Neurogenin1 Defines Zebrafish Cranial Sensory Ganglia Precursors

Abstract

Cells delaminate from epithelial placodes to form sensory ganglia in the vertebrate head. We describe the formation of cranial neurogenic placodes in the zebrafish, Danio rerio, using bHLH transcription factors as molecular markers. A single neurogenin gene, neurogenin1 (ngn1), is required for the development of all zebrafish cranial ganglia, which contrasts with other described vertebrates. Expression of ngn1 delineates zebrafish ganglionic placodes, including trigeminal, lateral line, and epibranchial placodes. In addition, ngn1 is expressed in a subset of cells within the otic vesicle that will delaminate to form the octaval (statoacoustic) ganglion. The trigeminal placode is the first to differentiate, and forms just lateral and adjacent to the neural crest. Expression of ngn1 is transient and prefigures expression of a related bHLH transcription factor, neuroD. Interfering with ngn1 function using a specific antisense morpholino oligonucleotide blocks differentiation of all cranial ganglia but not associated glial cells. Lateral line sensory neuromasts develop independently of ngn1 function, suggesting that two derivatives of lateral line placodes, ganglia and migrating primordia, are under separate genetic control.

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

“…To identify the four subdomains at later stages, we compared the expression of sox3 at 26 hpf with that of ngn1, which is specifically expressed in the individual epibranchial ganglia of zebrafish embryos (Andermann et al, 2002). Two-color in situ hybridization revealed that ngn1 is expressed in the anterior sox3-expressing subdomains p1 and p2 (Fig.…”

“…For example, members of the basic helixloop-helix transcription factor family, neurogenin1 (ngn1) and neurogenin2 (ngn2) are expressed in different subsets of ganglia dependent on species, and functional analyses showed that ngn genes are important for the development of the epibranchial ganglia (Fode et al, 1998;Ma et al, 1998;Schlosser and Northcutt, 2000;AbuElmagd et al, 2001;Andermann et al, 2002). Indeed, ectopic expression of ngn1 induces formation of excessive neurons in Xenopus and zebrafish embryos (Ma et al, 1996;Blader et al, 1997).…”

“…Indeed, ectopic expression of ngn1 induces formation of excessive neurons in Xenopus and zebrafish embryos (Ma et al, 1996;Blader et al, 1997). Gene targeting in mice showed that Ngn2 is required for delamination, migration, and differentiation of neurons in the facial and glossopharyngeal placodes (Fode et al, 1998), and morpholino knockdown of ngn1 in zebrafish blocked differentiation of all cranial ganglia (Andermann et al, 2002). Furthermore, many studies have shown that sox2 and sox3, members of the Sox gene family, are expressed in the epibranchial placodes at the earliest stage of placode development in chicks Ishii et al, 2001), frogs (Mizuseki et al, 1998), medaka (Koster et al, 2000), and zebrafish (Okuda et al, 2006).…”

Cadherin‐4 plays a role in the development of zebrafish cranial ganglia and lateral line system

“…The zebrafish cranial ganglia, located ventrolateral to the hindbrain, consist of the trigeminal (gV), facial (gVII), statoacoustic (gVIII), glossopharyngeal (gIX), and vagal (gX) ganglia (Raible and Kruse, 2000). The gV becomes recognizable as early as 9 hr post fertilization (hpf), the earliest of the cranial ganglia (Andermann et al, 2002). The gVIII is formed from delaminating otic epithelium between 22-30 hpf (Haddon and Lewis, 1996).…”

“…The zebrafish lateral line system contains four ganglia and sets of neuromasts (Metcalfe, 1985(Metcalfe, , 1989Raible and Kruse, 2000). The posterior lateral line ganglion (gP), caudal to the otic vesicle, can be recognized as early as 14 hpf (Andermann et al, 2002). The anterodorsal ganglion (gAD) and anteroventral ganglion (gAV), located anterior to the otic vesicle, develop from the anterior lateral line placode area around 24 hpf, while the middle lateral line ganglion (gM), located anteromedial to the gP, develops after 26 hpf (Andermann et al, 2002).…”