Investigating cellular and molecular mechanisms of neurogenesis in Capitella teleta sheds light on the ancestor of Annelida.

IF 3.4 Q1 Agricultural and Biological Sciences
A Sur, A Renfro, P J Bergmann, N P Meyer
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引用次数: 0

Abstract

Background: Diverse architectures of nervous systems (NSs) such as a plexus in cnidarians or a more centralized nervous system (CNS) in insects and vertebrates are present across Metazoa, but it is unclear what selection pressures drove evolution and diversification of NSs. One underlying aspect of this diversity lies in the cellular and molecular mechanisms driving neurogenesis, i.e. generation of neurons from neural precursor cells (NPCs). In cnidarians, vertebrates, and arthropods, homologs of SoxB and bHLH proneural genes control different steps of neurogenesis, suggesting that some neurogenic mechanisms may be conserved. However, data are lacking for spiralian taxa.

Results: To that end, we characterized NPCs and their daughters at different stages of neurogenesis in the spiralian annelid Capitella teleta. We assessed cellular division patterns in the neuroectoderm using static and pulse-chase labeling with thymidine analogs (EdU and BrdU), which enabled identification of NPCs that underwent multiple rounds of division. Actively-dividing brain NPCs were found to be apically-localized, whereas actively-dividing NPCs for the ventral nerve cord (VNC) were found apically, basally, and closer to the ventral midline. We used lineage tracing to characterize the changing boundary of the trunk neuroectoderm. Finally, to start to generate a genetic hierarchy, we performed double-fluorescent in-situ hybridization (FISH) and single-FISH plus EdU labeling for neurogenic gene homologs. In the brain and VNC, Ct-soxB1 and Ct-neurogenin were expressed in a large proportion of apically-localized, EdU+ NPCs. In contrast, Ct-ash1 was expressed in a small subset of apically-localized, EdU+ NPCs and subsurface, EdU- cells, but not in Ct-neuroD+ or Ct-elav1+ cells, which also were subsurface.

Conclusions: Our data suggest a putative genetic hierarchy with Ct-soxB1 and Ct-neurogenin at the top, followed by Ct-ash1, then Ct-neuroD, and finally Ct-elav1. Comparison of our data with that from Platynereis dumerilii revealed expression of neurogenin homologs in proliferating NPCs in annelids, which appears different than the expression of vertebrate neurogenin homologs in cells that are exiting the cell cycle. Furthermore, differences between neurogenesis in the head versus trunk of C. teleta suggest that these two tissues may be independent developmental modules, possibly with differing evolutionary trajectories.

Abstract Image

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研究 Capitella teleta 神经发生的细胞和分子机制有助于了解无脊椎动物的祖先。
背景:神经系统(NSs)的结构多种多样,如网虫的神经丛或昆虫和脊椎动物的更中枢化的神经系统(CNS),这些结构存在于整个后生动物中,但目前还不清楚是什么选择压力推动了神经系统的进化和多样化。这种多样性的一个基本方面在于驱动神经发生(即从神经前体细胞生成神经元)的细胞和分子机制。在刺胞动物、脊椎动物和节肢动物中,SoxB 和 bHLH proneural 基因的同源物控制着神经发生的不同步骤,这表明某些神经发生机制可能是保守的。然而,目前还缺乏螺旋类群的相关数据:为此,我们描述了螺旋纲环带动物 Capitella teleta 在神经发生不同阶段的 NPCs 及其子代的特征。我们使用胸腺嘧啶类似物(EdU和BrdU)进行静态和脉冲追逐标记,评估了神经外胚层的细胞分裂模式,从而确定了经历多轮分裂的NPCs。发现活跃分裂的脑NPC位于顶部,而活跃分裂的腹侧神经索(VNC)NPC位于顶部、基部和更靠近腹侧中线的位置。我们利用系谱追踪来描述躯干神经外胚层边界变化的特征。最后,为了开始建立遗传层次结构,我们进行了双荧光原位杂交(FISH)和单荧光原位杂交加EdU标记,以寻找神经源基因同源物。在大脑和 VNC 中,Ct-soxB1 和 Ct-neurogenin 在大量顶部定位、EdU+的 NPC 中表达。相反,Ct-ash1在一小部分顶部定位、EdU+的NPC和表面下、EdU-的细胞中表达,但不在Ct-neuroD+或Ct-elav1+细胞中表达,这些细胞也是表面下细胞:我们的数据表明,Ct-soxB1和Ct-neurogenin是一个假定的遗传层次,其次是Ct-ash1,然后是Ct-neuroD,最后是Ct-elav1。 将我们的数据与Platynereis dumerilii的数据进行比较,发现环纹类动物增殖的NPC中有神经原蛋白同源物的表达,这似乎与脊椎动物神经原蛋白同源物在退出细胞周期的细胞中的表达不同。此外,C. teleta头部与躯干神经发生的差异表明,这两个组织可能是独立的发育模块,可能具有不同的进化轨迹。
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来源期刊
BMC Evolutionary Biology
BMC Evolutionary Biology 生物-进化生物学
CiteScore
5.80
自引率
0.00%
发文量
0
审稿时长
6 months
期刊介绍: BMC Evolutionary Biology is an open access, peer-reviewed journal that considers articles on all aspects of molecular and non-molecular evolution of all organisms, as well as phylogenetics and palaeontology.
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