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摘要: 细胞膜是细胞与外部环境进行物质与能量交换的界面, 是调节细胞正常生命活动的重要结构基础. 细胞膜上力敏感受体可通过力学作用方式参与并影响细胞的力信号转导等功能. 整合素和钙黏素是细胞膜上典型的力敏感受体, 可介导细胞与细胞周围基质或邻近细胞发生力学作用, 并将力学刺激信号转导为生化信号, 进而激活细胞内一系列应答反应, 最终影响细胞生长、分化、增殖、凋亡和迁移等功能. 力敏感受体介导细胞功能调控研究已成为探索细胞主动响应外界复杂力学微环境的力学生物学机制的关键, 为进一步深入认识生理和病理状态下细胞功能变化规律, 为揭示疾病的发生、发展机制提供重要的力学生物学理论与实验依据. 本文总结了力敏感受体介导细胞功能调控的国内外研究进展; 介绍了黏附界面处典型力敏感受体的结构和功能; 总结了这些力敏感受体参与的细胞力信号感知与响应的数理模型; 概述了细胞通过力敏感受体进行力学信号转导的过程; 介绍了黏附介导细胞功能调控的力学生物学过程和机制; 简述了体外构建模拟细胞力学微环境中细胞−细胞外基质和细胞−细胞力学相互作用的技术; 指出了力敏感受体介导细胞功能调控的力学生物学研究发展趋势和未来方向.Abstract: As the interface between cells and their external environment for materials and energy exchange, the cell membrane is an important structure that regulates cellular activities. Representative transmembrane force-sensitive receptors, such as integrins and cadherins, are found to play key roles in mediating cellular interactions with the ECM or adjacent cells. These interactions will then transduce mechanical stimuli into biochemical signals, which in turn activate a series of intracellular signaling cascade, and ultimately affect cell growth, differentiation, proliferation, migration and apoptosis etc. The investigation of cellular mechanobiology regulated by force-sensitive adhesion receptors has thus become the key to explore the mechanobiological mechanisms of cellular actively in response to complex mechanical microenvironments. This provides valuable theoretical and experimental basis for further understanding of the changes in cell functions under physiological and pathological conditions, as well as for revealing the mechanism of disease development. This review summarizes the cutting-edge progresses in cellular mechanobiology regulated force-sensitive adhesion receptors. This review begins by introducing the structure and function of force-sensitive receptors at the adhesion interface, and followed by elaborating systematic mathematical models of how cells sense and respond to mechanical signals mediated by these receptors. It also outlines the processes of mechanical signal transduction through force-sensitive receptors, and the mechanobiological mechanism of adhesion-mediated changes in cell functions. In addition, the techniques for constructing of in vitro mechanical microenvironment that mimic cell-ECM (via integrin ligation) and cell-cell (via cadherin ligation) interactions are described. Finally, we identify the future directions of mechanobiology in terms of force-sensitive receptors regulated cell functions.
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图 3 整合素和钙黏素介导的黏附相互作用之间的串扰(Barcelona-Estaje et al. 2021)
图 4 整合素-配体结合的LSM模型示意图(Paszek et al. 2009). (a) Cell-ECM界面. 整合素和配体分别分布在代表细胞膜和ECM的两平板表面; (b) 格子弹簧模型 (LSM) , 整合素-配体键由弹簧连接来表示; (c) 形成1,2,3个整合素-配体键引起的膜变形云图, 插图为对应的俯视图; 当更多的键形成时, 膜与ECM表面将更为接近
图 5 整合素聚集与力致解离模型(Cheng et al. 2020). (a) 细胞膜上的整合素聚集动力学, 整合素具有激活/失活两种状态. 踝蛋白头部域可促进整合素的激活, 激活的整合素可以通过PI(4,5)P2或整合素跨膜区域产生聚集, (b) 整合素聚集的二维空间蒙特卡洛模型, 考虑了整合素在质膜上的激活和失活、扩散和聚集, (c) 整合素可以结合胞外ECM和细胞内基于肌球蛋白的类肌节收缩单位(CUs), (d) 将整合素聚集体所黏附的ECM建模为弹簧, 将整合素聚集体-ECM的力学作用建模为CU在位移边界条件下拉伸的逆锁/滑移键为滑移键断裂速率;
$ {k}_{b} $ (s−1) 为逆锁键断裂速率;$ {F}_{a} $ (pN) 为滑移键特征断裂力;$ {F}_{b} $ (pN) 为逆锁键特征断裂力. 在较低的分子键张力范围内 (小于20 pN) , 逆锁键占主导地位, 解离速率随力的增加而降低; 而在较大的分子键张力范围内 (大于25 pN) , 滑移键占主导地位, 解离速率随力的增加而增加
图 6 黏着斑各向异性生长的线性弹簧链模型. (a) 黏着斑(FAs)的结构示意图. 上层、中层、下层分别为相连的应力纤维, 蛋白斑块以及力敏感的斑块蛋白与整合素结合体(Besser & Safran 2006), (b) 一维黏附弹簧链模型(Nicolas et al. 2004). 力敏蛋白与ECM的锚定连接用正弦势函数V(x)表示, 锚点之间的距离a (nm) 为整合素间距, un (nm) 为第n个粒子在无力情况下的位移
图 7 二维黏附分子模型示意图(Walcott et al. 2011). 每个分子可以与其相邻分子形成四个横向键, 可以通过柔性域与表面结合, 并且可以以两种状态存在
图 8 整合素聚集过程的4种状态示意图(Peng et al. 2012). 用蓝色、绿色、红色的实心圆分别表示未激活、激活但未结合配体和已结合配体的整合素分子; 左图为俯视图, 箭头所指为自由的整合素分子可能扩散的位置, 而已结合的整合素则固定在原位; 右图为整合素在聚集过程中的4种状态, 聚集的整合素由踝蛋白 (紫色短线) 连接
图 9 基质/核刚度调节黏着斑尺寸的力-化耦合模型(Cao et al. 2015). (a) 细胞-ECM黏附示意图, (b) ECM&黏着斑-肌球蛋白-细胞核结构的简化模型
图 10 黏着斑的微观结构示意图(Kong et al. 2010). 整合素的内部结构域通过衔接蛋白(如黏着斑蛋白和踝蛋白)黏附在肌动蛋白应力纤维上, 而外部结构域与配体结合, 在细胞和基质之间形成整合素-配体分子键. 虚线矩形表示与相关衔接蛋白结合的整合素, 将其整体建模为整合素复合单元(ICU); 右上为ICU与黏着斑的结合或分离示意图; 右下为整合素-配体键的形成和断裂示意图
图 11 在倾斜牵拉应力作用下, 两种不同弹性介质间黏附分子键的周期性排列示意图(Qian et al. 2008)
图 12 细胞黏附复合物的纳米尺度结构(Xia & Kanchanawong 2017)
图 13 Motor-Clutch模型. (a) 弹性基质上黏附细胞的刚度感知机制示意图模型(Chan & Odde 2008). 肌球蛋白马达以相当的速度和力将肌动蛋白丝 (F-actin) 拉向左侧 (细胞中心) ; Clutch可逆地与肌动蛋白丝结合/解离, 以抑制向细胞中心方向的回退流, (b) 细胞迁移模型的示意图(Bangasser et al. 2017). 用“Motor-Clutch”模块来等效细胞伪足的功能, 多个模块共同作用以实现迁移行为
图 14 考虑黏附增强的“Motor-Clutch”模型(Elosegui-Artola et al. 2016). (a)当Clutch以速率
$ {k}_{\mathrm{o}\mathrm{n}} $ (s−1) 与基质结合, 随着肌球蛋白收缩, 力逐渐加载到踝蛋白, 打开了其隐藏的黏着斑蛋白结合位点, 并导致其招募黏着斑蛋白, 从而实现黏附增强, (b)顶部为踝蛋白结构是否解折叠而决定两种力-刚度关系的机制示意图, 下部为对应的数据结果: 实验结果 (点) 与有/无踝蛋白展开的模型预测结果对比(实线); 蓝/红线表示有/无黏附增强时, 模型预测的牵张力-刚度关系
图 15 配体间距与黏附增强的Motor-Clutch模型(Oria et al. 2017). (a) 通过在每个Clutch中设置张力阈值来引入力学敏感性, 当分子键张力超过阈值时, 会触发进一步的整合素招募 (暗棕星) . 弹性基质由连接配体到基质的弹簧 (
$ {k}_{\mathrm{s}\mathrm{u}\mathrm{b}} $ , 黑色) 和相互连接的弹簧 ($ {k}_{\mathrm{l}\mathrm{i}\mathrm{n}\mathrm{k}} $ , 橙色) 表示, (b) 随着配体间距的减小, 每个独立分子键上的张力载荷也减小
图 16 ECM粘弹性对细胞行为的影响示意图(Gong et al. 2018)
图 17 基于Motor-Clutch的转录因子重定位模型(Zhang et al. 2021). 模型解释了HAVDI连接在MSCs中改变YAP核定位中的作用; HAVDI的连接 (N-钙黏素为基础的黏附连接) 扰乱了整合素的聚集, 降低了整合素与RGD结合的
$ {k}_{\mathrm{o}\mathrm{n}} $ (s−1) 值, 由此降低肌动蛋白丝中的$ {F}_{\mathrm{t}\mathrm{r}\mathrm{a}\mathrm{c}} $ (pN) , 导致粘弹性核的变形改变影响了核孔尺寸、YAP在核内外的转运速率, 最终导致在HAVDI/RGD基质上的YAP 核/质比改变
图 18 细胞在弹性或粘弹性基质上铺展的模型示意图(Chaudhuri et al. 2015a). 细胞前缘的肌动蛋白丝通过形成分子键的方式与基质结合, 这些分子键通过负载减缓了肌球蛋白马达驱动的肌动蛋白丝回退流; 将基质等效为由Hookean弹簧 (代表弹性基质) 或Burgers模型单元 (代表应力松弛的粘弹性基质) 连接的节点阵列
图 19 细胞铺展前缘的受力示意图(Craig et al. 2015). 肌动蛋白网络粘性力、黏着斑-基质牵张力与肌球蛋白收缩力之间的平衡, 其中肌球蛋白和黏附都以一定的速率与肌动蛋白网络相结合/分离
图 20 细胞迁移的模拟示意图(Stephanou et al. 2008). 细胞周围形成的各种黏附类型 (A: 黏附点; FX: 黏附复合物; FA: 黏着斑) . 只有黏着斑对计算单元的位移有贡献 (左) ; 细胞质心被拉向
$ {\theta }_{\mathrm{M}} $ 方向, 对应于锚定在相关黏附点上的纤维的最大牵引力; 向量r表示细胞质心从初始位置 (深灰色) 到最终位置 (浅灰色) 的位移.
图 21 细胞前缘突出动力学模型(Welf et al. 2013)
图 22 预测细胞集体趋硬性的广义Motor-Clutch模型(Sunyer et al. 2016). (a) 在模型中, 用连续的弹性体模拟单层相连的细胞, 并通过弹簧与基质连接, (b) (上)将每个黏着斑等效为“Clutch”以传递使基质变形的力; (下) 为保持力平衡, 基质中柔软一侧的变形更大(
$ {d}_{1} > {d}_{2} $ ), 使单层细胞整体表现为向较硬一侧的基质靠近 ($ {{d}_{\mathrm{C}\mathrm{M}}=d}_{1}-{d}_{2} $ )
图 23 通过Motor-Clutch模型动态调控正/负向趋硬行为的示意图(Isomursu et al. 2022). 在没有黏附强化 (d) 的情况下, Motor-Clutch模型预测牵张力和基质刚度 (a-c) 之间的双相关系
图 24 FAK磷酸化水平模型(Cheng et al. 2020). (a) 整合素和FAK分子的空间模拟示意图; FAK可在细胞质内自由扩散, 整合素聚集体固定在细胞膜上, (b) FAK可以被整合素聚集体中的整合素胞内结构域激活, (c) FAK与整合素簇的结合和分离分别由
$ {k}_{\mathrm{i}\mathrm{n}} $ (s−1) 和$ {k}_{\mathrm{o}\mathrm{u}\mathrm{t}} $ (s−1) 描述; 在整合素聚集体或细胞质中, FAK通过磷酸酶和张力素同源物 (PTEN) 的脱磷酸化而激活和失活, 分别用$ {k}_{\mathrm{e}+} $ (s−1) 和$ {k}_{\mathrm{e}-} $ (s−1) 来描述
图 25 细胞前缘突出的力-化耦合模型. (a) 信号反馈回路新生黏附和周转的速率取决于膜突出的速度 (v) , 形成速率取决于ECM的密度, Rac的激活进一步促进膜突出; 新生黏附的稳定被肌球蛋白介导的反馈加强, 而稳定的黏附可拮抗膜突出(Cirit et al. 2010), (b) 基于正反馈信号回路的前缘运动模型(Chandra et al. 2022); 新生黏附被分子键稳定, 并介导下游信号通路以激活肌球蛋白和促进肌动蛋白聚合
图 26 基质刚度和IL-1β介导的信号通路数学模型(Cheng et al. 2016)
图 27 经典钙黏素反式与顺式相互作用的结构示意图(Brasch et al. 2012). (a) 经典钙黏素的单体及反式二聚体的构象转换 (单体中仅展示2个结构域) . 钙黏素单体相互作用形成X-二聚体后经链交换成熟为S-二聚体, 小球表示结合的Ca2+，(b) 胞外结构形成顺式和跨外结构域的的黏附连接. 左为同侧钙黏素分子的胞外结构域 (EC1-5) ; 相邻的S-二聚体分子的EC1和EC2形成顺式界面连接 (中) , 与反式相互作用方向大致垂直; 顺式和反式相互作用的结合使粘连蛋白外域形成有序的网络 (右) , 是钙黏素实现跨膜连接的基础
图 28 钙黏素二维晶格模型示意图(Wu et al. 2010). (a) 两种相互作用的钙黏素胞外区域结构示意图. 绿色为下层膜中的钙黏素分子, 红色为上层膜的钙黏素, EC1结构域由实心椭圆标记; 如果相邻的EC1结构域形成反式二聚体, 则标记为实蓝色. 空心椭圆表示EC2-EC5结构域, (b) 二维方格显示了所有EC1结构域 (偶极子/单体) 相互作用的俯视图.每个晶格只能容纳最多一个的上层膜单体(红色偶极子)或下层膜单体(绿色偶极子); 当格子被夹角为90°的两单体 (蓝色实心圆) 占据时, 代表反式二聚体形成
图 29 二维膜空间中钙黏素形成二聚体过程的示意图(Wu et al. 2011). (a) 分子只能在二维空间内自由扩散, 旋转运动受到限制. 钙黏素五个细胞外区域以椭球形表示, 反式二聚体(蓝色)由两个相邻细胞表面的两个钙黏素单体形成, (b) EC1域的转动自由度由三个欧拉角
$\phi{(^\circ)}$ ,$\theta{(^\circ)}$ 和$\psi{(^\circ)}$ 表征
图 30 基于RB方法(Xie et al. 2014)的钙黏素分子聚集模拟示意图(Chen et al. 2016). (a) 每个钙黏素都被简化为一个刚性圆柱. 细胞界面由2个相互重叠的平面表示. 每个圆柱的顶部有1个反式结合位点, 两侧有2个顺式结合位点, (b) 钙黏素反式和顺式二聚体的各向异性排列形成二维超分子结构簇, (c) 采用扩散-反应算法进行的空间动力学模拟
图 31 E-钙黏素分子状态转变的计算模型示意图(Chen et al. 2021). (a) 三维计算域示意图, 两个内表面代表相邻细胞的细胞膜, 两个外表面代表肌动球蛋白细胞骨架, (b) 参与状态转换计算的蛋白分子示意图, (c) E-钙黏素分子状态转换的动力学示意图
图 32 钙黏素二聚体状态的调控机制示意图(Hong et al. 2011). (a) 溶液中的钙黏素二聚体不受牵张力的调节, 在X-和链交换模式之间自由转转, (b) 已形成细胞-细胞黏附连接的二聚体不能在两种模式间自由转换
图 33 E-钙黏素突变体力依赖性的键寿命(Priest et al. 2017). (a) S-二聚体形成滑移键, 寿命随力的增加而迅速下降, (b) X-二聚体形成逆锁-滑移键, 在临界张力之前, 键寿命随力增加, (c) 野生型E-钙黏素形成与力无关的理想键
图 34 双态逆锁键动力学模型(Buckley et al. 2014). 状态1和状态2分别是弱结合态和强结合态, 状态0为未结合状态 (左) ; 状态1和状态2之间的转化以速率k12 (s−1) 和k21 (s−1) 发生, 这些转换不会发生在独立结合态模型中(右)
图 35 外力引起的钙黏素-连环蛋白-肌动蛋白复合物的构象变化(Adhikari et al. 2018). (a) 相关蛋白的晶体结构组合图, (b) αE-连环蛋白的M区域, 较小的力下有利于M2和M3区域之间呈现小角度α的构象, (c) 与b对应, 更大的力易于促成大角度的构象, 引起FABD-肌动蛋白相互作用的增强, 最终导致逆锁键行为
图 36 E-钙黏素介导的黏附初期信号回路模型(Perez et al. 2008)
图 37 钙黏素黏附与Wnt信号通路相互作用(Chen et al. 2014). (a) 网络模型的整体示意图. 3个模块由正常和激活的β-连环蛋白连接 (仅后者可激活基因表达) , 数字表示Wnt信号与细胞黏附之间的串话, (b) Cad/Cat复合物通过多个步骤形成黏附连接
图 38 NMII-RhoA双稳态信号网络模型(Priya et al. 2015). (a) 上皮细胞黏附带的稳定的Rho区域示意图, (b) 双稳态信号网络模型的结构及结算结果; 图中信号分子处的箭头和T形接头代表连接招募的刺激和抑制
图 39 肌球蛋白驱动肌动蛋白的收缩、解聚和重组装示意图. (a) 肌动蛋白丝的运动驱动肌动蛋白网络的收缩(Clark et al. 2007), (b) 肌球蛋白Ⅱ会刺激肌动蛋白网络的解聚与重新组装(Sonal et al. 2018)
图 41 细胞-ECM界面分子键断裂动力学(Cheng et al. 2016)
图 42 ECM-核机械耦合使 YAP 易位以响应基质刚度(Elosegui-Artola et al. 2017)
图 43 黏附介导的细胞极化(Ladoux et al. 2016)
图 44 细胞迁移过程(Sun, Guo et al. 2016)
图 46 钙黏素介导的黏附调控细胞力学感知(Cosgrove et al. 2016)
图 48 整合素α5β1的表达影响胰腺癌的进展(Kuninty et al. 2019). (a)胰腺癌组织中整合素α5β1的高表达与5年生存率下降相关; (b)整合素α5β1的敲除可以显著抑制胰腺星状细胞的功能, 抑制胰腺肿瘤体积的增长
图 50 CAF通过和癌细胞间的黏附作用促进癌细胞迁移. (a-c) CAF和癌细胞共培养体系中标记蛋白染色结果(Richardson et al. 2018); (d-f) CAF和癌细胞之间存在黏附作用(Labernadie et al. 2017); (d) CAF表达的N-钙黏素和癌细胞表达的E-钙黏素直接作用的染色结果; (e-f) CAF产生的牵引力的表征(紫色线表示CAF作用于癌细胞的牵引力的大小和方向); (g) CAF与癌细胞通过整合素/纤连蛋白力传导进行迁移示意图(Miyazaki et al. 2019); (h) 癌细胞和CAF共培养的实时检测结果显示肺癌细胞沿着CAF突起迁移(Miyazaki et al. 2019)
图 51 微环境中的各种生物力学因素诱导细胞命运(Romanazzo et al. 2020)
图 52 图案化的基质诱导细胞重编程示意图(Roy et al. 2018, Xu et al. 2014)
图 54 HAVDI与钙黏素受体重编程硬基质上已分化的间充质干细胞(Zhang et al. 2021)
图 55 24种整合类型及其对应的配体类型(Slack et al. 2022)
图 56 基于钙黏素的生物材料调控MSC行为(Zhang et al. 2020)
图 57 E-钙黏素表面修饰的材料用于间充质干细胞研究的示意图(Zhang et al. 2016)
图 58 RGD和HAVDI修饰的水凝胶黏附界面示意图(Zhang et al. 2021)
表 1 细胞-ECM界面的力敏感蛋白及功能
细胞-ECM 黏附界面的力敏感蛋白 结构 功能 整合素 (integrin) 介导细胞与ECM相互作用, 可以识别、结合ECM中相应的配体, 为细胞黏附提供附着点; 调整细胞骨架结构, 调节蛋白的磷酸化水平和基因表达, 从而调控细胞的运动增殖和凋亡. 踝蛋白(talin) 通过与多种黏着斑蛋白、细胞骨架蛋白及肌动蛋白丝相结合并相互作用, 参与细胞的力-化学信号转导; 在细胞黏附、伸展、运动、增殖、存活等过程中起重要作用. 黏着斑蛋白(vinculin) 激活整合素; 作为细胞骨架肌动蛋白结合蛋白在膜蛋白与细胞骨架结构的偶联以及信号转导中起到了非常重要的作用. 肌动蛋白丝(F-actin) 与肌球蛋白一起作用, 使细胞产生和传导机械力, 并促进细胞运动; 细胞形态维持、细胞运动等细胞基本生物学行为的调控. 
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表 2 细胞-细胞界面的力敏感蛋白及功能
细胞-细胞黏附界面的
力敏感蛋白结构 功能 钙黏素 (cadherin) 介导同型或异型细胞间的黏附相互作用; 与其他黏附蛋白共同形成黏附复合物, 与细胞骨架建立连接, 介导细胞-细胞力学信号转导, 进而调控细胞功能. β-连环蛋白
(β-catenin)作为黏附分子, 通过磷酸化调控与钙黏素结合形成功能复合体, 参与细胞间的黏附调节从而影响细胞的活动; 可以募集α-连环蛋白. α-连环蛋白
(α-catenin)作为力敏感蛋白, 受到力学刺激变为激活构型, 暴露出结合位点募集黏着斑蛋白, 进而激活下游信号分子; 调节钙黏素的功能, 其表达下调将影响细胞间黏附复合物的活性.
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