Identification of neural progenitor cells and their progeny reveals long distance migration in the developing octopus brain.
Identification of neural progenitor cells and their progeny reveals long distance migration in the developing octopus brain.
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DOI：
10.7554/elife.69161
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发表时间：
2021-08-24
期刊：
影响因子：
7.7
通讯作者：
Seuntjens E
中科院分区：
文献类型：
--
作者：
Deryckere A;Styfhals R;Elagoz AM;Maes GE;Seuntjens E
就神经元数量和丰富的行为输出而言，鲸足类进化出了与哺乳动物大脑相似的神经系统。头足类动物的大脑是如何发育的，目前只在形态学水平上进行了描述，而且还不清楚祖细胞位于何处，以及哪些分子因素驱动神经发生。利用组织学技术，我们定位章鱼胚胎分裂细胞，神经祖细胞和有丝分裂后神经元。我们的研究结果表明，一个重要的池的祖细胞，表达保守的bHLH转录因子achaete-scute或neurogenin，位于中央脑索外的侧唇附近的眼睛，这表明新形成的神经元迁移到索。随后的谱系追踪实验表明，祖细胞根据其在侧唇中的位置，为不同的叶产生神经元，类似于鱿鱼Doryteuthis pealeii。章鱼新生神经元长距离迁移的发现让人想起脊椎动物的神经发生，并表明这可能是大脑发育的基本策略。章鱼已经进化出了令人难以置信的巨大而复杂的神经系统，使它们能够执行令人印象深刻的行为，比如提前计划，导航和解决难题。普通章鱼（也称为普通章鱼）的神经系统包含超过5亿个神经细胞，称为神经元，与小型灵长类动物的数量相似。其中三分之二的细胞位于章鱼的手臂上，其余的细胞组成了位于眼睛之间的中央大脑。关于这个中央大脑在胚胎中是如何形成的，包括细胞的起源以及哪些分子因素促使它们成熟为成年细胞，我们知之甚少。为了帮助回答这些问题，Deryckere等人使用各种细胞染色和成像技术研究了章鱼在早期发育不同阶段的大脑。这些实验确定了一个重要的分裂细胞池，位于中央大脑外的一个称为“侧唇”的区域。在这些细胞中，已知在其他动物神经发育中发挥作用的基因是活跃的，这表明这些细胞还没有达到最终的成熟状态。相比之下，在生长最旺盛的时候，中枢大脑似乎不包含任何这些未成熟的细胞。为了进一步研究这一点，Deryckere等人使用荧光标记来跟踪发育过程中分裂细胞的后代。这揭示了侧唇中的细胞在迁移到它们在中枢脑中的目标区域之前具有特定的神经元命运。新成熟的神经元在脊椎动物的胚胎中也被证明可以长距离移动，这表明这种机制可能是构建大型复杂大脑的常见策略。虽然普通章鱼的神经系统与哺乳动物相当，但它们是从生命之树的一个非常遥远的分支进化而来的;事实上，它们最后的共同祖先是一种生活在大约6亿年前的蠕虫状动物。因此，研究普通章鱼的大脑，就像这里所做的那样，可以为复杂的神经系统（包括我们自己的神经系统）如何随着时间的推移而进化提供新的见解。
Cephalopods have evolved nervous systems that parallel the complexity of mammalian brains in terms of neuronal numbers and richness in behavioral output. How the cephalopod brain develops has only been described at the morphological level, and it remains unclear where the progenitor cells are located and what molecular factors drive neurogenesis. Using histological techniques, we located dividing cells, neural progenitors and postmitotic neurons in Octopus vulgaris embryos. Our results indicate that an important pool of progenitors, expressing the conserved bHLH transcription factors achaete-scute or neurogenin, is located outside the central brain cords in the lateral lips adjacent to the eyes, suggesting that newly formed neurons migrate into the cords. Lineage-tracing experiments then showed that progenitors, depending on their location in the lateral lips, generate neurons for the different lobes, similar to the squid Doryteuthis pealeii. The finding that octopus newborn neurons migrate over long distances is reminiscent of vertebrate neurogenesis and suggests it might be a fundamental strategy for large brain development. Octopuses have evolved incredibly large and complex nervous systems that allow them to perform impressive behaviors, like plan ahead, navigate and solve puzzles. The nervous system of the common octopus (also known as Octopus vulgaris) contains over half a billion nerves cells called neurons, similar to the number found in small primates. Two thirds of these cells reside in the octopuses’ arms, while the rest make-up a central brain that sits between their eyes. Very little is known about how this central brain forms in the embryo, including where the cells originate and which molecular factors drive their maturation in to adult cells. To help answer these questions, Deryckere et al. studied the brain of Octopus vulgaris at different stages of early development using various cell staining and imaging techniques. The experiments identified an important pool of dividing cells which sit in an area outside the central brain called the ‘lateral lips’. In these cells, genes known to play a role in neural development in other animals are active, indicating that the cells had not reached their final, mature state. In contrast, the central brain did not seem to contain any of these immature cells at the point when it was growing the most. To investigate this further, Deryckere et al. used fluorescent markers to track the progeny of the dividing cells during development. This revealed that cells in the lateral lips take on a specific neuronal fate before migrating to their target region in the central brain. Newly matured neurons have also been shown to travel large distances in the embryos of vertebrates, suggesting that this mechanism may be a common strategy for building large, complex brains. Although the nervous system of the common octopus is comparable to mammals, they evolved from a very distant branch of the tree of life; indeed, their last common ancestor was a worm-like animal that lived about 600 million years ago. Studying the brain of the common octopus, as done here, could therefore provide new insights into how complex nervous systems, including our own, evolved over time.