Three-Dimensional Cell Geometry Controls Excitable Membrane Signaling in Dictyostelium Cells

Three-Dimensional Cell Geometry Controls Excitable Membrane Signaling in Dictyostelium Cells
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DOI:
10.1016/j.bpj.2018.12.012
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发表时间:
2019-01-22
影响因子:
3.4
通讯作者:
Shibata, Tatsuo
Shibata, Tatsuo
中科院分区:
生物学3区
文献类型:
--
作者:
Hoerning, Marcel;Shibata, Tatsuo

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磷脂酰肌醇(3-5)-三磷酸(PtdInsP 3)是一种在细胞膜上以波的形式传播的蛋白质,它与网骨藻和哺乳动物细胞的膜扩散活性有关。虽然已经有一些尝试来研究这些过程的三维(3D)动力学,大多数研究都集中在从单个焦平面提取的动力学。然而,动态和3D细胞形状之间的关系仍然难以捉摸,因为缺乏关于膜的未观察部分的信号信息。在这里,我们表明PtdlnsP 3波动力学直接受3D几何形状(即,大小和形状)的质膜。通过引入一种分析方法,提取整个细胞膜上的3D时空活动,我们表明,PtdlnsP 3波自我调节其动态范围内的有限的膜区域。这导致速度,方向和模式演变的变化,信号转导系统的潜在兴奋性。我们的研究结果强调了质膜拓扑结构在反应扩散驱动的生物系统中的作用,并表明其在其他哺乳动物系统中的重要性。
Phosphatidylinositol (3-5)-trisphosphate (PtdInsP3) is known to propagate as waves on the plasma membrane and is related to the membrane-protrusive activities in Dictyostelium and mammalian cells. Although there have been a few attempts to study the three-dimensional (3D) dynamics of these processes, most studies have focused on the dynamics extracted from single focal planes. However, the relation between the dynamics and 3D cell shape remains elusive because of the lack of signaling information about the unobserved part of the membrane. Here, we show that PtdlnsP3 wave dynamics are directly regulated by the 3D geometry (i.e., size and shape) of the plasma membrane. By introducing an analysis method that extracts the 3D spatiotemporal activities on the entire cell membrane, we show that PtdlnsP3 waves self-regulate their dynamics within the confined membrane area. This leads to changes in speed, orientation, and pattern evolution, following the underlying excitability of the signal transduction system. Our findings emphasize the role of the plasma membrane topology in reaction-diffusion-driven biological systems and indicate its importance in other mammalian systems.