Fluid shear stress facilitates prostate cancer metastasis through Piezo1-Src-YAP axis

Kim, Ok-Hyeon; Choi, Young Wook; Hong, Soon Auck; Hong, Min Eui; Chang, In Ho; Lee, Hyun Jung

doi:10.1016/j.lfs.2022.120936

Cited by 31 publications

(18 citation statements)

References 40 publications

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“…This was done to ensure that the assay was sensitive enough in the various shear stress scenarios and to investigate the role and importance of cell-to-cell signaling in NLRP3 inflammasome activation. A more widely studied example of this is cell-to-cell interactions between circulating cells and resident cells, as is the case in tumor extravasation, which is more widely studied when investigating the effect of shear stress on the ability of tumor cells to extravasate and metastasize to other organs. ,− However, the cell-to-cell signaling cascade in the context of NLRP3 inflammasome activation due to shear stress has not been widely studied and will provide important insights into how these mechanisms are affected by the NLRP3 inflammasome activation pathway. One study investigated the effect of pannexins, a group of gap-junction proteins that can form intercellular channels, on cell-to-cell communication and determined that pannexin1 can be open due to mechanical stress, such as shear stress, applied to cells and are active at physiological extracellular concentrations of calcium ions creating channels that are conducive to cell-to-cell communication. − Pannexin 1 facilitates the transport of extracellular calcium ions and mediates the release of ATP, indicating that it has a clear involvement in NLRP3 inflammasome activation and the subsequent secretion of IL-1β. ,− This indicates that shear stress has the potential to be conducive to increased cell-to-cell communication under conditions of inflammasome activation.…”

Section: Resultsmentioning

confidence: 99%

Flow-Induced Shear Stress Primes NLRP3 Inflammasome Activation in Macrophages via Piezo1

Fish,

Kulkarni

2024

ACS Appl. Mater. Interfaces

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The NLRP3 inflammasome is a crucial component of the innate immune system, playing a pivotal role in initiating and regulating the body's inflammatory response to various pathogens and cellular damage. Environmental stimuli, such as temperature, pH level, and nutrient availability, can influence the behavior and functions of innate immune cells, including immune cell activity, proliferation, and cytokine production. However, there is limited understanding regarding how mechanical forces, like shear stress, govern the intrinsic inflammatory reaction, particularly the activation of the NLRP3 inflammasome, and how shear stress impacts NLRP3 inflammasome activation through its capacity to induce alterations in gene expression and cytokine secretion. Here, we investigated how shear stress can act as a priming signal in NLRP3 inflammasome activation by exposing immortalized bone marrow-derived macrophages (iBMDMs) to numerous physiologically relevant magnitudes of shear stress before chemically inducing inflammasome activation. We demonstrated that shear stress of large magnitudes was able to prime iBMDMs more effectively for inflammasome activation compared to lower shear stress magnitudes, as quantified by the percentage of cells where ASC-CFP specks formed and IL-1β secretion, the hallmarks of inflammasome activation. Testing this in NLRP3 and caspase-1 knockout iBMDMs showed that the NLRP3 inflammasome was primarily primed for activation due to shear stress exposure. Quantitative polymerase chain reaction (qPCR) and a small-molecule inhibitor study mechanistically determined that shear stress regulates the NLRP3 inflammasome by upregulating Piezo1, IKKβ, and NLRP3. These findings offer insights into the mechanistic relationship among physiological shear stresses, inflammasome activation, and their impact on the progression of inflammatory diseases and their interconnected pathogenesis.

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Section: Resultsmentioning

confidence: 99%

Flow-Induced Shear Stress Primes NLRP3 Inflammasome Activation in Macrophages via Piezo1

Fish,

Kulkarni

2024

ACS Appl. Mater. Interfaces

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“…YAP, known as sensors and mediators of mechanical cues, regulates various aspects of cell behavior, including proliferation, differentiation, and cancer malignant progression (42). Multiple evidences have shown that YAP, as a downstream of Piezo1, conducted mechanotransduction signaling for tumor progression and cardiac fibrosis (43)(44)(45). In addition, Santoro et al (24) revealed that matrix stiffness by two-dimensional poly-acrylamide gels activated YAP translocation to promote VIC differentiation.…”

Section: Discussionmentioning

confidence: 99%

Activation of Piezo1 promotes osteogenic differentiation of aortic valve interstitial cell through YAP-dependent glutaminolysis

Zhong

et al. 2023

Sci. Adv.

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Hemodynamic overload and dysregulation of cellular metabolism are involved in development of calcific aortic valve disease (CAVD). However, how mechanical stress relates to metabolic changes in CAVD remains unclear. Here, we show that Piezo1, a mechanosensitive ion channel, regulated glutaminase 1 (GLS1)–mediated glutaminolysis to promote osteogenic differentiation of valve interstitial cells (VICs). In vivo, two models of aortic valve stenosis were constructed by ascending aortic constriction (AAC) and direct wire injury (DWI). Inhibition of Piezo1 and GLS1 in these models respectively mitigated aortic valve lesion. In vitro, Piezo1 activation induced by Yoda1 and oscillatory stress triggered osteogenic responses in VICs, which were prevented by Piezo1 inhibition or knockdown. Mechanistically, Piezo1 activation promoted calcium-dependent Yes-associated protein (YAP) activation. YAP modulated GLS1-mediated glutaminolysis, which enhanced osteogenic differentiation through histone acetylation of runt-related transcription factor 2 (RUNX2) promoters. Together, our work provided a cross-talk between mechanotransduction and metabolism in the context of CAVD.

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“…However, the existence of LTS had a greater disruption of endothelial orientation than polarization. Shear stress-induced activation of mechanosensitive ion channels, such as Piezo1 [62], and clustering of mechanoreceptors, such as integrins [63,64], were highlighted in cancer metastasis. Additionally, we found that the cavity between an expanding tumor spheroid and the adjacent endothelium was significantly suppressed by shear stress as opposed to the static condition.…”

Section: Discussionmentioning

confidence: 99%

3D spheroid-microvasculature-on-a-chip for tumor-endothelium mechanobiology interplay

et al. 2023

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During the final stage of cancer metastasis, tumor cells embed themselves in distant capillary beds, from where they extravasate and establish secondary tumors. Recent findings underscore the pivotal roles of blood/lymphatic flow and shear stress in this intricate tumor extravasation process. Despite the increasing evidence, there is a dearth of systematic and biomechanical methodologies that accurately mimic intricate 3D microtissue interactions within a controlled hydrodynamic microenvironment. Addressing this gap, we introduce an easy-to-operate 3D Spheroid-Microvasculature-On-A-Chip (SMAC) model. Operating under both static and regulated flow conditions, the SMAC model facilitates the replication of the biomechanical interplay between heterogeneous tumor spheroids and endothelium in a quantitative manner. Serving as an in vitro model for metastasis mechanobiology, our model unveils the phenomena of 3D spheroid-induced endothelial compression and cell-cell junction degradation during tumor migration and expansion. Furthermore, we investigated the influence of shear stress on endothelial orientation, polarization, and tumor spheroid expansion. Collectively, our SMAC model provides a compact, cost-efficient, and adaptable platform for probing the mechanobiology of metastasis.

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Fluid shear stress facilitates prostate cancer metastasis through Piezo1-Src-YAP axis

Cited by 31 publications

References 40 publications

Flow-Induced Shear Stress Primes NLRP3 Inflammasome Activation in Macrophages via Piezo1

Flow-Induced Shear Stress Primes NLRP3 Inflammasome Activation in Macrophages via Piezo1

Activation of Piezo1 promotes osteogenic differentiation of aortic valve interstitial cell through YAP-dependent glutaminolysis

3D spheroid-microvasculature-on-a-chip for tumor-endothelium mechanobiology interplay

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