Nano-mechanical signature of brain tumours

Ciasca, Gabriele; Sassun, Tanya Enny; Minelli, Eleonora; Antonelli, Manila; Papi, Massimiliano; Santoro, Antonio; Giangaspero, Felice; Delfini, Roberto; Spirito, Marco De

doi:10.1039/c6nr06840e

Cited by 80 publications

(83 citation statements)

References 73 publications

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“…Recent experimental evidence [15][16][17][18] have revealed that tumor cells exhibit a broad distribution of various biomechanical properties. These include intra-tumor heterogeneity in cell stiffnesses [17,[19][20][21][22], stresses, and cell-cell interactions [21,23]. However, there is no consensus on how these heterogeneities affect the mechanical behavior at the tissue level.…”

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confidence: 99%

Mechanical Heterogeneity in Tissues Promotes Rigidity and Controls Cellular Invasion

Das

2019

Phys. Rev. Lett.

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We study the influence of cell-level mechanical heterogeneity in epithelial tissues using a vertex-based model. Heterogeneity in single cell stiffness is introduced as a quenched random variable in the preferred shape index(p 0 ) for each cell. We uncovered a crossover scaling for the tissue shear modulus, suggesting that tissue collective rigidity is controlled by a single parameter f r , which accounts for the fraction of rigid cells. Interestingly, the rigidity onset occurs at f r = 0.21, far below the contact percolation threshold of rigid cells. Due to the separation of rigidity and contact percolations, heterogeneity can enhance tissue rigidity and gives rise to an intermediate solid state. The influence of heterogeneity on tumor invasion dynamics is also investigated. There is an overall impedance of invasion as the tissue becomes more rigid. Invasion can also occur in the intermediate heterogeneous solid state and is characterized by significant spatial-temporal intermittency.

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confidence: 99%

Mechanical Heterogeneity in Tissues Promotes Rigidity and Controls Cellular Invasion

Das

2019

Phys. Rev. Lett.

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“…This makes standard experimental probes probing the average structure inadequate for the visualization of this heterogeneity, requiring highly spatially resolved probes. Biological tissues are typically intrinsically heterogeneous; indeed, nowadays new features and properties have been visualized using scanning methods with high spatial resolutions, such as by Atomic Force Microscopy [38][39][40], Confocal Microscopy [40], Scanning Electron Microscopy [35] and Scanning micro X-ray diffraction [15][16][17][18][19][20][21]. Correlated spatial structural fluctuations in biological systems have been correlated with the emergence of quantum coherence in biological matter [35,41], in photosystems [42] and intrinsically disordered proteins [43,44], as well as in lamellar oxides showing quantum coherence [45][46][47][48], where non-Euclidean spatial geometries for signal transmission are able to emerge from a correlated disorder [22,48].…”

Section: Discussionmentioning

confidence: 99%

Correlated Disorder in Myelinated Axons Orientational Geometry and Structure

et al. 2017

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While the ultrastructure of myelin is considered a quasi-crystalline stable system, nowadays its multiscale complex dynamics appear to play a key role in its functionality, degeneration and repair processes following neurological diseases and trauma. In this work, we investigated the fluctuation of the myelin supramolecular assembly by measuring the spatial distribution of orientation fluctuations of axons in a Xenopus Laevis sciatic nerve associated with nerve functionality. To this end, we used scanning micro X-ray diffraction (SµXRD), a non-invasive technique that has already been applied to other heterogeneous systems presenting complex geometries from microscale to nanoscale. We found that the orientation of the spatial fluctuations of fresh axons show a Levy flight distribution, which is a clear indication of correlated disorder. We found that the Levy flight distribution was missing in the aged nerve prepared in an unfresh state. This result shows that the spatial distribution of axon orientation fluctuations in unfresh nerve state loses the correlated disorder and assumes a random disorder behavior. This work provides a deeper understanding of the ultrastructure-function nerve relation and paves the way for the study of other materials and biomaterials using the SµXRD technique to detect fluctuations in their supramolecular structure.

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“…Moreover, tumor microenvironments can include heterogeneous regions, from necrotic to non-necrotic ones, with various ECM composition and stiffness. This was demonstrated in recent works both with non-invasive magnetic resonance elastrography and by using atomic force microscopy (AFM) nanoindentation (Ciasca et al, 2016;Pepin et al, 2018).…”

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confidence: 88%

Hyaluronan‐based hydrogels as versatile tumor‐like models: Tunable ECM and stiffness with genipin‐crosslinking

Bonnesœur

Morin-Grognet

Thoumire

et al. 2020

J Biomedical Materials Res

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Three‐dimensional (3D) biomimetic cell culture platforms offer more realistic microenvironments that cells naturally experience in vivo. We developed a tunable hyaluronan‐based hydrogels that could easily be modified to mimic healthy or malignant extracellular matrices (ECMs). For that, we pre‐functionalized our hydrogels with an adhesive polypeptide (poly‐l‐lysine, PLL) or ECM proteins (type III and type IV collagens), naturally present in tumorous tissues, and next, we tuned their stiffness by crosslinking with gradual concentrations of genipin (GnP). Then, we thoroughly characterized our substrates before testing them with glioblastoma and breast cancer cells, and thereafter with endothelial cells. Overall, our hydrogels exhibited (a) increasing stiffness with GnP concentration for every pre‐functionalization and (b) efficient enzyme resistance with PLL treatment, and also with type IV collagen but to a lesser extent. While PLL‐treated hydrogels were not favorable to the culture of any glioblastoma cell lines, they enhanced the proliferation of breast cancer cells in a stiffness‐dependent manner. Contrary to type III collagen, type IV collagen pre‐treated hydrogels supported the proliferation of glioblastoma cells. The as‐desired HA‐based 3D tumor‐like models we developed may provide a useful platform for the study of various cancer cells by simply tuning their biochemical composition and their mechanical properties.

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Nano-mechanical signature of brain tumours

Cited by 80 publications

References 73 publications

Mechanical Heterogeneity in Tissues Promotes Rigidity and Controls Cellular Invasion

Mechanical Heterogeneity in Tissues Promotes Rigidity and Controls Cellular Invasion

Correlated Disorder in Myelinated Axons Orientational Geometry and Structure

Hyaluronan‐based hydrogels as versatile tumor‐like models: Tunable ECM and stiffness with genipin‐crosslinking

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