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Hindbrain neuropore tissue geometry determines asymmetric cell-mediated closure dynamics in mouse embryos [Developmental Biology]
Proceedings of the National Academy of Sciences of the United States of America ( IF 9.412 ) Pub Date : 2021-05-11 , DOI: 10.1073/pnas.2023163118
Eirini Maniou, Michael F. Staddon, Abigail R. Marshall, Nicholas D. E. Greene, Andrew J. Copp, Shiladitya Banerjee, Gabriel L. Galea

Gap closure is a common morphogenetic process. In mammals, failure to close the embryonic hindbrain neuropore (HNP) gap causes fatal anencephaly. We observed that surface ectoderm cells surrounding the mouse HNP assemble high-tension actomyosin purse strings at their leading edge and establish the initial contacts across the embryonic midline. Fibronectin and laminin are present, and tensin 1 accumulates in focal adhesion-like puncta at this leading edge. The HNP gap closes asymmetrically, faster from its rostral than caudal end, while maintaining an elongated aspect ratio. Cell-based physical modeling identifies two closure mechanisms sufficient to account for tissue-level HNP closure dynamics: purse-string contraction and directional cell motion implemented through active crawling. Combining both closure mechanisms hastens gap closure and produces a constant rate of gap shortening. Purse-string contraction reduces, whereas crawling increases gap aspect ratio, and their combination maintains it. Closure rate asymmetry can be explained by asymmetric embryo tissue geometry, namely a narrower rostral gap apex, whereas biomechanical tension inferred from laser ablation is equivalent at the gaps’ rostral and caudal closure points. At the cellular level, the physical model predicts rearrangements of cells at the HNP rostral and caudal extremes as the gap shortens. These behaviors are reproducibly live imaged in mouse embryos. Thus, mammalian embryos coordinate cellular- and tissue-level mechanics to achieve this critical gap closure event.



中文翻译:

后脑神经孔组织的几何形状决定了小鼠胚胎中不对称细胞介导的闭合动力学[发育生物学]

间隙闭合是常见的形态发生过程。在哺乳动物中,未能缩小胚胎后脑神经孔(HNP)间隙会导致致命的无脑。我们观察到,围绕小鼠HNP的表面外胚层细胞在其前缘组装了高压放线菌素钱包链,并在整个胚胎中线建立了初始接触。存在纤连蛋白和层粘连蛋白,并且张力蛋白1在该前缘积聚在粘着斑状点状。HNP间隙从尾端开始不对称闭合,比尾端快,同时保持延长的长宽比。基于细胞的物理建模确定了两种足以说明组织级HNP闭合动力学的闭合机制:荷包弦收缩和通过主动爬行实现的定向细胞运动。两种封闭机制的结合会加速间隙的闭合,并产生恒定的间隙缩短率。钱包字符串收缩减少,而爬行则增加间隙长宽比,并且它们的组合保持了它。闭合率的不对称性可以用不对称的胚胎组织几何形状来解释,即较窄的延髓缘间隙顶点,而从激光消融推断出的生物力学张力在间隙的延髓缘和尾部闭合点是等效的。在细胞水平上,物理模型预测随着间隙的缩短,HNP鼻端和尾端的细胞会发生重排。这些行为在小鼠胚胎中可复制地实时成像。因此,哺乳动物胚胎协调细胞和组织水平的机制,以实现这一关键的缺口关闭事件。而爬行会增加间隙的长宽比,并且它们的组合可以保持间隙长宽比。闭合率的不对称性可以用不对称的胚胎组织几何形状来解释,即较窄的延髓缘间隙顶点,而从激光消融推断出的生物力学张力在间隙的延髓缘和尾部闭合点是等效的。在细胞水平上,物理模型预测随着间隙的缩短,HNP鼻端和尾端的细胞会发生重排。这些行为在小鼠胚胎中可复制地实时成像。因此,哺乳动物胚胎协调细胞和组织水平的机制,以实现这一关键的缺口关闭事件。而爬行会增加间隙的长宽比,并且它们的组合可以保持间隙长宽比。闭合率的不对称性可以用不对称的胚胎组织几何形状来解释,即较窄的延髓缘间隙顶点,而从激光消融推断出的生物力学张力在间隙的延髓缘和尾部闭合点是等效的。在细胞水平上,物理模型预测随着间隙的缩短,HNP鼻端和尾端的细胞会发生重排。这些行为在小鼠胚胎中可复制地实时成像。因此,哺乳动物胚胎协调细胞和组织水平的机制,以实现这一关键的缺口关闭事件。而激光消融所推导的生物力学张力在缝隙的鼻尖和尾巴闭合点处是等效的。在细胞水平上,物理模型预测随着间隙的缩短,HNP鼻端和尾端的细胞会发生重排。这些行为在小鼠胚胎中可复制地实时成像。因此,哺乳动物胚胎协调细胞和组织水平的机制,以实现这一关键的缺口关闭事件。而激光消融所推导的生物力学张力在缝隙的鼻尖和尾巴闭合点处是等效的。在细胞水平上,物理模型预测随着间隙的缩短,HNP鼻端和尾端的细胞会发生重排。这些行为在小鼠胚胎中可复制地实时成像。因此,哺乳动物胚胎协调细胞和组织水平的机制,以实现这一关键的缺口关闭事件。

更新日期:2021-05-03
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