<i>Hoxd13</i> expression in the developing limbs of the short‐tailed fruit bat, <i>Carollia perspicillata</i>

Chen, Chih Hsin; Cretekos, Chris J.; Rasweiler, John J.; Behringer, Richard R.

doi:10.1111/j.1525-142x.2005.05015.x

Cited by 61 publications

(46 citation statements)

References 51 publications

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“…Such an approach is necessary due to the sensitivity of various digit morphologies to both the dose and quality of Hox gene functions delivered during fetal development Zakany and Duboule 2007). Variations in this quantitative regulation have been proposed to partially account for important morphological differences between mammalian digits (e.g., Chen et al 2005); hence, the understanding of this regulatory control may help explain what determines the various digital formulae of mammalian hands and feet.…”

Section: Hox Gene Regulation In Digits Genes and Development 353mentioning

confidence: 99%

Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness

Montavon¹,

Garrec²,

Kerszberg³

et al. 2008

Genes Dev.

142

174

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During the development of mammalian digits, clustered Hoxd genes are expressed following a collinear regulatory strategy, leading to both the growth of digits and their morphological identities. Because gene dosage is a key parameter in this system, we used a quantitative approach, associated with a collection of mutant stocks, to investigate the nature of the underlying regulatory mechanism(s). In parallel, we elaborated a mathematical model of quantitative collinearity, which was progressively challenged and validated by the experimental approach. This combined effort suggested a two-step mechanism, which involves initially the looping and recognition of the cluster by a complex including two enhancer sequences, followed by a second step of microscanning of genes located nearby. In this scenario, the respective rank of the genes, with respect to the 5 extremity of the cluster, is primordial, as well as different gene-specific affinities. This model accounts for the quantitative variations observed in our many mutant strains, and reveals the molecular constraint leading to thumbness; i.e., why a morphological difference must occur between the most anterior digit and the others. We also show that the same model applies to the collinear regulation of Hox genes during the emergence of external genitalia, though with some differences likely illustrating the distinct functionalities of these structures in adults.[Keywords: Limbs; genitals; regulatory landscapes; modeling, looping] Supplemental material is available at http://www.genesdev.org.

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Section: Hox Gene Regulation In Digits Genes and Development 353mentioning

confidence: 99%

Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness

Montavon¹,

Garrec²,

Kerszberg³

et al. 2008

Genes Dev.

142

174

View full text Add to dashboard Cite

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“…However, so far, targeted candidate gene approaches have identified only seven genes with differences in expression in bat forelimb compared with hindlimb and mouse limbs during development. Only two of these are transcription factors that may play an upstream and regulatory role for bat wing development [4][5][6][7][8][9]. Thus, the full complexity of the mechanism of bat wing evolution remains to be shown, and the key differentially expressed genes contributing to this unique morphology remain to be identified.…”

Section: Introductionmentioning

confidence: 99%

Unique expression patterns of multiple key genes associated with the evolution of mammalian flight

et al. 2014

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Bats are the only mammals capable of true flight. Critical adaptations for flight include a pair of dramatically elongated hands with broad wing membranes. To study the molecular mechanisms of bat wing evolution, we perform genomewide mRNA sequencing and in situ hybridization for embryonic bat limbs. We identify seven key genes that display unique expression patterns in embryonic bat wings and feet, compared with mouse fore- and hindlimbs. The expression of all 5′HoxD genes ( Hoxd9–13 ) and Tbx3 , six known crucial transcription factors for limb and digit development, is extremely high and prolonged in the elongating wing area. The expression of Fam5c , a tumour suppressor, in bat limbs is bat-specific and significantly high in all short digit regions (the thumb and foot digits). These results suggest multiple genetic changes occurred independently during the evolution of bat wings to elongate the hand digits, promote membrane growth and keep other digits short. Our findings also indicate that the evolution of limb morphology depends on the complex integration of multiple gene regulatory networks and biological processes that control digit formation and identity, chondrogenesis, and interdigital regression or retention.

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“…In particular, we show here that a very localized dosage effect can impact upon a single digit independently from the neighboring digits, a phenomenon that may underlie the development of those autopods where the shape and/or the length of digits are notoriously heterogeneous within the same handplate, as seen, e.g., in bat wings (31,32). Our work also suggests that any group 12 or 13 HOX protein may contribute to these processes, thus increasing the realm of possibilities for morphological variation to occur.…”

Section: Discussionmentioning

confidence: 98%

Reshuffling genomic landscapes to study the regulatory evolution of Hox gene clusters

Tschopp

Fraudeau

Béna³

et al. 2011

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

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The emergence of Vertebrata was accompanied by two rounds of whole-genome duplications. This enabled paralogous genes to acquire novel functions with high evolutionary potential, a process suggested to occur mostly by changes in gene regulation, rather than in protein sequences. In the case of Hox gene clusters, such duplications favored the appearance of distinct global regulations. To assess the impact of such "regulatory evolution" upon neofunctionalization, we developed PANTHERE (PAN-genomic Translocation for Heterologous Enhancer RE-shuffling) to bring the entire megabase-scale HoxD regulatory landscape in front of the HoxC gene cluster via a targeted translocation in vivo. At this chimeric locus, Hoxc genes could both interpret this foreign regulation and functionally substitute for their Hoxd counterparts. Our results emphasize the importance of evolving regulatory modules rather than their target genes in the process of neo-functionalization and offer a genetic tool to study the complexity of the vertebrate regulatory genome.genetics | limb development | global gene regulation | long-range enhancers | mouse genetics

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Hoxd13 expression in the developing limbs of the short‐tailed fruit bat, Carollia perspicillata

Cited by 61 publications

References 51 publications

Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness

Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness

Unique expression patterns of multiple key genes associated with the evolution of mammalian flight

Reshuffling genomic landscapes to study the regulatory evolution of Hox gene clusters

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