Emergence of tissue-like mechanics from fibrous networks confined by close-packed cells

Oosten, Anne S. G. van; Chen, Xingyu; Chin, LiKang; Cruz, Katrina; Patteson, Alison E.; Pogoda, Katarzyna; Shenoy, Vivek B.; Janmey, Paul A.

doi:10.1038/s41586-019-1516-5

Cited by 141 publications

(176 citation statements)

References 19 publications

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“…Albeit, across the 25-fold increase in strain rate, the materials stiffness increased only marginally. Additionally, we found that whole blood clots dissipate energy during the first loading-unloading cycle via Mullins effect 35 , which is possibly enhanced compared to pure fibrin by the inclusion of RBCs as classical filler particles 14,36 . This initial energy dissipation due to the Mullins effect is compounded through hysteresis, which we continued to observe during subsequent loading cycles, not just the first.…”

Section: Discussionmentioning

confidence: 86%

“…Lastly, red blood cells contribute to clot mechanics by filling space and re-distributing loads. Although their role is passive, recent work has demonstrated that they drastically transform the behavior of their host material 14 . Finally, driven by gradients in pore pressure, interstitial plasma permeates through the clot matrix and ostensibly contributes to its time-dependent behavior as it exchanges momentum with the surrounding matrix 15 .…”

Section: Introductionmentioning

confidence: 99%

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Toward understanding thrombus fracture: Dissipative phenomena of whole blood clots

Sugerman

Parekh

Rausch

2020

Preprint

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When thrombus fractures and breaks off it can occlude vital vessels such as those of the heart, lung, or brain. These thromboembolic conditions are responsible for 1 in 4 deaths world-wide. This problem is also of significant current interest as 1 in 3 COVID-19 intensive care patients exhibit thromboembolic complications. Thrombus resistance to fracture is driven by its intrinsic fracture toughness as well as other, non-surface-creating dissipative mechanisms. In our current work, we identify and quantify these latter mechanisms toward future studies that aim to delineate fracture from other forms of dissipation. To this end, we use an in vitro thrombus mimic system to produce whole blood clots and explore their dissipative mechanics under simple uniaxial extension, cyclic loading, and stress-relaxation. We found that whole blood clots exhibit Mullins effect, hysteresis, permanent set, strain-rate dependence, and nonlinear stress-relaxation. Interestingly, we found that performing these tests under dry or submerged conditions did not change our results. However, performing these tests under room temperature or body temperature conditions yielded differences. Overall, we have demonstrated that whole blood clots show several dissipative phenomena - similarly to hydrogels - that will be critical to our understanding of thrombus fracture.

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Section: Discussionmentioning

confidence: 86%

Section: Introductionmentioning

confidence: 99%

Toward understanding thrombus fracture: Dissipative phenomena of whole blood clots

Sugerman

Parekh

Rausch

2020

Preprint

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“…Recent work suggests that the interaction between collagen fibrous networks and the cells which adhere to them is critical in defining tissue mechanics. [ 10 ] Another important mechanical feature of collagen is that it is piezoelectric. None of these properties of collagen have been easy to mimic in engineered systems.…”

Section: Fibrosis From a Materials Perspectivementioning

confidence: 99%

“…For example, hyperelasticity of tissues has been observed with AFM and compression testing and changes with fibrosis progression–fibrotic tissues often display linearly elastic responses to strain while pre‐fibrotic tissues display nonlinearly elastic responses. [ 10,24 ] The viscoelasticity of tissues can be measured from the macro to microscale using stress relaxation tests, where a constant strain is applied and the relaxation or decrease in stress is measured over time. As stress decays, a characteristic relaxation time is obtained and the time it takes for the stress to relax to 50% of its peak value ( T 1/2 ) can be reported.…”

Section: Multiscale Mechanical Properties Of Tissuesmentioning

confidence: 99%

“…[ 7 ] Liver, like other soft tissues, undergoes compression stiffening, and this is dramatically increased in fibrosis. [ 10,17,24 ] To elucidate the role of ECM structure and organization and force dependent material properties (e.g., compression stiffening) on hepatocyte function and myofibroblast activation, new dynamic material systems (tunable compression stiffening hydrogels) and material fabrication strategies (e.g., electrospinning) could be combined to accurately address these questions. Additionally, to understand how small spatiotemporal changes in liver stiffness influence hepatocyte function and myofibroblast activation, new biomaterial systems should be developed where small changes (100 s of pascals) can be introduced in a spatiotemporal manner.…”

Section: Mechanical Changes and Pathogenesis Of Fibrosis Across Tissuesmentioning

confidence: 99%

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Engineered Biomaterial Platforms to Study Fibrosis

Davidson

Burdick

Wells

2020

Adv Healthcare Materials

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Many pathologic conditions lead to the development of tissue scarring and fibrosis, which are characterized by the accumulation of abnormal extracellular matrix (ECM) and changes in tissue mechanical properties. Cells within fibrotic tissues are exposed to dynamic microenvironments that may promote or prolong fibrosis, which makes it difficult to treat. Biomaterials have proved indispensable to better understand how cells sense their extracellular environment and are now being employed to study fibrosis in many tissues. As mechanical testing of tissues becomes more routine and biomaterial tools become more advanced, the impact of biophysical factors in fibrosis are beginning to be understood. Herein, fibrosis from a materials perspective is reviewed, including the role and mechanical properties of ECM components, the spatiotemporal mechanical changes that occur during fibrosis, current biomaterial systems to study fibrosis, and emerging biomaterial systems and tools that can further the understanding of fibrosis initiation and progression. This review concludes by highlighting considerations in promoting wide‐spread use of biomaterials for fibrosis investigations and by suggesting future in vivo studies that it is hoped will inspire the development of even more advanced biomaterial systems.

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Breast Tumor Cell Survival and Morphology in a Brain‐like Extracellular Matrix Depends on Matrix Composition and Mechanical Properties

Türker,

Andrade Mier,

Faber

et al. 2024

Advanced Biology

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Triple‐negative breast cancer (TNBC) is the most invasive type of breast cancer with high risk of brain metastasis. To better understand interactions between breast tumors with the brain extracellular matrix (ECM), a 3D cell culture model is implemented using a thiolated hyaluronic acid (HA‐SH) based hydrogel. The latter is used as HA represents a major component of brain ECM. Melt‐electrowritten (MEW) scaffolds of box‐ and triangular‐shaped polycaprolactone (PCL) micro‐fibers for hydrogel reinforcement are utilized. Two different molecular weight HA‐SH materials (230 and 420 kDa) are used with elastic moduli of 148 ± 34 Pa (soft) and 1274 ± 440 Pa (stiff). Both hydrogels demonstrate similar porosities. The different molecular weight of HA‐SH, however, significantly changes mechanical properties, e.g., stiffness, nonlinearity, and hysteresis. The breast tumor cell line MDA‐MB‐231 forms mainly multicellular aggregates in both HA‐SH hydrogels but sustains high viability (75%). Supplementation of HA‐SH hydrogels with ECM components does not affect gene expression but improves cell viability and impacts cellular distribution and morphology. The presence of other brain cell types further support numerous cell–cell interactions with tumor cells. In summary, the present 3D cell culture model represents a novel tool establishing a disease cell culture model in a systematic way.

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Emergence of tissue-like mechanics from fibrous networks confined by close-packed cells

Cited by 141 publications

References 19 publications

Toward understanding thrombus fracture: Dissipative phenomena of whole blood clots

Toward understanding thrombus fracture: Dissipative phenomena of whole blood clots

Engineered Biomaterial Platforms to Study Fibrosis

Breast Tumor Cell Survival and Morphology in a Brain‐like Extracellular Matrix Depends on Matrix Composition and Mechanical Properties

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