Expression of Dlx genes during the development of the murine dentition

Zhao, Zhiyong; Stock, David W.; Buchanan, Anne V.; Weiss, Kenneth M.

doi:10.1007/s004270050314

Cited by 82 publications

(93 citation statements)

References 4 publications

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“…19). Dlx genes are expressed at numerous stages of tooth development in the zebrafish (20) and the mouse (21), and loss of Dlx function leads to early arrest of tooth development in the mouse (22). We have argued previously that Dlx genes are likely downstream of the cause of cypriniform oral tooth loss (19) and are thus a good model for the fate of developmental pathways once an initiation signal has been modified in evolution.…”

Section: Ollo's Law Of the Irreversibility Of Evolution States That Anmentioning

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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Section: Ollo's Law Of the Irreversibility Of Evolution States That Anmentioning

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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“…This includes molecules such as Msx1 (MacKenzie et al 1992;Tucker et al 1998a) and Dlx genes Thomas et al 1997;Zhao et al 2000) that are regionally restricted prior to the appearance of tooth germs.…”

Section: Dissociability and The Evolution Of Tooth Locationmentioning

confidence: 99%

The genetic basis of modularity in the development and evolution of the vertebrate dentition

Stock

2001

Phil. Trans. R. Soc. Lond. B

109

121

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The construction of organisms from units that develop under semi-autonomous genetic control (modules) has been proposed to be an important component of their ability to undergo adaptive phenotypic evolution. The organization of the vertebrate dentition as a system of repeated parts provides an opportunity to study the extent to which phenotypic modules, identi¢ed by their evolutionary independence from other such units, are related to modularity in the genetic control of development. The evolutionary history of vertebrates provides numerous examples of both correlated and independent evolution of groups of teeth. The dentition itself appears to be a module of the dermal exoskeleton, from which it has long been under independent genetic control. Region-speci¢c tooth loss has been a common trend in vertebrate evolution. Novel deployment of teeth and reacquisition of lost teeth have also occurred, although less frequently. Tooth shape di¡erences within the dentition may be discontinuous (referred to as heterodonty) or graded. The occurrence of homeotic changes in tooth shape provides evidence for the decoupling of tooth shape and location in the course of evolution. Potential mechanisms for regionspeci¢c evolutionary tooth loss are suggested by a number of mouse gene knockouts and human genetic dental anomalies, as well as a comparison between fully-developed and rudimentary teeth in the dentition of rodents. These mechanisms include loss of a tooth-type-speci¢c initiation signal, alterations of the relative strength of inductive and inhibitory signals acting at the time of tooth initiation and the overall reduction in levels of proteins required for the development of all teeth. Ectopic expression of tooth initiation signals provides a potential mechanism for the novel deployment or reacquisition of teeth; a single instance is known of a gene whose ectopic expression in transgenic mice can lead to ectopic teeth. Di¡er-ences in shape between incisor and molar teeth in the mouse have been proposed to be controlled by the region-speci¢c expression of signalling molecules in the oral epithelium. These molecules induce the expression of transcription factors in the underlying jaw mesenchyme that may act as selectors of tooth type. It is speculated that shifts in the expression domains of the epithelial signalling molecules might be responsible for homeotic changes in tooth shape. The observation that these molecules are regionally restricted in the chicken, whose ancestors were not heterodont, suggests that mammalian heterodonty may have evolved through the use of patterning mechanisms already acting on skeletal elements of the jaws. In general, genetic and morphological approaches identify similar types of modules in the dentition, but the data are not yet su¤cient to identify exact correspondences. It is speculated that modularity may be achieved by gene expression di¡erences between teeth or by di¡erences in the time of their development, causing mutations to have cumulative e¡ects on later-developing teeth. The mam...

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“…Whole-mount in situ hybridization was performed as described (Zhao and Rivkees, 2000b;Zhao et al, 2000). Briefly, embryos were fixed in 4% PFA for 2 hr and permeated with 10 g/ml proteinase K for 10 -15 min at 37°C.…”

Section: In Situ Hybridizationmentioning

confidence: 99%

Rho‐associated kinases play an essential role in cardiac morphogenesis and cardiomyocyte proliferation

Zhao

Rivkees

2002

Developmental Dynamics

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Rho-associated coiled-coil kinases (ROCKs), initially identified as effectors for Rho GTPases, play a role in cardiac cell physiology and are also expressed in the developing heart. However, their role in cardiac development is not known. To investigate the role of these kinases in cardiac development, we examined cardiac development in cultured murine embryos treated with the ROCK inhibitor Y27632. After inhibition of ROCK activity, we found disturbed cardiac chamber formation and trabeculation. To further examine the mechanisms by which ROCK blockade causes cardiac hypoplasia, we assessed programmed cell death and cell proliferation in the hearts. We found decreased cell proliferation in the Y27632-treated hearts, but no changes in programmed cell death. We further observed that ROCK inhibition decreased cardiac myocyte proliferation, suggesting that ROCK kinases regulate cardiomyocyte division. To identify factors involved in ROCK action in regulation of cardiac cell division, we examined expression of cell cycle proteins by using Western blot analysis. We found that ROCK blockade decreased expression of cell cycle proteins, cyclin D3, CDK6, and p27 KIP1 in the hearts and cardiomyocytes, which are required for initiation of cell cycle and G1/S phase transition. These observations show that ROCK kinases play a role in cardiac development and that ROCK kinases regulate cardiac cell proliferation and cell cycle protein expression. Developmental Dynamics 226:24 -32, 2003.

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Expression of Dlx genes during the development of the murine dentition

Cited by 82 publications

References 4 publications

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

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

The genetic basis of modularity in the development and evolution of the vertebrate dentition

Rho‐associated kinases play an essential role in cardiac morphogenesis and cardiomyocyte proliferation

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