Initial specification of the epibranchial placode in zebrafish embryos depends on the fibroblast growth factor signal

Abstract

In vertebrates, cranial sensory ganglia are mainly derived from ectodermal placodes, which are focal thickenings at characteristic positions in the embryonic head. Here, we provide the first description of the early development of the epibranchial placode in zebrafish embryos using sox3 as a molecular marker. By the one-somite stage, we saw a pair of single sox3-expressing domains appear lateral to the future hindbrain. The sox3 domain, which is referred to here as the early lateral placode, is segregated during the early phase of segmentation to form a pax2a-positive medial area and a pax2a-negative lateral area. The medial area subsequently developed to form the otic placode, while the lateral area was further segregated along the anteroposterior axis, giving rise to four sox3-positive subdomains by 26 hr postfertilization. Given their spatial relationship with the expression of the markers for the epibranchial ganglion, as well as their positions and temporal changes, we propose that these four domains correspond to the facial, glossopharyngeal, vagal, and posterior lateral line placodes in an anterior-to-posterior order. The expression of sox3 in the early lateral placode was absent in mutants lacking functional fgf8, while implantation of fibroblast growth factor (FGF) beads restored the sox3 expression. Using SU5402, which inhibits the FGF signal, we were able to demonstrate that formation of both the early lateral domains and later epibranchial placodes depends on the FGF signal operating at the beginning of somitogenesis. Together, these data provide evidence for the essential role of FGF signals in the development of the epibranchial placodes. Developmental Dynamics 236:564 -571, 2007.

Molecular analysis of neurogenic placode development in a basal ray‐finned fish

“…It is expressed in the ''posterior placodal area'' (Schlosser and Ahrens, 2004) within which the otic, epibranchial, and lateral line placodes form (reviewed in Ladher et al, 2010;Schlosser, 2006Schlosser, , 2010. We were particularly interested in examining its expression in paddlefish because of its strong expression in developing lateral line placodes and lateral line primordia in Xenopus (Schlosser and Ahrens, 2004) and its reported putative expression in lateral line placodes in medaka and zebrafish (Köster et al, 2000;Nikaido et al, 2007). As previously mentioned, these species only possess the mechanosensory division of the lateral line, whereas paddlefish also retain the electrosensory division.…”

“…Sox3 was reported as a particularly strong marker for lateral line placodes and elongating lateral line primordia in Xenopus (Schlosser and Ahrens, 2004), and in two teleosts, medaka and zebrafish (Köster et al, 2000;Nikaido et al, 2007). However, Xenopus, medaka, and zebrafish all lack the electrosensory division of the lateral line system: electrosensory ampullary organs were lost in anuran amphibians (Bullock, 1982;Bullock et al, 1983) and in the actinopterygian radiation leading to teleosts (although electroreception was independently ''re-invented'' at least twice within different groups of teleosts; Alves-Gomes, 2001; Bullock et al, 1983).…”

Patterning and cell fate in ear development

“…Thus, depending on the length of exposure of signals the appearance of some molecular markers, as Pax2 and Sox3 can be dissociated. In parallel, inhibition of FGF signalling in zebrafish indicates that induction of Sox3 and Pax2 requires FGF signalling in the oticepibranchial region but not in an interdependent manner (Groves and Bronner-Fraser, 2000;Nikaido et al, 2007;Sun et al, 2007). Results of our laboratory indicate that suppression of FGF signalling at specific stages let the embryo allow the development of otic cups, but devoid of Sox3 expression and neurons (Abello and Alsina, unpublished results).…”

“…required for epibranchial induction in chick and zebrafish (AbuElmagd et al, 2001), and recent data reinforced the idea that otic and epibranchial placodes do not emerge as separate identities by different inducing signals but, instead, share the same developmental origin (Millimaki et al, 2007;Nikaido et al, 2007;Sun et al, 2007).…”

Mechanisms of cranial placode assembly

“…Beside its known role in placode induction, specification and differentiation Freter et al, 2008;Ladher, 2005;Maier et al, 2010;Martin, 2006;Nechiporuk et al, 2006;Nikaido et al, 2007;Sun et al, 2007), Fgf signalling controls some aspects of the movements and behaviours driving placode coalescence.…”