Dynamic control of head mesoderm patterning

Bothe, Ingo; Tenin, Gennadiy; Oseni, Adelola O.; Dietrich, Susanne

doi:10.1242/dev.062737

Cited by 61 publications

(88 citation statements)

References 77 publications

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“…to the heart- and tail bud-associated progenitor fields) [16]. This action is mediated by RAR/RXR heterodimers binding to a repressive DR2 RARE located upstream of the FGF8 gene [22, 23] that, in turn, activates CYP26 expression both anteriorly and posteriorly to limit the extent of RA activity [16, 24, 25]. In addition, the expression of CYP26A1 and CYP26B1 have been shown to be dependent on RA activity, thereby generating a CYP26 -controlled negative feedback loop in RA sensitive tissues to reduce the overall amount of available RA [9, 18, 26, 27].…”

Section: Introductionmentioning

confidence: 99%

Lineage-specific duplication of amphioxus retinoic acid degrading enzymes (CYP26) resulted in sub-functionalization of patterning and homeostatic roles

et al. 2017

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BackgroundDuring embryogenesis, tight regulation of retinoic acid (RA) availability is fundamental for normal development. In parallel to RA synthesis, a negative feedback loop controlled by RA catabolizing enzymes of the cytochrome P450 subfamily 26 (CYP26) is crucial. In vertebrates, the functions of the three CYP26 enzymes (CYP26A1, CYP26B1, and CYP26C1) have been well characterized. By contrast, outside vertebrates, little is known about CYP26 complements and their biological roles. In an effort to characterize the evolutionary diversification of RA catabolism, we studied the CYP26 genes of the cephalochordate amphioxus (Branchiostoma lanceolatum), a basal chordate with a vertebrate-like genome that has not undergone the massive, large-scale duplications of vertebrates.ResultsIn the present study, we found that amphioxus also possess three CYP26 genes (CYP26-1, CYP26-2, and CYP26-3) that are clustered in the genome and originated by lineage-specific duplication. The amphioxus CYP26 cluster thus represents a useful model to assess adaptive evolutionary changes of the RA signaling system following gene duplication. The characterization of amphioxus CYP26 expression, function, and regulation by RA signaling demonstrated that, despite the independent origins of CYP26 duplicates in amphioxus and vertebrates, they convergently assume two main roles during development: RA-dependent patterning and protection against fluctuations of RA levels. Our analysis suggested that in amphioxus RA-dependent patterning is sustained by CYP26-2, while RA homeostasis is mediated by CYP26-1 and CYP26-3. Furthermore, comparisons of the regulatory regions of CYP26 genes of different bilaterian animals indicated that a CYP26-driven negative feedback system was present in the last common ancestor of deuterostomes, but not in that of bilaterians.ConclusionsAltogether, this work reveals the evolutionary origins of the RA-dependent regulation of CYP26 genes and highlights convergent functions for CYP26 enzymes that originated by independent duplication events, hence establishing a novel selective mechanism for the genomic retention of gene duplicates.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0863-1) contains supplementary material, which is available to authorized users.

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Section: Introductionmentioning

confidence: 99%

Lineage-specific duplication of amphioxus retinoic acid degrading enzymes (CYP26) resulted in sub-functionalization of patterning and homeostatic roles

et al. 2017

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“…In these previous studies, the expression patterns of pax1/9 cognates were affected, corresponding to defects in the posterior pouches caused by the lack of RA (Wendling et al, 2000). Additionally, Tbx1 reportedly modulates the dynamics of RA signaling in the developing vertebrate head by regulating Cyp26 genes, which encode RA-degrading enzymes (Roberts et al, 2006;Bothe et al, 2011). Regarding the function of Fgf signaling in pouch formation, it has been shown that its inhibition causes complete loss of the pharyngeal pouches forming posterior to the second arch (Abu-Issa et al, 2002;Crump et al, 2004).…”

Section: Impact Of Pax1 On Pharyngeal Segmentation and Derivativesmentioning

confidence: 99%

Reiterative expression of pax1 directs pharyngeal pouch segmentation in medaka (Oryzias latipes)

et al. 2016

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A striking characteristic of vertebrate development is the pharyngeal arches, which are a series of bulges on the lateral surface of the head of vertebrate embryos. Although each pharyngeal arch is segmented by the reiterative formation of endodermal outpocketings called pharyngeal pouches, the molecular network underlying the reiterative pattern remains unclear. Here, we show that pax1 plays crucial roles in pouch segmentation in medaka (Oryzias latipes) embryos. Importantly, pax1 expression in the endoderm prefigures the location of the next pouch before the cells bud from the epithelium. TALEN-generated pax1 mutants did not form pharyngeal pouches posterior to the second arch. Segmental expression of tbx1 and fgf3, which play essential roles in pouch development, was almost nonexistent in the pharyngeal endoderm of pax1 mutants, with disturbance of the reiterative pattern of pax1 expression. These results suggest that pax1 plays a key role in generating the primary pattern for segmentation in the pharyngeal endoderm by regulating tbx1 and fgf3 expression. Our findings illustrate the crucial roles of pax1 in vertebrate pharyngeal segmentation and provide insights into the evolutionary origin of the deuterostome gill slit.

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“…Likewise, inhibition of FGF signaling using retinoic acid (RA) downregulated MyoR and Tbx1. Thus, low levels of RA promote FGF signaling and consequently MyoR and Tbx1 activation (Bothe, Tenin, Oseni, & Dietrich, 2011; Scheven von, Alvares, Mootoosamy, & Dietrich, 2006). FGF signaling has been found to be an important regulator of myogenesis in the limb.…”

Section: Fibroblast Growth Factor Signalingmentioning

confidence: 99%