Laboratory for Physical Biology, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan; Institute of Biomaterials and Biomolecular Systems, University of Stuttgart, Stuttgart, Germany; Institute for Integrated Cell-Material Sciences, Kyoto University, Kyoto, Japan.
Laboratory for Physical Biology, RIKEN Center for Biosystems Dynamics Research, Kobe, Japan.
Biophys J. 2019 Jan 22;116(2):372-382. doi: 10.1016/j.bpj.2018.12.012. Epub 2018 Dec 20.
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 PtdInsP3 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 PtdInsP3 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.
磷脂酰肌醇（3-5）-三磷酸（PtdInsP3）已知在质膜上呈波状传播，与变形虫和哺乳动物细胞中的膜突起活性有关。尽管已经有一些尝试来研究这些过程的三维（3D）动力学，但大多数研究都集中在从单个焦平面提取的动力学上。然而，由于缺乏关于膜未观察部分的信号信息，膜动力学和 3D 细胞形状之间的关系仍然难以捉摸。在这里，我们表明 PtdInsP3 波动力学直接受质膜的 3D 几何形状（即大小和形状）的调节。通过引入一种分析方法，该方法提取整个细胞膜上的 3D 时空活性，我们表明 PtdInsP3 波在受限的膜区域内自我调节其动力学。这导致速度、方向和图案演化的变化，遵循信号转导系统的基本激活性。我们的发现强调了质膜拓扑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。
