Expression of the <i>dlx</i> gene family during formation of the cranial bones in the zebrafish (<i>Danio rerio</i>): Differential involvement in the visceral skeleton and braincase

Verreijdt, L.; Debiais-Thibaud, Mélanie; Borday-Birraux, Véronique; heyden, Christine Van der; Sire, Jean Yves; Huysseune, Ann

doi:10.1002/dvdy.20734

Cited by 35 publications

(31 citation statements)

References 73 publications

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“…All arch expression of dlx2a is ventral to the neurocranium (see Fig. S2 in the supplementary material), consistent with previous findings (Verreijdt et al, 2006). dlx5a is expressed within cartilages in the Meckel's-palatoquadrate and the hyosymplectic-ceratohyal joint regions at 60 hpf.…”

Section: Early Arch Expression Domains Map Onto the Developing Skeletonsupporting

confidence: 91%

hand2 and Dlx genes specify dorsal, intermediate and ventral domains within zebrafish pharyngeal arches

2010

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SUMMARYThe ventrally expressed secreted polypeptide endothelin1 (Edn1) patterns the skeleton derived from the first two pharyngeal arches into dorsal, intermediate and ventral domains. Edn1 activates expression of many genes, including hand2 and Dlx genes. We wanted to know how hand2/Dlx genes might generate distinct domain identities. Here, we show that differential expression of hand2 and Dlx genes delineates domain boundaries before and during cartilage morphogenesis. Knockdown of the broadly expressed genes dlx1a and dlx2a results in both dorsal and intermediate defects, In zebrafish, dlx3b and dlx5a are redundantly required for patterning specifically within intermediate domain-derived skeleton (Walker et al., 2006). By contrast, zebrafish hand2 nulls exhibit loss of lower jaws, but not upper jaws . hand2 is expressed ventral to nkx3.2, a marker of the jaw joint region . In zebrafish, hand2 mutants, nkx3.2 expands ventrally, indicating that hand2 patterns lower jaw identity in part by repressing jaw joint identity . However, it was unclear whether hand2 represses intermediate domain identity, because hand2 mutants consistently lose jointed-jaw skeleton .Fate-mapping experiments have indicated approximately where skeletal patterning domains arise within early pharyngeal arches Crump et al., 2004;Eberhart et al., 2006). However, these fate maps lacked the precision to directly connect early gene expression patterns to later skeletal shapes. Here, we present expression patterns that allow us to precisely define the dorsal, intermediate and ventral domains within zebrafish pharyngeal arches. We propose that the ventral domain comprises the hand2-expressing pharyngeal arch region, and the skeletal elements that are formed in this region. The ventral domain contains most of Meckel's and ceratohyal cartilages, and the dentary bone. The intermediate domain is the region of pharyngeal arches that expresses all Dlx genes, besides dlx2b (which is not expressed in anterior arches). Expression of the most restricted Dlx gene, dlx4a, reveals the borders of the intermediate domain. The intermediate domain includes the jaw joint region, and the second arch joint region, as well as the opercle and branchiostegal bones. Arch mesenchymal expression of dlx3b and dlx4b is also restricted to the intermediate domain. The dorsal domain is the region of the pharyngeal arch dorsal to dlx4a expression. Because dlx2a is expressed throughout the arch dorsoventral axis, co-labeling of dlx2a and dlx4a reveals the dorsal domain. The dorsal domain contains most of the palatoquadrate cartilage, including the distinctive pterygoid process, the hyomandibular cartilage and the maxillary bone. dlx5a and dlx6a expression does not correspond to a single domain.In addition to defining D-I-V domains, this report examines the functional requirements for D-I-V patterning. We show that along with dlx3b and dlx5a, dlx4b is also redundantly required for intermediate domain skeleton. We report a transgenic revealing the expression pattern of trps1, a gen...

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Section: Early Arch Expression Domains Map Onto the Developing Skeletonsupporting

confidence: 91%

hand2 and Dlx genes specify dorsal, intermediate and ventral domains within zebrafish pharyngeal arches

2010

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“…This search was to investigate whether the dlx2b:GFP reporter construct may be missing a repressor that normally turns off dlx2b expression orally or whether in situ studies failed to detect an endogenous oral domain of dlx2b. We examined larvae at Ϸ12-h intervals from 72 to 144 hpf, and while expression was found laterally in jaw mesenchyme in what may represent dlx2b expression in developing bone (30), there was no expression in epithelium where teeth would be expected to develop (data not shown). This finding suggests that the dlx2b:GFP reporter recapitulates the endogenous zebrafish expression pattern of dlx2b in pharyngeal tooth germs and its absence from oral epithelium.…”

Section: The Zebrafish Dlx2b: Gfp Reporter Drives Expression In Zebramentioning

confidence: 99%

Transgenic analysis of Dlx regulation in fish tooth development reveals evolutionary retention of enhancer function despite organ loss

Jackman

Stock

2006

Proc. Natl. Acad. Sci. U.S.A.

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It has been considered a ''law'' that a lost structure cannot reappear in evolution. The common explanation, that genes required for the development of the lost structure degrade by mutation, remains largely theoretical, however. Additionally, the extent to which this mechanism applies to systems of repeated parts, where individual modules are likely to exhibit few unique aspects of genetic control, is unclear. We investigated reversibility of evolution in one such system, the vertebrate dentition, using as a model loss of oral teeth in cypriniform fishes, which include the zebrafish. This evolutionary event, which occurred >50 million years ago, has not been reversed despite subsequent diversification of feeding modes and retention of pharyngeal teeth. We asked whether the cis-regulatory region of a gene whose expression loss parallels cypriniform tooth loss, Dlx2b, retains the capacity for expression in oral teeth. We first created a zebrafish reporter transgenic line that recapitulates endogenous dlx2b expression. We then showed that this zebrafish construct drives reporter expression in oral teeth of the related characiform Astyanax mexicanus. This result, along with our finding that Dlx genes are required for normal tooth development, suggests that changes in trans-acting regulators of these genes were responsible for loss of cypriniform oral teeth. Preservation of oral enhancer function unused for >50 million years could be the result of pleiotropic function in the pharyngeal dentition. If enhancers of other genes in the tooth developmental pathway are similarly preserved, teeth lost from specific regions may be relatively easy to reacquire in evolution.Astyanax ͉ Dollo's Law ͉ zebrafish

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“…As in mammals, zebrafish ossify by achondral, perichondral and endochondral route (Cubbage and Mabee, 1996;Verreijdt et al, 2006). Markers of osteoblast and chondrocyte differentiation are conserved during zebrafish bone formation (Li et al, 2009;Yan et al, 2002) and mutations that accurately model several human diseases have been identified (Clement et al, 2008;Fisher et al, 2003;Lang et al, 2006).…”

Section: Introductionmentioning

confidence: 96%

Hedgehog signalling is required for perichondral osteoblast differentiation in zebrafish

Felber

Roehl

2011

Mechanisms of Development

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In tetrapod long bones, Hedgehog signalling is required for osteoblast differentiation in the perichondrium. In this work we analyse skeletogenesis in zebrafish larvae treated with the Hedgehog signalling inhibitor cyclopamine. We show that cyclopamine treatment leads to the loss of perichondral ossification of two bones in the head. We find that the Hedgehog co-receptors patched1 and patched2 are expressed in regions of the perichondrium that will form bone before the onset of ossification. We also show that cyclopamine treatment strongly reduces the expression of osteoblast markers in the perichondrium and that perichondral ossification is enhanced in patched1 mutant fish. This data suggests a conserved role for Hedgehog signalling in promoting perichondral osteoblast differentiation during vertebrate skeletal development. However, unlike what is seen during long bone development, we did not observe ectopic chondrocytes in the perichondrium when Hedgehog signalling is blocked. This result may point to subtle differences between the development of the skeleton in the skull and limb.

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Expression of the dlx gene family during formation of the cranial bones in the zebrafish (Danio rerio): Differential involvement in the visceral skeleton and braincase

Cited by 35 publications

References 73 publications

hand2 and Dlx genes specify dorsal, intermediate and ventral domains within zebrafish pharyngeal arches

hand2 and Dlx genes specify dorsal, intermediate and ventral domains within zebrafish pharyngeal arches

Transgenic analysis of Dlx regulation in fish tooth development reveals evolutionary retention of enhancer function despite organ loss

Hedgehog signalling is required for perichondral osteoblast differentiation in zebrafish

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