Comparative expression analysis of transcription factor genes in the endostyle of invertebrate chordates

Abstract

The endostyle of invertebrate chordates is a pharyngeal organ that is thought to be homologous with the follicular thyroid of vertebrates. Although thyroid-like features such as iodine-concentrating and peroxidase activities are located in the dorsolateral part of both ascidian and amphioxus endostyles, the structural organization and numbers of functional units are different. To estimate phylogenetic relationships of each functional zone with special reference to the evolution of the thyroid, we have investigated, in ascidian and amphioxus, the expression patterns of thyroid-related transcription factors such as TTF-2/FoxE4 and Pax2/5/8, as well as the forkhead transcription factors FoxQ1 and FoxA. Comparative gene expression analyses depicted an overall similarity between ascidians and amphioxus endostyles, while differences in expression patterns of these genes might be specifically related to the addition or elimination of a pair of glandular zones. Expressions of Ci-FoxE and BbFoxE4 suggest that the ancestral FoxE class might have been recruited for the formation of thyroid-like region in a possible common ancestor of chordates. Furthermore, coexpression of FoxE4, Pax2/5/8, and TPO in the dorsolateral part of both ascidian and amphioxus endostyles suggests that genetic basis of the thyroid function was already in place before the vertebrate lineage.

Evolution of the thyroid: Anterior–posterior regionalization of theOikopleuraendostyle revealed byOtx,Pax2/5/8, andHox1expression

“…Previous cytochemical studies suggest that the iodination of proteins secreted by the glandular cells is probably catalyzed by extracellular peroxidases when the secreted substance passes the corridor cells toward the pharynx (Fredriksson et al, 1985). Overall, our observations in live animals complement past comparative studies between larvaceans and other chordates, and are consistent with the idea that the endostyle of Oikopleura shares a ground plan with all other known endostyles in chordates with respect to the organization of various types of cells involved in food-trapping and iodinating functions, and the fact that urochordates, cephalochordates, and vertebrates share the genetic machinery that patterns different functional zones in the dorsoventral axis (Hiruta et al, 2005).…”

“…Results show that a combinatorial code of molecular markers defines each zone of the endostyle across its dorsoventral axis (Hiruta et al, 2005). The conservation of this code of molecular markers between cephalochordates and urochordates reveals structural homologies that support a common evolutionary origin (Hiruta et al, 2005).…”

“…In a cross-section of the endostyle, these zones are numbered bilaterally from midventral to dorsolateral, and although the exact number and configuration of the zones differs among species, the endostyles in various chordates generally share an overall organization that includes midventral glandular zones, dorsolateral iodinebinding zones, and intervening zones of support cells (Hiruta et al, 2005).…”

“…Comparative analyses of the expression patterns of endostyle genes (e.g., Tpo, Pax2/5/8,FoxE4,FoxQ1,FoxA, in amphioxus and ascidians help us to understand the evolutionary origin of the vertebrate thyroid (Kozmik et al, 1999;Ogasawara et al, 1999;Ristoratore et al, 1999;Venkatesh et al, 1999;Ogasawara, 2000;Murakami et al, 2001;Ogasawara and Satou, 2003;Sasaki et al, 2003;Hiruta et al, 2005;Mazet et al, 2005). Results show that a combinatorial code of molecular markers defines each zone of the endostyle across its dorsoventral axis (Hiruta et al, 2005).…”

Morphogenesis of the thyroid gland

“…FoxE genes are expressed in the thyroid Page 34 of 68 A c c e p t e d M a n u s c r i p t 34 homolog of the adult endostyle that remains contiguous with the pharyngeal endoderm (Ogasawara and Satou, 2003;Hiruta et al, 2005). It has therefore been hypothesized that a function of a FoxE gene arose in the endostyle already in urochordates to regulate thyroid specific gene expression before a putative morphogenetic function developed (Hiruta et al, 2005). In Xenopus, a FoxE1 gene homologous to murine Foxe1 is expressed in the presumptive pituitary and thyroid that later buds off from the maternal germ layer (El-Hodiri et al, 2005).…”