Developmental Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany; Collaboration for joint Ph.D. degree between EMBL and Heidelberg University, Faculty of Biosciences 69117 Heidelberg, Germany.
Genome Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.
Curr Biol. 2024 Jan 22;34(2):361-375.e9. doi: 10.1016/j.cub.2023.12.021. Epub 2024 Jan 4.
A hallmark of animals is the coordination of whole-body movement. Neurons and muscles are central to this, yet coordinated movements also exist in sponges that lack these cell types. Sponges are sessile animals with a complex canal system for filter-feeding. They undergo whole-body movements resembling "contractions" that lead to canal closure and water expulsion. Here, we combine live 3D optical coherence microscopy, pharmacology, and functional proteomics to elucidate the sequence and detail of shape changes, the tissues and molecular physiology involved, and the control of these movements. Morphometric analysis and targeted perturbation suggest that the movement is driven by the relaxation of actomyosin stress fibers in epithelial canal cells, which leads to whole-body deflation via collapse of the incurrent and expansion of the excurrent canal system. Thermal proteome profiling and quantitative phosphoproteomics confirm the control of cellular relaxation by an Akt/NO/PKG/PKA pathway. Agitation-induced deflation leads to differential phosphorylation of proteins forming epithelial cell junctions, implying their mechanosensitive role. Unexpectedly, untargeted metabolomics detect a concomitant decrease in antioxidant molecules during deflation, reflecting an increase in reactive oxygen species. Together with the secretion of proteinases, cytokines, and granulin, this indicates an inflammation-like state of the deflating sponge reminiscent of vascular endothelial cells experiencing oscillatory shear stress. These results suggest the conservation of an ancient relaxant-inflammatory response of perturbed fluid-carrying systems in animals and offer a possible mechanism for whole-body coordination through diffusible paracrine signals and mechanotransduction.
动物的一个标志是全身运动的协调。神经元和肌肉是这方面的核心，但也存在于缺乏这些细胞类型的海绵中。海绵是具有用于过滤喂养的复杂管道系统的固着动物。它们会进行全身运动，类似于导致管道关闭和水排出的“收缩”。在这里，我们结合活体 3D 光学相干显微镜、药理学和功能蛋白质组学来阐明形状变化的顺序和细节、涉及的组织和分子生理学以及这些运动的控制。形态计量分析和靶向扰动表明，运动是由上皮管细胞中的肌动球蛋白应力纤维松弛驱动的，这导致整个身体通过传入通道系统的坍塌和传出通道系统的扩张而泄气。热蛋白质组图谱和定量磷酸化蛋白质组学证实了 Akt/NO/PKG/PKA 途径对细胞松弛的控制。搅动诱导的泄气导致形成上皮细胞连接的蛋白质的差异磷酸化，暗示其机械敏感性作用。出乎意料的是，非靶向代谢组学在泄气过程中检测到抗氧化分子同时减少，这反映了活性氧的增加。与蛋白酶、细胞因子和颗粒素的分泌一起，这表明泄气海绵处于类似于经历振荡剪切应力的血管内皮细胞的炎症样状态。这些结果表明，在动物中，扰动的流体输送系统的古老松弛-炎症反应得到了保守，并且通过可扩散的旁分泌信号和机械转导提供了全身协调的可能机制。
