Luu Ngoc, Zhang Shuhao, Lam Raymond H W, Chen Weiqiang
Department of Biomedical Engineering, New York University, Brooklyn, NY, USA.
Department of Mechanical and Aerospace Engineering, New York University, Brooklyn, NY, USA.
Mechanobiol Med. 2024 Mar;2(1). doi: 10.1016/j.mbm.2023.100027. Epub 2023 Oct 29.
The mechanical constraints in the overcrowding glioblastoma (GBM) microenvironment have been implicated in the regulation of tumor heterogeneity and disease progression. Especially, such mechanical cues can alter cellular DNA transcription and give rise to a subpopulation of tumor cells called cancer stem cells (CSCs). These CSCs with stem-like properties are critical drivers of tumorigenesis, metastasis, and treatment resistance. Yet, the biophysical and molecular machinery underlying the emergence of CSCs in tumor remained unexplored. This work employed a two-dimensional micropatterned multicellular model to examine the impact of mechanical constraints arisen from geometric confinement on the emergence and spatial patterning of CSCs in GBM tumor. Our study identified distinct spatial distributions of GBM CSCs in different geometric patterns, where CSCs mostly emerged in the peripheral regions. The spatial pattern of CSCs was found to correspond to the gradients of mechanical stresses resulted from the interplay between the cell-ECM and cell-cell interactions within the confined environment. Further mechanistic study highlighted a Piezo1-RhoA-focal adhesion signaling axis in regulating GBM cell mechanosensing and the subsequent CSC phenotypic transformation. These findings provide new insights into the biophysical origin of the unique spatial pattern of CSCs in GBM tumor and offer potential avenues for targeted therapeutic interventions.
胶质母细胞瘤(GBM)微环境过度拥挤中的机械约束与肿瘤异质性调节和疾病进展有关。特别是,这种机械信号可以改变细胞DNA转录,并产生一种称为癌症干细胞(CSCs)的肿瘤细胞亚群。这些具有干细胞样特性的CSCs是肿瘤发生、转移和治疗耐药性的关键驱动因素。然而,肿瘤中CSCs出现的生物物理和分子机制仍未得到探索。这项工作采用二维微图案化多细胞模型来研究几何限制产生的机械约束对GBM肿瘤中CSCs出现和空间模式的影响。我们的研究确定了GBM CSCs在不同几何图案中的不同空间分布,其中CSCs大多出现在周边区域。发现CSCs的空间模式与受限环境中细胞-细胞外基质和细胞-细胞相互作用之间相互作用产生的机械应力梯度相对应。进一步的机制研究强调了Piezo1-RhoA-粘着斑信号轴在调节GBM细胞机械传感和随后的CSC表型转化中的作用。这些发现为GBM肿瘤中CSCs独特空间模式的生物物理起源提供了新见解,并为靶向治疗干预提供了潜在途径。