journal article·2022-06Open access

Magneto-mechanical system to reproduce and quantify complex strain patterns in biological materials

Miguel Angel Moreno-Mateos, Jorge Gonzalez-Rico, Emanuel Nunez-Sardinha, Clara Gomez-Cruz, Maria Luisa Lopez-Donaire, Sergio Lucarini, Angel Arias, Arrate Muñoz-Barrutia, Diego Velasco, Daniel Garcia-Gonzalez

Abstract

Biological cells and tissues are continuously subjected to mechanical stress and strain cues from their surrounding substrate. How these forces modulate cell and tissue behavior is a major question in mechanobiology. To conduct studies under controlled varying physiological strain scenarios, a new virtually-assisted experimental system is proposed allowing for non-invasive and real-time control of complex deformation modes within the substrates. This approach is based on the use of extremely soft magneto-active polymers, which mimic the stiffness of biological materials. Thus, the system enables the untethered control of biological substrates providing reversible mechanical changes and controlling heterogeneous patterns. Motivated on a deep magneto-mechanical characterization across scales, a multi-physics and multi-scale in silico framework was developed to guide the experimental stimulation setup. The versatility and viability of the system have been demonstrated through its ability to reproduce complex mechanical scenarios simulating local strain patterns in brain tissue during a head impact, and its capability to transmit physiologically relevant mechanical forces to dermal fibroblasts. The proposed framework opens the way to understanding the mechanobiological processes that occur during complex and dynamic deformation states, e.g., in traumatic brain injury, pathological skin scarring or fibrotic heart remodeling during myocardial infarction.
Source: openalex_inverted_index · Quality: baseline

Research context

OpenAlex topics: Cellular Mechanics and Interactions · Elasticity and Material Modeling · Electrospun Nanofibers in Biomedical Applications

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (67)

Show source-provided references
1. Effects of extracellular matrix viscoelasticity on cellular behaviour10.1038/s41586-020-2612-2 ↗
2. Action potential alterations induced by single F11 neuronal cell loading10.1016/j.pbiomolbio.2020.12.003 ↗
3. Extracellular matrix plasticity as a driver of cell spreading10.1073/pnas.2008801117 ↗
4. Preventing Engrailed-1 activation in fibroblasts yields wound regeneration without scarring10.1126/science.aba2374 ↗
5. Physical models of collective cell migration10.1146/annurev-conmatphys-031218-013516 ↗
6. Dorsoventral polarity directs cell responses to migration track geometries10.1126/sciadv.aba6505 ↗
7. Engineering a uniaxial substrate-stretching device for simultaneous electrophysiological measurements and imaging of strained peripheral neurons10.1016/j.medengphy.2019.02.014 ↗
8. High stretchability, strength, and toughness of living cells enabled by hyperelastic vimentin intermediate filaments10.1073/pnas.1903890116 ↗
9. Functional polymer surfaces for controlling cell behaviors10.1016/j.mattod.2017.07.002 ↗
10. Sensitive detection of cell-derived force and collagen matrix tension in microtissues undergoing large-scale densification10.1073/pnas.2106061118 ↗
11. Structural and mechanical remodeling of the cytoskeleton maintains tensional homeostasis in 3D microtissues under acute dynamic stretch10.1038/s41598-020-64725-7 ↗
12. Force-mediated cellular anisotropy and plasticity dictate the elongation dynamics of embryos10.1126/sciadv.abg3264 ↗
13. Extracellular matrix anisotropy is determined by TFAP2C-dependent regulation of cell collisions10.1038/s41563-019-0504-3 ↗
14. Stress fiber anisotropy contributes to force-mode dependent chromatin stretching and gene upregulation in living cells10.1038/s41467-020-18584-5 ↗
15. Elastic Anisotropy governs the range of cell-induced displacements10.1016/j.bpj.2019.12.033 ↗
16. Concussion, microvascular injury, and early tauopathy in young athletes after impact head injury and an impact concussion mouse model10.1093/brain/awx350 ↗
17. Cognition based bTBI mechanistic criteria; a tool for preventive and therapeutic innovations10.1038/s41598-018-28271-7 ↗
18. Glial tissue mechanics and mechanosensing by glial cells10.3389/fncel.2018.00025 ↗
19. Measuring mechanical stress in living tissues10.1038/s42254-020-0184-6 ↗
20. How tissue mechanical properties affect enteric neural crest cell migration
21. Tissue stiffening coordinates morphogenesis by triggering collective cell migration in vivo10.1038/nature25742 ↗
22. Integrating chemical and mechanical signals in neural crest cell migration10.1016/j.gde.2019.06.004 ↗
23. Campo A del. 4D hydrogel for dynamic cell culture with orthogonal, wavelength-dependent mechanical and biochemical cues10.1039/C9MH00665F ↗
24. Ultra-soft PDMS-based magnetoactive elastomers as dynamic cell culture substrata10.1371/journal.pone.0076196 ↗
25. Tunable and reversible substrate stiffness reveals a dynamic mechanosensitivity of cardiomyocytes10.1021/acsami.9b02446 ↗
26. Engineered extracellular matrices with integrated wireless microactuators to study mechanobiology10.1002/adma.202102641 ↗
27. Soft-bodied adaptive multimodal locomotion strategies in fluid-filled confined spaces10.1126/sciadv.abh2022 ↗
28. Permanent magnet array–driven navigation of wireless millirobots inside soft tissues10.1126/sciadv.abi8932 ↗
29. Wirelessly actuated thermo- and magneto-responsive soft bimorph materials with programmable shape-morphing
30. A review on magneto-mechanical characterizations of magnetorheological elastomers10.1016/j.compositesb.2020.108348 ↗
31. Ncorr: open-source 2D digital image correlation matlab software10.1007/s11340-015-0009-1 ↗
32. Magneto-diffusion-viscohyperelasticity for magneto-active hydrogels: Rate dependences across time scales10.1016/j.jmps.2020.103934 ↗
33. Experiments and numerical implementation of a boundary value problem involving a magnetorheological elastomer layer subjected to a nonuniform magnetic field10.1115/1.4050534 ↗
34. Modelling of iron-filled magneto-active polymers with a dispersed chain-like microstructure10.1016/j.euromechsol.2014.10.005 ↗
35. Numerical solution of some boundary value problems in nonlinear magneto-elasticity10.1177/1045389X14522533 ↗
36. An explicit dissipative model for isotropic hard magnetorheological elastomers10.1016/j.jmps.2021.104361 ↗
37. Wrinkling to crinkling transitions and curvature localization in a magnetoelastic film bonded to a non-magnetic substrate10.1016/j.jmps.2019.103734 ↗
38. Two-field surface pattern control via marginally stable magnetorheological elastomers10.1039/C7SM00996H ↗
39. Experiments and numerical implementation of a boundary value problem involving a magnetorheological elastomer layer subjected to a nonuniform magnetic field10.1115/1.4050534 ↗
40. Transforms and operators for directional bioimage analysis: a survey10.1007/978-3-319-28549-8_3 ↗
41. A computational framework for magnetically hard and soft viscoelastic magnetorheological elastomers10.1016/j.cma.2021.114500 ↗
42. New experimental insights into magneto-mechanical rate dependences of magnetorheological elastomers10.1016/j.compositesb.2021.109148 ↗
43. Influence of elastomeric matrix and particle volume fraction on the mechanical response of magneto-active polymers10.1016/j.compositesb.2021.108796 ↗
44. Shear force-based genetic screen reveals negative regulators of cell adhesion and protrusive activity10.1073/pnas.1616600114 ↗
45. Factors influencing the mechanical properties of soft elastomer substrates for traction force microscopy10.1007/s42558-020-00021-8 ↗
46. A microstructural-based approach to model magneto-viscoelastic materials at finite strains
47. Chain formation mechanism of magnetic particles in magnetorheological elastomers during pre-structure10.1016/j.jmmm.2020.167693 ↗
48. Preventing Engrailed-1 activation in fibroblasts yields wound regeneration without scarring10.1126/science.aba2374 ↗
49. In vivo estimates of axonal stretch and 3D brain deformation during mild head impact10.1016/j.brain.2020.100015 ↗
50. The myofibroblast: one function, multiple origins10.2353/ajpath.2007.070112 ↗
51. Mechanical stimulation induces rapid fibroblast proliferation and accelerates the early maturation of human skin substitutes
52. Role of boundary conditions in determining cell alignment in response to stretch10.1073/pnas.1715059115 ↗
53. Mechanically activated ion channel Piezo1 modulates macrophage polarization and stiffness sensing10.1038/s41467-021-23482-5 ↗
54. Passive myocardial mechanical properties: meaning, measurement, models10.1007/s12551-021-00838-1 ↗
55. Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis10.1152/ajpgi.00032.2007 ↗
56. Mechanotransduction and extracellular matrix homeostasis10.1038/nrm3896 ↗
57. Embryonic and induced pluripotent stem cells: understanding, creating, and exploiting the nano-niche for regenerative medicine10.1021/nn3037094 ↗
58. Mechanobiology of cell migration in the context of dynamic two-way cell–matrix interactions10.1016/j.jbiomech.2015.12.023 ↗
59. Computational insights into the influence of substrate stiffness on collective cell migration10.1016/j.eml.2020.100928 ↗
60. Collective cell durotaxis emerges from long-range intercellular force transmission10.1126/science.aaf7119 ↗
61. Modeling of anisotropic wound healing10.1016/j.jmps.2015.03.009 ↗
62. YAP-mediated mechanotransduction tunes the macrophage inflammatory response10.1126/sciadv.abb8471 ↗
63. Biointerface anisotropy modulates migration of breast cancer cell10.1016/j.colsurfb.2020.110973 ↗
64. Single-cell morphology encodes metastatic potential10.1126/sciadv.aaw6938 ↗
65. Magnetic living hydrogels for intestinal localization, retention, and diagnosis10.1002/adfm.202010918 ↗
66. The force loading rate drives cell mechanosensing through both reinforcement and cytoskeletal softening10.1038/s41467-021-24383-3 ↗
67. Enhanced substrate stress relaxation promotes filopodia-mediated cell migration10.1038/s41563-021-00981-w ↗