Biomechanics of Collective Cell Migration in Cancer Progression: Experimental and Computational Methods

Spatarelu, Catalina-Paula; Zhang, Hao; Nguyen, Dung; Han, Xinyue; Liu, Ruchuan; Guo, Qiaohang; Notbohm, Jacob; Fan, Jing; Liu, Liyu; Chen, Zi

doi:10.1021/acsbiomaterials.8b01428

Cited by 39 publications

(33 citation statements)

References 200 publications

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“…Based on the migratory model, the migratory potential of highly invasive cells (MDA-MB-231) is in critical range and higher compared with invasive and non-invasive cells. As discussed earlier, invasive cells are assumed to be highly migratory and vice versa [20,23,[26][27][28][29][30], suggesting that our model could be also useful to predict the invasiveness of cells based on their bulk stiffness.…”

Section: Effects Of Substrate Elasticity On the Migratory Indexmentioning

confidence: 88%

“…In this range, as shown in the schematic (figure 8), under a constant internal force, not only the contractile force is effectively transmitted through cytoskeletal networks, but also cells have enough deformation, allowing cells to spread fast. Migration plays a central role in cancer progression and metastasis [20,[26][27][28][29], and based on the migratory index, it is thought that cancerous and invasive cells tend to possess a bulk stiffness in the critical range (between S1 and S2) at which they have the maximum migratory potential. This critical range is essential to interpret the behaviour of cells based on their cell mechanics; however, further detailed computational and experimental studies are required to determine the extent of the critical migratory index (S1 and S2).…”

Section: Migratory Index Of Normal Cells and Cancer Cellsmentioning

confidence: 99%

“…Open Sci. 7: 200747 [26][27][28][29][30]. For example, as mentioned earlier, under some treatments, the invasive ability of invasive cancers is reduced along with a reduction in their migratory ability [23,24].…”

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confidence: 96%

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Cancer cells optimize elasticity for efficient migration

Kashani

Packirisamy

2020

R. Soc. open sci.

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Cancer progression is associated with alternations in the cytoskeletal architecture of cells and, consequently, their mechanical properties such as stiffness. Changing the mechanics of cells enables cancer cells to migrate and invade to distant organ sites. This process, metastasis, is the main reason for cancer-related mortality. Cell migration is an essential step towards increasing the invasive potential of cells. Although many studies have shown that the migratory speed and the invasion of cells can be inversely correlated to the stiffness of cells, some other investigations indicate opposing results. In the current work, based on the strain energy stored in cells due to the contractile forces, we defined an energy-dependent term, migratory index, to approximate how changes in the mechanical properties of cells influence cell migration required for cancer progression. Cell migration involves both cell deformation and force transmission within cells. The effects of these two parameters can be represented equally by the migratory index. Our mechanical modelling and computational study show that cells depending on their shape, size and other physical parameters have a maximum migratory index taking place at a specific range of cell bulk elasticity, indicating the most favourable conditions for invasive mobility. This approximate model could be used to explain why the stiffness of cells varies during cancer progression. We believe that the stiffness of cancer or malignant cells depending on the stiffness of their normal or non-malignant counterparts is either decreased or increased to reach the critical condition in which the mobility potential of cells is approximated to be maximum.

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Section: Effects Of Substrate Elasticity On the Migratory Indexmentioning

confidence: 88%

Section: Migratory Index Of Normal Cells and Cancer Cellsmentioning

confidence: 99%

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Cancer cells optimize elasticity for efficient migration

Kashani

Packirisamy

2020

R. Soc. open sci.

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“…They recommend further investigation of mechanical assumptions in models, and of more realistic tissue size. A thorough review of the biomechanics of collective cell migration appears in [ 2 ], with a primary focus on cancer. In contrast with other reviews, this paper also provides an excellent summary of experimental methods.…”

Section: Introductionmentioning

confidence: 99%

Bridging from single to collective cell migration: A review of models and links to experiments

Buttenschön

Edelstein‐Keshet

2020

PLoS Comput Biol

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Mathematical and computational models can assist in gaining an understanding of cell behavior at many levels of organization. Here, we review models in the literature that focus on eukaryotic cell motility at 3 size scales: intracellular signaling that regulates cell shape and movement, single cell motility, and collective cell behavior from a few cells to tissues. We survey recent literature to summarize distinct computational methods (phase-field, polygonal, Cellular Potts, and spherical cells). We discuss models that bridge between levels of organization, and describe levels of detail, both biochemical and geometric, included in the models. We also highlight links between models and experiments. We find that models that span the 3 levels are still in the minority.

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“…Evaluation of migration and invasion properties of target cells has been significant in understanding cell behavior during normal proliferation, immune responses, disease development, and cancer progression. 1 − 3 Using this approach, researchers have been able to test the regulatory and stimulatory factors involved in the migration capacity of cells with genome reconstitution or transformation. Traditionally, modified Boyden chamber assays, Transwell insert migration assays, and wound closure assays have been frequently conducted to demonstrate the migratory behavior derived from regulatory signals or other stimuli.…”

Section: Introductionmentioning

confidence: 99%

Nonspectroscopic Migratory Cell Monitoring Method Using Retroreflective Janus Microparticles

et al. 2020

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This study aims to suggest a simple migratory cell monitoring method in the Transwell system by utilizing retroreflective Janus microparticles (RJPs) as an optical probe. The RJP could be internalized on cells without compromising the cell viability and can be registered as bright spots within the cell body by inducing retroreflection from nonspectroscopic light sources. Conventional optical probes (e.g., fluorophores, chromogens, and nanoparticles) have been extensively studied and applied across diverse platforms (e.g., Boyden chamber, wound closing, and microfluidic chips) for understanding in vitro kinetic cell behavior. However, the complexities of running such platforms and setting up analytical instruments are limiting. In this regard, we aimed to demonstrate a modified Transwell migration assay by introducing the retroreflection principle to the cell quantification procedures that ensure a simplified optical setup, assure easy signal acquisition, and are compatible with conventional platforms. To demonstrate retroreflection as a signaling principle, a half-metal-coated silica particle that can induce interior retroreflection was synthesized. Because the RJPs can concentrate incident light and reflect it back to the light source, retroreflection was distinctively recognizable and enabled sensitive visualization. To verify the applicability of the developed migration assay, cell quantification during the incremental progress of macrophage migration, and cell quantification under gradients of chemoattractant monocyte protein-1, was accomplished by obtaining phagocytosed RJP-mediated retroreflection signals. Considering that conventional assays are designed as endpoint measurements, we anticipate the proposed retroreflection-based cell quantification technique to be a promising solution, bypassing current limitations.

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Biomechanics of Collective Cell Migration in Cancer Progression: Experimental and Computational Methods

Cited by 39 publications

References 200 publications

Cancer cells optimize elasticity for efficient migration

Cancer cells optimize elasticity for efficient migration

Bridging from single to collective cell migration: A review of models and links to experiments

Nonspectroscopic Migratory Cell Monitoring Method Using Retroreflective Janus Microparticles

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