Claussen Nikolas H, Brauns Fridtjof, Shraiman Boris I
Department of Physics, University of California Santa Barbara, Santa Barbara, CA 93106.
Kavli Institute for Theoretical Physics, University of California Santa Barbara, Santa Barbara, CA 93106.
Proc Natl Acad Sci U S A. 2024 Oct;121(40):e2321928121. doi: 10.1073/pnas.2321928121. Epub 2024 Sep 27.
Convergent extension of epithelial tissue is a key motif of animal morphogenesis. On a coarse scale, cell motion resembles laminar fluid flow; yet in contrast to a fluid, epithelial cells adhere to each other and maintain the tissue layer under actively generated internal tension. To resolve this apparent paradox, we formulate a model in which tissue flow in the tension-dominated regime occurs through adiabatic remodeling of force balance in the network of adherens junctions. We propose that the slow dynamics within the manifold of force-balanced configurations is driven by positive feedback on myosin-generated cytoskeletal tension. Shifting force balance within a tension network causes active cell rearrangements (T1 transitions) resulting in net tissue deformation oriented by initial tension anisotropy. Strikingly, we find that the total extent of tissue deformation depends on the initial cellular packing order. T1s degrade this order so that tissue flow is self-limiting. We explain these findings by showing that coordination of T1s depends on coherence in local tension configurations, quantified by a geometric order parameter in tension space. Our model reproduces the salient tissue- and cell-scale features of germ band elongation during gastrulation, in particular the slowdown of tissue flow after approximately twofold elongation concomitant with a loss of order in tension configurations. This suggests local cell geometry contains morphogenetic information and yields experimentally testable predictions. Defining biologically controlled active tension dynamics on the manifold of force-balanced states may provide a general approach to the description of morphogenetic flow.
上皮组织的汇聚延伸是动物形态发生的一个关键模式。从宏观尺度来看，细胞运动类似于层流；然而与流体不同的是，上皮细胞相互黏附，并在主动产生的内部张力作用下维持组织层。为了解决这一明显的矛盾，我们构建了一个模型，其中在张力主导的状态下，组织流动是通过黏着连接网络中力平衡的绝热重塑来实现的。我们提出，力平衡构型流形内的缓慢动力学是由对肌球蛋白产生的细胞骨架张力的正反馈驱动的。张力网络内力平衡的改变会导致活跃的细胞重排（T1转变），从而产生由初始张力各向异性定向的净组织变形。令人惊讶的是，我们发现组织变形的总程度取决于初始细胞堆积顺序。T1转变会破坏这种顺序，从而使组织流动具有自我限制作用。我们通过表明T1转变的协调取决于局部张力构型的相干性来解释这些发现，这种相干性由张力空间中的一个几何序参量来量化。我们的模型再现了原肠胚形成过程中胚带伸长的显著组织和细胞尺度特征，特别是在伸长约两倍后组织流动的减缓以及张力构型中有序性的丧失。这表明局部细胞几何形状包含形态发生信息，并产生了可通过实验验证的预测。在力平衡状态流形上定义生物控制的主动张力动力学可能为描述形态发生流动提供一种通用方法。
