Dynamics and mechanical stability of the developing dorsoventral organizer of the wing imaginal disc.
Dynamics and mechanical stability of the developing dorsoventral organizer of the wing imaginal disc.
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DOI：
10.1371/journal.pcbi.1002153
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发表时间：
2011-09
影响因子：
4.3
通讯作者：
Buceta J
中科院分区：
文献类型：
--
作者：
Canela-Xandri O;Sagués F;Casademunt J;Buceta J
在发育过程中形成原基依赖于能够控制细胞分离的力量和机制。在果蝇的想象盘中，形成翅膀叶片背部和腹部的细胞群是分开的，不会混合。由背侧和腹侧细胞结构域的边界指定的细胞群体，即所谓的组织者，控制着这一过程。在本文中，我们研究了果蝇翅膀成像盘的背腹组织者在细胞增殖过程中的动力学和稳定性。我们的方法基于一个顶点模型来执行完全动态的电子实验，并考虑了可用的实验数据，如：细胞堆积属性，细胞分裂的方向，对膜消融的响应，以及对快速生长克隆引起的机械扰动的稳健性。我们的结果揭示了细胞骨架力学、细胞周期、细胞生长和细胞相互作用之间的复杂相互作用，以便将背腹组织者塑造为一个强大的位置信息源和谱系控制器。具体地说，我们阐明了增强其功能的必要和充分的成分：独特的机械性能，包括增加的张力，更长的细胞周期持续时间，以及满足赫特威格规则的切割标准。我们的结果为驱动DV组织者动态的发育机制提供了新的见解，并以定量的方式定义了所谓的缺口栅栏模型。在发育过程中，组织被塑造成具有特定功能的器官。这一过程依赖于控制细胞分离和迁移的机制。果蝇的想象盘在变态过程中经历的形态发生事件很好地说明了这些概念。具体地说，形成叶片背侧(D)和腹侧(V)部分的细胞群是分离的，不会混合。所谓的组织者，即由D和V细胞域的边界指定的细胞群体，对此负责。然而，DV组织者如何有力地处理细胞生长，以防止细胞混合？此外，随着组织的生长，组织者如何方便地进行缩放？在这里，我们使用一种计算方法来解决这些问题，该方法考虑了可用的实验数据。因此，我们的研究揭示了以定量和可预测的方式理解强健生长的DV组织者的动力学、结构和稳定性所必需的和充分的元素：细胞的独特机械属性、细胞周期持续时间的差异和明确的切割标准。
Shaping the primordia during development relies on forces and mechanisms able to control cell segregation. In the imaginal discs of Drosophila the cellular populations that will give rise to the dorsal and ventral parts on the wing blade are segregated and do not intermingle. A cellular population that becomes specified by the boundary of the dorsal and ventral cellular domains, the so-called organizer, controls this process. In this paper we study the dynamics and stability of the dorsal-ventral organizer of the wing imaginal disc of Drosophila as cell proliferation advances. Our approach is based on a vertex model to perform in silico experiments that are fully dynamical and take into account the available experimental data such as: cell packing properties, orientation of the cellular divisions, response upon membrane ablation, and robustness to mechanical perturbations induced by fast growing clones. Our results shed light on the complex interplay between the cytoskeleton mechanics, the cell cycle, the cell growth, and the cellular interactions in order to shape the dorsal-ventral organizer as a robust source of positional information and a lineage controller. Specifically, we elucidate the necessary and sufficient ingredients that enforce its functionality: distinctive mechanical properties, including increased tension, longer cell cycle duration, and a cleavage criterion that satisfies the Hertwig rule. Our results provide novel insights into the developmental mechanisms that drive the dynamics of the DV organizer and set a definition of the so-called Notch fence model in quantitative terms. During development, tissues are shaped in order to form organs with specific functionalities. This process relies on mechanisms that control cell segregation and migration. These concepts are beautifully illustrated by the morphogenetic events that the imaginal discs of Drosophila undergo during metamorphosis. In particular, the cellular populations that will give rise to the dorsal (D) and ventral (V) parts on the wing blade are segregated and do not intermingle. The so-called organizer, a cellular population that becomes specified by the boundary of the D and V cellular domains, is responsible for this. Yet, how does the DV organizer robustly deal with the cellular growth in order to prevent cell mixing? Moreover, how can the organizer be conveniently scaled as the tissue grows? Herein we address these questions using a computational approach that takes into account the available experimental data. Thus, our study unveils the elements that are necessary and sufficient for understanding in a quantitative and predictive manner the dynamics, structure, and stability of a robust growing DV organizer: distinctive mechanical properties of cells, differences in cell cycle duration, and a well-defined cleavage criterion.
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