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Dive into the research topics where David W. Stock is active.

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Featured researches published by David W. Stock.


Nature | 2004

Hedgehog signalling controls eye degeneration in blind cavefish

Yoshiyuki Yamamoto; David W. Stock; William R. Jeffery

Hedgehog (Hh) proteins are responsible for critical signalling events during development but their evolutionary roles remain to be determined. Here we show that hh gene expression at the embryonic midline controls eye degeneration in blind cavefish. We use the teleost Astyanax mexicanus, a single species with an eyed surface-dwelling form (surface fish) and many blind cave forms (cavefish), to study the evolution of eye degeneration. Small eye primordia are formed during cavefish embryogenesis, which later arrest in development, degenerate and sink into the orbits. Eye degeneration is caused by apoptosis of the embryonic lens, and transplanting a surface fish embryonic lens into a cavefish optic cup can restore a complete eye. Here we show that sonic hedgehog (shh) and tiggy-winkle hedgehog (twhh) gene expression is expanded along the anterior embryonic midline in several different cavefish populations. The expansion of hh signalling results in hyperactivation of downstream genes, lens apoptosis and arrested eye growth and development. These features can be mimicked in surface fish by twhh and/or shh overexpression, supporting the role of hh signalling in the evolution of cavefish eye regression.


Development | 2003

Zebrafish fgf24 functions with fgf8 to promote posterior mesodermal development.

Bruce W. Draper; David W. Stock; Charles B. Kimmel

Fibroblast growth factor (Fgf) signaling plays an important role during development of posterior mesoderm in vertebrate embryos. Blocking Fgf signaling by expressing a dominant-negative Fgf receptor inhibits posterior mesoderm development. In mice, Fgf8 appears to be the principal ligand required for mesodermal development, as mouse Fgf8 mutants do not form mesoderm. In zebrafish, Fgf8 is encoded by the acerebellar locus, and, similar to its mouse otholog, is expressed in early mesodermal precursors during gastrulation. However, zebrafish fgf8 mutants have only mild defects in posterior mesodermal development, suggesting that it is not the only Fgf ligand involved in the development of this tissue. We report here the identification of an fgf8-related gene in zebrafish, fgf24, that is co-expressed with fgf8 in mesodermal precursors during gastrulation. Using morpholino-based gene inactivation, we have analyzed the function of fgf24 during development. We found that inhibiting fgf24 function alone has no affect on the formation of posterior mesoderm. Conversely, inhibiting fgf24 function in embryos mutant for fgf8 blocks the formation of most posterior mesoderm. Thus, fgf8 and fgf24 are together required to promote posterior mesodermal development. We provide both phenotypic and genetic evidence that these Fgf signaling components interact with no tail and spadetail, two zebrafish T-box transcription factors that are required for the development of all posterior mesoderm. Last, we show that fgf24 is expressed in early fin bud mesenchyme and that inhibiting fgf24 function results in viable fish that lack pectoral fins.


Critical Reviews in Oral Biology & Medicine | 1998

Dynamic Interactions and the Evolutionary Genetics of Dental Patterning

Kenneth M. Weiss; David W. Stock; Zhiyong Zhao

The mammalian dentition is a segmental, or periodically arranged, organ system whose components are arrayed in specific number and in regionally differentiated locations along the linear axes of the jaws. This arrangement evolved from simpler dentitions comprised of many single-cusp teeth of relatively indeterminate number. The different types of mammalian teeth have subsequently evolved as largely independent units. The experimentally documented developmental autonomy of dental primordia shows that the basic dental pattern is established early in embryogenesis. An understanding of how genetic patterning processes may work must be consistent with the different modes of development, and partially independent evolution, of the upper and lower dentition in mammals. The periodic nature of the location, number, and morphological structure of teeth suggests that processes involving the quantitative interaction of diffusible signaling factors may be involved. Several extracellular signaling molecules and their interactions have been identified that may be responsible for locating teeth along the jaws and for the formation of the incisor field. Similarly, the wavelike expression of signaling factors within developing teeth suggests that dynamic interactions among those factors may be responsible for crown patterns. These factors seem to be similar among different tooth types, but the extent to which crown differences can be explained strictly in terms of variation in the parameters of interactions among the same genes, as opposed to tooth-type-specific combinatorial codes of gene expression, is not yet known. There is evidence that combinatorial expression of intracellular transcription factors, including homeobox gene families, may establish domains within the jaws in which different tooth types are able to develop. An evolutionary perspective can be important for our understanding of dental patterning and the designing of appropriate experimental approaches, but dental patterns also raise basic unresolved questions about the nature of the evolutionary assumptions made in developmental genetics.


Evolution & Development | 2003

Development and evolution of craniofacial patterning is mediated by eye-dependent and -independent processes in the cavefish Astyanax.

Yoshiyuki Yamamoto; Luis Espinasa; David W. Stock; William R. Jeffery

Summary We studied the development and evolution of craniofacial features in the teleost fish, Astyanax mexicanus. This species has an eyed surface dwelling form (surface fish) and many different cave dwelling forms (cavefish) with various degrees of reduced eyes and pigmentation. The craniofacial features we examined are the tooth‐bearing maxillary bones, the nasal and antorbital bones, the circumorbital bones, and the opercular bones, all of which show evolutionary modifications in different cavefish populations. Manipulations of eye formation by transplantation of the embryonic lens, by lentectomy, or by removing the optic vesicle showed that eye‐dependent and ‐independent processes change both the surface fish and cavefish craniofacial skeletons. The size of the olfactory pits, which the nasal and antorbital bones define, and the size and positioning of the circumorbital bones were found to correlate with eye development. For the six suborbital bones (SO1–6), the relationship with the developing eye appears to be due to ossification initiated from foci in the suborbital canal of cranial neuromasts, whose patterning is also highly correlated with the presence or absence of an eye. By contrast, we found that the number of maxillary teeth, the number of SO3 bone elements, the positioning of SO4–6 with respect to the opercular bone, and the shape of the opercular bone are not dependent on eye formation and vary among different cavefish populations. The results suggest that evolution of the cavefish craniofacial skeleton is controlled by multiple developmental events, some a direct consequence of eye degeneration and others unrelated to loss of the eye.


Development | 2006

Developmental genetic mechanisms of evolutionary tooth loss in cypriniform fishes

David W. Stock; William R. Jackman; Josh Trapani

The fossil record indicates that cypriniform fishes, a group including the zebrafish, lost oral teeth over 50 million years ago. Despite subsequent diversification of feeding modes, no cypriniform has regained oral teeth, suggesting the zebrafish as a model for studying the developmental genetic basis of evolutionary constraint. To investigate the mechanism of cypriniform tooth loss, we compared the oral expression of seven genes whose mammalian orthologs are involved in tooth initiation in the zebrafish and the Mexican tetra, Astyanax mexicanus, a related species retaining oral teeth. The most significant difference we found was an absence in zebrafish oral epithelium of expression of dlx2a and dlx2b, transcription factors that are expressed in early Astyanax odontogenic epithelium. Analysis of orthologous genes in the Japanese medaka (Oryzias latipes) and a catfish (Synodontis multipunctatus) suggests that expression was lost in cypriniforms, rather than gained in Astyanax. Treatment of Astyanax with an inhibitor of Fibroblast growth factor (Fgf) signaling produced a partial phenocopy of the zebrafish oral region, in that oral teeth, and expression of dlx2a and dlx2b, were lost, whereas shh and pitx2, genes whose expression is present in zebrafish oral epithelium, were unaffected. We hypothesize that a loss of Fgf signaling to oral epithelium was associated with cypriniform tooth loss.


Development Genes and Evolution | 2000

Expression of Dlx genes during the development of the murine dentition

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

Abstract The mammalian Dlx homeobox gene family has been shown to play multiple roles in tooth development, but a detailed comparison of the expression pattern of all members throughout tooth development has been lacking. We provide such an analysis for the six known murine Dlx genes. The expression patterns for these genes allow a refinement of previously proposed models for the role of Dlx genes in tooth type specification and raise the possibility of roles for subsets of these genes in tooth initiation, morphogenesis (enamel navel formation, enamel knot induction, cervical loop growth), and enamel formation. The relationship of Dlx gene expression to their genomic organization suggests coordinate regulation of linked genes at early stages but regulatory differences at later stages.


Proceedings of the National Academy of Sciences of the United States of America | 2002

Genomic structure and functional control of the Dlx3-7 bigene cluster

Kenta Sumiyama; Steven Q. Irvine; David W. Stock; Kenneth M. Weiss; Kazuhiko Kawasaki; Nobuyoshi Shimizu; Cooduvalli S. Shashikant; Webb Miller; Frank H. Ruddle

The Dlx genes are involved in early vertebrate morphogenesis, notably of the head. The six Dlx genes of mammals are arranged in three convergently transcribed bigene clusters. In this study, we examine the regulation of the Dlx3-7 cluster of the mouse. We obtained and sequenced human and mouse P1 clones covering the entire Dlx3-7 cluster. Comparative analysis of the human and mouse sequences revealed several highly conserved noncoding regions within 30 kb of the Dlx3-7-coding regions. These conserved elements were located both 5′ of the coding exons of each gene and in the intergenic region 3′ of the exons, suggesting that some enhancers might be shared between genes. We also found that the protein sequence of Dlx7 is evolving more rapidly than that of Dlx3. We conducted a functional study of the 79-kb mouse genomic clone to locate cis-element activity able to reproduce the endogenous expression pattern by using transgenic mice. We inserted a lacZ reporter gene into the first exon of the Dlx3 gene by using homologous recombination in yeast. Strong lacZ expression in embryonic (E) stage E9.5 and E10.5 mouse embryos was found in the limb buds and first and second visceral arches, consistent with the endogenous Dlx3 expression pattern. This result shows that the 79-kb region contains the major cis-elements required to direct the endogenous expression of Dlx3 at stage E10.5. To test for enhancer location, we divided the construct in the mid-intergenic region and injected the Dlx3 gene portion. This shortened fragment lacking Dlx7-flanking sequences is able to drive expression in the limb buds but not in the visceral arches. This observation is consistent with a cis-regulatory enhancer-sharing model within the Dlx bigene cluster.


Evolution & Development | 2006

Expression of Dlx genes during the development of the zebrafish pharyngeal dentition: evolutionary implications

Véronique Borday-Birraux; Christine Van der heyden; Mélanie Debiais-Thibaud; L. Verreijdt; David W. Stock; A. Huysseune; Jy Sire

SUMMARY In order to investigate similarities and differences in genetic control of development among teeth within and between species, we determined the expression pattern of all eight Dlx genes of the zebrafish during development of the pharyngeal dentition and compared these data with that reported for mouse molar tooth development. We found that (i) dlx1a and dlx6a are not expressed in teeth, in contrast to their murine orthologs, Dlx1 and Dlx6; (ii) the expression of the six other zebrafish Dlx genes overlaps in time and space, particularly during early morphogenesis; (iii) teeth in different locations and generations within the zebrafish dentition differ in the number of genes expressed; (iv) expression similarities and differences between zebrafish Dlx genes do not clearly follow phylogenetic and linkage relationships; and (v) similarities and differences exist in the expression of zebrafish and mouse Dlx orthologs. Taken together, these results indicate that the Dlx gene family, despite having been involved in vertebrate tooth development for over 400 million years, has undergone extensive diversification of expression of individual genes both within and between dentitions. The latter type of difference may reflect the highly specialized dentition of the mouse relative to that of the zebrafish, and/or genome duplication in the zebrafish lineage facilitating a redistribution of Dlx gene function during odontogenesis.


Evolution & Development | 2006

Conservation and divergence of Bmp2a, Bmp2b, and Bmp4 expression patterns within and between dentitions of teleost fishes

Sarah B. Wise; David W. Stock

SUMMARY The diversity of tooth location in teleost fishes provides an excellent system for comparing genetic divergence between teeth in different species (phylogenetic homologs) with divergence between teeth within one species (iterative homologs). We have chosen to examine the expression of three members of the bone morphogenetic protein (Bmp) family because they are known to play multiple roles in tooth development and evolution in tetrapod vertebrates. We characterized expression of Bmp2a, Bmp2b, and Bmp4 during the development of oral and pharyngeal dentitions in three species of teleost fishes, the zebrafish (Danio rerio), Mexican tetra (Astyanax mexicanus), and Japanese medaka (Oryzias latipes). We found that expression in teleosts is generally highly conserved, with minor differences found among both iteratively homologous and phylogenetically homologous teeth. Expression of orthologous genes differs in several ways between the teeth of teleost fishes and those of the mouse, but between these vertebrate groups the summed expression pattern of Bmp genes is highly conserved. Significantly, the toothless oral region of the zebrafish lacks Bmp expression domains found in teleosts with oral teeth, implicating these genes in evolutionary tooth loss. We conclude that Bmp expression has been largely conserved in vertebrate tooth development over evolutionary time, and that loss of Bmp expression is correlated with region‐specific loss of the dentition in a major group of fishes.


Proceedings of the National Academy of Sciences of the United States of America | 2006

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

William R. Jackman; David W. Stock

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.

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Kenneth M. Weiss

Pennsylvania State University

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Zhiyong Zhao

Pennsylvania State University

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Anne V. Buchanan

Pennsylvania State University

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Josh Trapani

University of Colorado Boulder

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Sarah B. Wise

University of Colorado Boulder

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