<i>Dlx</i> gene expression during chick inner ear development

Brown, Stephen; Wang, Juemei; Groves, Andrew K.

doi:10.1002/cne.20418

Cited by 52 publications

(50 citation statements)

References 90 publications

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“…FGF8 is expressed on the medial side of the placode and in the frontonasal mass ectoderm from stage 15-22 (Song et al, 2004). The transcription factor, DLX5, is expressed in the olfactory placode and pit (Bhattacharyya et al, 2004;Brown et al, 2005;McLarren et al, 2003). SP8 is an FGF8-responsive, buttonhead-like transcription factor (Kawakami et al, 2004;Sahara et al, 2007).…”

Section: Nasal Placode Extirpation Decreases the Expression Of Nasal mentioning

confidence: 99%

Novel skeletogenic patterning roles for the olfactory pit

et al. 2009

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The position of the olfactory placodes suggests that these epithelial thickenings might provide morphogenetic information to the adjacent facial mesenchyme. To test this, we performed in ovo manipulations of the nasal placode in the avian embryo. Extirpation of placodal epithelium or placement of barriers on the lateral side of the placode revealed that the main influence is on the lateral nasal, not the frontonasal, mesenchyme. These early effects were consistent with the subsequent deletion of lateral nasal skeletal derivatives. We then showed in rescue experiments that FGFs are required for nasal capsule morphogenesis. The instructive capacity of the nasal pit epithelium was tested in a series of grafts to the face and trunk. Here, we showed for the first time that nasal pits are capable of inducing bone, cartilage and ectopic PAX7 expression, but these effects were only observed in the facial grafts. Facial mesenchyme also supported the initial projection of the olfactory nerve and differentiation of the olfactory epithelium. Thus, the nasal placode has two roles: as a signaling center for the lateral nasal skeleton and as a source of olfactory neurons and sensory epithelium.KEY WORDS: Chicken embryo, Placode, Nasal capsule, FGF8, Craniofacial, TuJ1, PAX7, Lateral nasal prominence Development 136, 219-229 (2009) MATERIALS AND METHODS EmbryosFertile White Leghorn chicken eggs (Gallus gallus; University of Alberta) and Japanese quail eggs (Coturnix coturnix japonica; Oregon State University, Corvalis) were used. Quail embryos were incubated ~12 hours after chicken embryos so that they reached the appropriate developmental stage (Schneider and Helms, 2003). Embryo work was approved by the UBC Animal Care Committee. Extirpations of nasal ectoderm, foil barrier placement and bead implantsNile Blue sulfate (0.1% in phosphate-buffered saline) was painted on the nasal placode of stage 15-16 (25-28 somites) embryos or on nasal pits of stage 20 embryos. The epithelium was removed with a tungsten needle. Control embryos received Nile Blue and the epithelium was left intact. Embryos were collected at 0, 6, 16 and 24 hours following surgery and gene expression was analyzed. Other embryos were collected at stage 38 for analysis of skeletal phenotypes. A third set of extirpated embryos had either an all-trans-retinoic acid-soaked bead (0.01 mg/ml; AG1X2 beads, BioRad) or an FGF8b-soaked bead (1 mg/ml, Peprotech; Affigel beads, Biorad) stapled onto the exposed mesenchyme. For barrier experiments, aluminium foil was inserted on the medial or lateral side of the nasal placode of stage 15 embryos. Grafting experiments Donor tissue preparationStage 20 or 26 donor (quail or chicken) frontonasal mass and lateral nasal prominences were collected in Hank's Balanced Salt Solution with Ca 2+ and Mg 2+ (HBSS). Frontonasal mass epithelium including the nasal pits was separated with 2% trypsin (see Fig. 1A) (Richman and Tickle, 1989). The surrounding surface epithelia were trimmed away from the nasal pit and 0.5% Neutral Red was adde...

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Section: Nasal Placode Extirpation Decreases the Expression Of Nasal mentioning

confidence: 99%

Novel skeletogenic patterning roles for the olfactory pit

et al. 2009

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“…2B, C; n¼10/11). However, Dlx3, another marker for the PPA (Brown et al, 2005) was unchanged in Fig. 1.…”

Section: Pax2 Does Not Regulate Ppa Identitymentioning

confidence: 89%

“…31, J; n¼8/8) and Dlx5 (Fig. 3K, L; n¼9/10), which normally mark a dorsal domain in the otocyst (Herbrand et al, 1998;Brown et al, 2005), were also unchanged. Tbx1, which is normally expressed laterally (Raft et al, 2004), showed a slight ventro-medial expansion of its expression domain ( Fig.…”

Section: Pax2 Influences Early Inner Ear Developmentmentioning

confidence: 90%

“…Whole-mount in situ hybridization was performed as described before, using chick probes for: Dlx3, Dlx5, Foxi2, Gbx2, Nkx5.1, Pax2, Phox2a, Phox2b, Soho1, and Tbx1 (Begbie and Graham, 2001;Brown et al, 2005;Freter et al, 2008). The neurofilament template was synthesized by PCR (primer details available on request).…”

Section: Whole-mount In Situ Hybridization and Immunohistochemistrymentioning

confidence: 99%

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Pax2 modulates proliferation during specification of the otic and epibranchial placodes

Freter¹,

Muta²,

O’Neill³

et al. 2012

Developmental Dynamics

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Background: The inner ear and epibranchial ganglia of vertebrates arise from a shared progenitor domain that is induced by FGF signalling, the posterior placodal area (PPA), before being segregated by Wnt signalling. One of the first genes activated in the PPA is the transcription factor Pax2. Loss-of-and gain-of function studies have defined a role for Pax2 in placodal morphogenesis and later inner ear development, but have not addressed the role Pax2 plays during the formation and maintenance of the PPA. Results: To understand the role of Pax2 during the development of the PPA, we used over-expression and repression of Pax2. Both gave rise to a smaller otocyst and repressed the formation of epibranchial placodes. In addition, cell cycle analysis revealed that Pax2 suppression reduced proliferation of the PPA. Key FindingsNeither suppression nor over-expression of Pax2 affects the extent of the precursor region of the inner ear and epibranchial placodes, the PPA. Suppressing and over-expressing Pax2 does affect the differentiation of the inner ear and the epibranchial placodes. Pax2 suppression reduces proliferation of PPA precursors.

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“…Dlx1 and Dlx6 (Brown et al, 2005), it is not yet clear whether the chicken expresses a functional Dlx4 protein (Brown et al, 2005; T. Coleman and A.J.B., unpublished). Additionally, no chicken Dlx bigene cluster has been cloned to date and the public chicken genome database does not contain any Dlx-bearing contigs large enough to reveal bigene cluster organization (Ensembl version 32.1h).…”

Section: Dlx3 Expression In Chick Brain 73mentioning

confidence: 99%

Dlx3 is expressed in the ventral forebrain of chicken embryos: implications for the evolution of the Dlx gene family

Zhu¹,

Bendall²

2006

Int. J. Dev. Biol.

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The archetypal genomic arrangement of vertebrate Dlx genes is as three bigene clusters (Dlx1/2, Dlx3/4, Dlx5/6). Phylogenetic sequence analysis of mouse and zebrafish Dlx clusters supports the notion that the Dlx3/4 cluster is more derived and the absence of expression of either Dlx3 or Dlx4 in the central nervous system, as reported to date, is consistent with this. Together, these observations have prompted a model in which cis-regulatory elements, responsible for directing Dlx gene transcription in the forebrain, were lost from the Dlx3/4 bigene cluster prior to the divergence of tetrapods from fish. Here, we describe Dlx3 expression in the forebrain of chicken embryos; this constitutes the first documented evidence of expression of either Dlx3 or Dlx4 in the central nervous system of a vertebrate. Our observations have implications for models of the evolutionary history of the Dlx gene family, for the genomic organization of Dlx genes in birds and for functional redundancy of Dlx gene function during avian forebrain development. KEY WORDS: Dlx3, transcription factor, chicken embryo, ventral forebrain, neurogenesisThe homeobox gene family that encodes Dlx transcription factors represents an example of a common paradigm in genome evolution wherein an archetypal gene (e.g. Distal-less) in a euchordate ancestor was serially duplicated over evolutionary time to give rise to a family of homologous genes in living vertebrates (e.g. Dlx1-Dlx6 in mammals). In extant mammals, the six Dlx genes are arranged as three linked pairs (or bigene clusters) on different chromosomes within syntenic regions that include three of the four Hox clusters (McGuinness et al., 1996, Nakamura et al., 1996, Liu et al., 1997. Zebrafish also have this genomic organization of six Dlx orthologues in three bigene clusters, although further large-scale duplications have left Danio rerio with an additional orphan paralogue for each of dlx2 and dlx4 , Ellies et al., 1997. Of the mammalian genomic loci cloned thus far, the Dlx intergenic region ranges from a minimum of 8.3 kb in the mouse Dlx1/2 cluster (McGuinness et al., 1996) to a maximum of 17.6 kb in the human DLX3/4 cluster . Intergenic regions for the genomically compact pufferfish Takifugu rubripes and Spheroides nephalus are smaller at 3-5 kb (Ghanem et al., 2003), with Danio rerio having intermediate sizes of 3.5 -7.3 kb (Ellies et al., 1997). Despite the significant variation in their size, several highly conserved non-coding sequence elements have been identified in the intergenic regions of Dlx bigene clusters and have been shown to behave as tissue-specific enhancers , Sumiyama et al., 2002, Ghanem et al., 2003 Int. J. Dev. Biol. 50: 71-75 (2006) , Park et al., 2004. Intergenic enhancer sharing therefore accounts for much of the overlap in expression of members of a Dlx bigene cluster.Phylogenetic sequence analysis of mouse and zebrafish Dlx clusters supports the notion that the Dlx3/4 cluster is more derived . Consistent with this, Dlx1, -2, -5 and -6 show more comm...

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Dlx gene expression during chick inner ear development

Cited by 52 publications

References 90 publications

Novel skeletogenic patterning roles for the olfactory pit

Novel skeletogenic patterning roles for the olfactory pit

Pax2 modulates proliferation during specification of the otic and epibranchial placodes

Dlx3 is expressed in the ventral forebrain of chicken embryos: implications for the evolution of the Dlx gene family

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