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超快巨细胞中的拓扑阻尼。

Topological damping in an ultrafast giant cell.

机构信息

Department of Bioengineering, Stanford University, Palo Alto, CA 94305.

Woods Institute for the Environment, Stanford University, Palo Alto, CA 94305.

出版信息

Proc Natl Acad Sci U S A. 2023 Oct 10;120(41):e2303940120. doi: 10.1073/pnas.2303940120. Epub 2023 Oct 4.


DOI:10.1073/pnas.2303940120
PMID:37792511
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC10576051/
Abstract

Cellular systems are known to exhibit some of the fastest movements in biology, but little is known as to how single cells can dissipate this energy rapidly and adapt to such large accelerations without disrupting internal architecture. To address this, we investigate -a giant cell (1-4 mm in length) well-known to exhibit ultrafast contractions (50% of body length) within 5 ms with a peak acceleration of 15[Formula: see text]. Utilizing transmitted electron microscopy and confocal imaging, we identify an association of rough endoplasmic reticulum (RER) and vacuoles throughout the cell-forming a contiguous fenestrated membrane architecture that topologically entangles these two organelles. A nearly uniform interorganelle spacing of 60 nm is observed between RER and vacuoles, closely packing the entire cell. Inspired by the entangled organelle structure, we study the mechanical properties of entangled deformable particles using a vertex-based model, with all simulation parameters matching 10 dimensionless numbers to ensure dynamic similarity. We demonstrate how entangled deformable particles respond to external loads by an increased viscosity against squeezing and help preserve spatial relationships. Because this enhanced damping arises from the entanglement of two networks incurring a strain-induced jamming transition at subcritical volume fractions, which is demonstrated through the spatial correlation of velocity direction, we term this phenomenon "topological damping." Our findings suggest a mechanical role of RER-vacuolar meshwork as a metamaterial capable of damping an ultrafast contraction event.

摘要

细胞系统以其在生物学中最快的运动速度而闻名,但对于单个细胞如何能够迅速消耗这种能量并适应如此大的加速度而不破坏内部结构,人们知之甚少。为了解决这个问题,我们研究了一种巨型细胞(长度为 1-4 毫米),这种细胞以在 5 毫秒内以 15[Formula: see text]的速度进行超快收缩(身体长度的 50%)而闻名。利用透射电子显微镜和共聚焦成像,我们发现内质网(RER)和液泡在整个细胞中形成连续的有窗孔的膜结构,拓扑上使这两个细胞器缠结在一起。在 RER 和液泡之间观察到近 60nm 的几乎均匀的细胞器间隔,使整个细胞紧密排列。受缠结细胞器结构的启发,我们使用基于顶点的模型研究了缠结可变形粒子的力学特性,所有模拟参数与 10 个无量纲数匹配,以确保动力学相似性。我们展示了缠结可变形粒子如何通过增加对挤压的粘性来响应外部负载,并有助于保持空间关系。因为这种增强的阻尼来自于两个网络的缠结,在亚临界体积分数下会发生应变诱导的堵塞转变,这可以通过速度方向的空间相关性来证明,所以我们将这种现象称为“拓扑阻尼”。我们的研究结果表明,RER-液泡网格作为一种超材料,能够阻尼超快收缩事件,起到机械作用。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/be2085a4b0dc/pnas.2303940120fig06.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/f648f8c32070/pnas.2303940120fig01.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/03c2e9aa128f/pnas.2303940120fig02.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/911e73792723/pnas.2303940120fig03.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/0cbad0377d53/pnas.2303940120fig04.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/778853c095e4/pnas.2303940120fig05.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/be2085a4b0dc/pnas.2303940120fig06.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/f648f8c32070/pnas.2303940120fig01.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/03c2e9aa128f/pnas.2303940120fig02.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/911e73792723/pnas.2303940120fig03.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/0cbad0377d53/pnas.2303940120fig04.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/778853c095e4/pnas.2303940120fig05.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/c502/10576051/be2085a4b0dc/pnas.2303940120fig06.jpg

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本文引用的文献

[1]
Giant proteins in a giant cell: Molecular basis of ultrafast Ca-dependent cell contraction.

Sci Adv. 2023-2-22

[2]
Endoplasmic reticulum membranes are continuously required to maintain mitotic spindle size and forces.

Life Sci Alliance. 2023-1

[3]
Cell cycle regulation of ER membrane biogenesis protects against chromosome missegregation.

Dev Cell. 2021-12-20

[4]
The Nesprin-1/-2 ortholog ANC-1 regulates organelle positioning in independently from its KASH or actin-binding domains.

Elife. 2021-4-16

[5]
Transcriptome Profiling Revealed Multiple Genes in the Species of (Protozoa: Ciliophora: Heterotrichea).

Front Microbiol. 2021-1-5

[6]
Toughening mechanisms of the elytra of the diabolical ironclad beetle.

Nature. 2020-10

[7]
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Proc Natl Acad Sci U S A. 2020-8-17

[8]
Mechanical properties and energy absorption characteristics of tropical fruit durian (Durio zibethinus).

J Mech Behav Biomed Mater. 2020-4

[9]
Collective intercellular communication through ultra-fast hydrodynamic trigger waves.

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[10]
Topological Methods for Polymeric Materials: Characterizing the Relationship Between Polymer Entanglement and Viscoelasticity.

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