Myogenesis in the sea urchin embryo: the molecular fingerprint of the myoblast precursors.

Myogenesis in the sea urchin embryo: the molecular fingerprint of the myoblast precursors.
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DOI:
10.1186/2041-9139-4-33
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发表时间:
2013-12-02
期刊:
影响因子:
4.1
通讯作者:
Arnone MI
Arnone MI
中科院分区:
生物学2区
文献类型:
--
作者:
Andrikou C;Iovene E;Rizzo F;Oliveri P;Arnone MI

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在海胆幼虫中,食管周围纤维形成了中胚层起源的突出肌肉系统。尽管这种肌肉系统的形态和后来的发育已经得到了很好的描述,但人们对这些细胞的分子特征或其在早期胚胎中的精确起源知之甚少。作为一种无脊椎动物后口动物,与其他常用的肌肉发生模型系统相比,海胆与脊椎动物的关系更为密切,海胆填补了一个重要的系统发育空白,并为肌肉细胞发育的进化提供了独特的视角。在这里,我们利用几种肌源性转录调节因子和分化基因表达的高分辨率定位,全面描述了海胆幼虫食管环肌谱系的发育,从中胚层起源开始。少数成肌细胞双侧分布于原肠尖端的口腔植物侧,首次出现于原肠胚晚期。分化基因肌球蛋白重链、原肌球蛋白 I 和 II 以及调节基因 MyoD2、FoxF、FoxC、FoxL1、Myocardin、Twist 和 Tbx6 的表达可独特地识别这些细胞。有趣的是,进化上保守的生肌因子,如 Mef2、MyoR 和 Six1/2 并不在海胆成肌细胞中表达,而是在原肠尖端的其他中胚层区域中发现。这些领域的监管状态得到了详细描述。此外,使用基因表达的组合分析,我们跟踪了 FoxF/FoxC 阳性细胞从表达开始到原肠胚形成结束的发育过程。我们的数据使我们能够在原肠胚早期阶段构建非骨骼中胚层的完整图谱,其中特定的分子特征识别不同细胞类型的前体。其中,FoxY 结构域内的一小群细胞也表达 FoxC 和 SoxE,已被鉴定为可能的成肌细胞前体细胞。总之,这些数据支持肌源谱系的非常早期的原肠胚阶段分离。通过这一分析,我们能够精确定义海胆胚胎中食管环肌的调节和分化特征。我们的发现对于在分子水平上理解肌肉细胞谱系的发育进化具有重要意义。这里提供的数据表明,在较宽的系统发育距离内,肌源规范机制具有高度的保守性,但也揭示了基因共选择的明显案例。
In sea urchin larvae the circumesophageal fibers form a prominent muscle system of mesodermal origin. Although the morphology and later development of this muscle system has been well-described, little is known about the molecular signature of these cells or their precise origin in the early embryo. As an invertebrate deuterostome that is more closely related to the vertebrates than other commonly used model systems in myogenesis, the sea urchin fills an important phylogenetic gap and provides a unique perspective on the evolution of muscle cell development. Here, we present a comprehensive description of the development of the sea urchin larval circumesophageal muscle lineage beginning with its mesodermal origin using high-resolution localization of the expression of several myogenic transcriptional regulators and differentiation genes. A few myoblasts are bilaterally distributed at the oral vegetal side of the tip of the archenteron and first appear at the late gastrula stage. The expression of the differentiation genes Myosin Heavy Chain, Tropomyosin I and II, as well as the regulatory genes MyoD2, FoxF, FoxC, FoxL1, Myocardin, Twist, and Tbx6 uniquely identify these cells. Interestingly, evolutionarily conserved myogenic factors such as Mef2, MyoR and Six1/2 are not expressed in sea urchin myoblasts but are found in other mesodermal domains of the tip of the archenteron. The regulatory states of these domains were characterized in detail. Moreover, using a combinatorial analysis of gene expression we followed the development of the FoxF/FoxC positive cells from the onset of expression to the end of gastrulation. Our data allowed us to build a complete map of the Non-Skeletogenic Mesoderm at the very early gastrula stage, in which specific molecular signatures identify the precursors of different cell types. Among them, a small group of cells within the FoxY domain, which also express FoxC and SoxE, have been identified as plausible myoblast precursors. Together, these data support a very early gastrula stage segregation of the myogenic lineage. From this analysis, we are able to precisely define the regulatory and differentiation signatures of the circumesophageal muscle in the sea urchin embryo. Our findings have important implications in understanding the evolution of development of the muscle cell lineage at the molecular level. The data presented here suggest a high level of conservation of the myogenic specification mechanisms across wide phylogenetic distances, but also reveal clear cases of gene cooption.
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