Developing an ancient epithelial appendage: FGF signalling regulates early tail denticle formation in sharks.

Developing an ancient epithelial appendage: FGF signalling regulates early tail denticle formation in sharks.
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DOI:
10.1186/s13227-017-0071-0
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发表时间:
2017
期刊:
影响因子:
4.1
通讯作者:
Fraser GJ
Fraser GJ
中科院分区:
生物学2区
文献类型:
--
作者:
Cooper RL;Martin KJ;Rasch LJ;Fraser GJ

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脊椎动物的上皮附属物构成了一组不同的器官,包括表皮结构,如爬行动物的鳞片,鸟类的羽毛和哺乳动物的毛发。最近的研究提供了新的证据的同源性的外皮器官的发展,在整个Aluminotes,尽管他们不同的最终形态。这些结构从保守的分子信号中心发展而来,称为上皮基板。目前还不确定这种同源性是否延伸到脊椎动物的表皮器官之外,因为缺乏关于它们在基础脊椎动物中发育的知识。作为骨脊椎动物的古老姐妹谱系,现存的软骨鱼类非常适合测试这种同源性的系统发育深度。板鳃类(鲨鱼、鳐和鳐鱼)拥有坚硬的、矿化的上皮附属物,称为齿突,包括牙齿和皮肤鳞片。齿类是已知最古老的脊椎动物的皮肤附属物,早于有颚类的起源。在这里,我们使用了一个新兴的模式鲨鱼(Scyliorhinus canicula)来测试的假设,denalpants同源的其他基板衍生的natroote外皮器官。为了研究假定的基因调控网络(GRN)成员功能的保守性,我们在尾侧齿状突形成过程中对成纤维细胞生长因子(FGF)信号进行了小分子抑制。我们发现,在早期的尾齿形态发生,鲨鱼表达的同源保守的发育基因家族,已知包括一个核心GRN早期基板形态发生在Escherotes。这包括FGF、音刺猬(shh)和骨形态发生蛋白4(bmp 4)的保守表达。此外,我们发现,齿状基板具有柱状上皮细胞的增殖率降低,一个保守的特点,denticle皮肤附件的发展。FGF信号的小分子抑制显示基板发育是FGF依赖性的,抑制FGF活性导致shh和bmp 4表达下调,与胎盘外皮附件GRN相比的预期一致。总的来说,这些发现表明,用于构建脊椎动物表皮上皮附属物的核心GRN在4.5亿年中一直高度保守。这为从鲨鱼到哺乳动物的所有有颌脊椎动物的上皮附器基板的连续的、历史的同源性提供了证据。上皮基板构成了不同脊椎动物表皮器官进化的共同基础。本文的在线版本(doi:10.1186/s13227-017-0071-0)包含补充材料,可供授权用户使用。
Vertebrate epithelial appendages constitute a diverse group of organs that includes integumentary structures such as reptilian scales, avian feathers and mammalian hair. Recent studies have provided new evidence for the homology of integumentary organ development throughout amniotes, despite their disparate final morphologies. These structures develop from conserved molecular signalling centres, known as epithelial placodes. It is not yet certain whether this homology extends beyond the integumentary organs of amniotes, as there is a lack of knowledge regarding their development in basal vertebrates. As the ancient sister lineage of bony vertebrates, extant chondrichthyans are well suited to testing the phylogenetic depth of this homology. Elasmobranchs (sharks, skates and rays) possess hard, mineralised epithelial appendages called odontodes, which include teeth and dermal denticles (placoid scales). Odontodes constitute some of the oldest known vertebrate integumentary appendages, predating the origin of gnathostomes. Here, we used an emerging model shark (Scyliorhinus canicula) to test the hypothesis that denticles are homologous to other placode-derived amniote integumentary organs. To examine the conservation of putative gene regulatory network (GRN) member function, we undertook small molecule inhibition of fibroblast growth factor (FGF) signalling during caudal denticle formation. We show that during early caudal denticle morphogenesis, the shark expresses homologues of conserved developmental gene families, known to comprise a core GRN for early placode morphogenesis in amniotes. This includes conserved expression of FGFs, sonic hedgehog (shh) and bone morphogenetic protein 4 (bmp4). Additionally, we reveal that denticle placodes possess columnar epithelial cells with a reduced rate of proliferation, a conserved characteristic of amniote skin appendage development. Small molecule inhibition of FGF signalling revealed placode development is FGF dependent, and inhibiting FGF activity resulted in downregulation of shh and bmp4 expression, consistent with the expectation from comparison to the amniote integumentary appendage GRN. Overall, these findings suggest the core GRN for building vertebrate integumentary epithelial appendages has been highly conserved over 450 million years. This provides evidence for the continuous, historical homology of epithelial appendage placodes throughout jawed vertebrates, from sharks to mammals. Epithelial placodes constitute the shared foundation upon which diverse vertebrate integumentary organs have evolved. The online version of this article (doi:10.1186/s13227-017-0071-0) contains supplementary material, which is available to authorized users.