggested that these cells and their descendents are homologous to vertebrate neural crest cells. Like some vertebrate neural crest cells, the cells of the A7.6 lineage in ascidians migrate and differentiate into adult body pigment cells in the ascidian Ecteinascidia turbinata, although in the ascidian, Halocynthia roretzi, the trunk lateral cells give rise to adult blood cells and body wall muscle, which are considered to be mesodermal in origin.…”