Magnetic bioprinting: shaping initial tissue geometry and probing tissue mechanics
Source abstract
Abstract
Abstract Mechanical and geometric cues play a crucial role in vivo , regulating both morphogenetic processes and proper tissue function. This is particularly evident in skeletal muscle, where aligned architecture is essential for myogenesis and functional force generation. However, precisely engineering tissue geometry at both macroscopic and microscopic scales while simultaneously controlling internal mechanical forces remains a significant challenge. In this study, we introduce a magnetic tissue engineering platform based on a magnetic bioprinting technique, enabling control of biophysical cues that guide in vitro tissue organization. Applied here to skeletal muscle, this approach allows for the rapid fabrication of cohesive tissues in any desired shape using cells labeled with magnetic nanoparticles. Additionally, multiple cell types can be incorporated and spatially organized within the same construct through magnetic segregation. As the tissues tend to transition toward a spherical shape after a few days, their geometry was optimized to further enable magnetic actuation, including the ability to trap and maintain tissue shape over time. Furthermore, this magnetic platform facilitates the investigation of how tissue architecture influences mechanical properties, such as resistance to rupture. Overall, this study highlights the significant potential of magnetic bioprinting and stimulation for controlling tissue morphology and advancing biomechanical research.
Source: crossref · Quality: baseline
Research context
OpenAlex topics: 3D Printing in Biomedical Research · Micro and Nano Robotics · Cellular Mechanics and Interactions
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
Affiliations
Sorbonne University, PSL University
Funding
Institut Pierre-Gilles de Gennes · French Agence Nationale de la Recherche
References (83)
Show source-provided references
1. Geometric control of tissue morphogenesis. biochimica et biophysica acta (BBA)10.1016/j.bbamcr.2008.12.014 ↗
2. Geometry can provide long-range mechanical guidance for embryogenesis10.1371/journal.pcbi.1005443 ↗
3. Multiscale assembly for tissue engineering and regenerative medicine10.1016/j.tibtech.2015.02.003 ↗
4. Reconstituting organ-level lung functions on a chip10.1126/science.1188302 ↗
5. Emulating the chondrocyte microenvironment using multi-directional mechanical stimulation in a cartilage-on-chip10.1039/D1LC01069G ↗
6. Testis-on-chip platform to study ex vivo primate spermatogenesis and endocrine dynamics10.1016/j.ooc.2022.100023 ↗
7. 3D bioelectronic model of the human intestine10.1002/adbi.202000306 ↗
8. Construction of a multitubular perfusable kidney-on-chip for the study of renal diseases
9. An in vitro model of cancer invasion with heterogeneous ECM created with droplet microfluidics10.3389/fbioe.2023.1267021 ↗
10. A cell pre‐wrapping seeding technique for hydrogel‐based tubular organ‐on‐a‐chip10.1002/advs.202400970 ↗
11. Developing an advanced gut on chip model enabling the study of epithelial cell/fibroblast interactions10.1039/D0LC00672F ↗
12. A multitubular kidney-on-chip to decipher pathophysiological mechanisms in renal cystic diseases10.3389/fbioe.2021.624553 ↗
13. Studying the impact of geometrical and cellular cues on myogenesis with a skeletal muscle-on-chip10.1039/D4LC00417E ↗
14. From shape to function: the next step in bioprinting10.1002/adma.201906423 ↗
15. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis10.1038/nrm2222 ↗
16. Geometry as a factor for tissue growth: towards shape optimization of tissue engineering scaffolds10.1002/adhm.201200159 ↗
17. Formation of elongated fascicle-inspired 3D tissues consisting of high-density, aligned cells using sacrificial outer molding10.1039/C4LC00023D ↗
18. Multiscale engineered human skeletal muscles with perfusable vasculature and microvascular network recapitulating the fluid compartments10.1088/1758-5090/ac933d ↗
19. Advances in engineering human tissue models10.3389/fbioe.2020.620962 ↗
20. A novel extrusion-based 3D bioprinting system for skeletal muscle tissue engineering10.1088/1758-5090/acb573 ↗
21. 3D bioprinted human skeletal muscle constructs for muscle function restoration10.1038/s41598-018-29968-5 ↗
22. Bioinks and bioprinting: a focused review10.1016/j.bprint.2020.e00080 ↗
23. Fabrication of liver microtissue with liver decellularized extracellular matrix (dECM) bioink by digital light processing (DLP) bioprinting10.1016/j.msec.2020.110625 ↗
24. A digital light processing 3D printed magnetic bioreactor system using silk magnetic bioink10.1088/1758-5090/abfaee ↗
25. Expanding and optimizing 3D bioprinting capabilities using complementary network bioinks10.1126/sciadv.abc5529 ↗
26. Mechanical stimulation improves tissue-engineered human skeletal muscle10.1152/ajpcell.00595.2001 ↗
27. Skeletal muscle tissue engineering: methods to form skeletal myotubes and their applications10.1089/ten.teb.2013.0534 ↗
28. Biomaterials in tendon and skeletal muscle tissue engineering: current trends and challenges10.3390/ma11071116 ↗
29. Smooth muscle cell alignment and phenotype control by melt spun polycaprolactone fibers for seeding of tissue engineered blood vessels10.1155/2015/434876 ↗
30. Mechanical stretching boosts expansion and regeneration of intestinal organoids through fueling stem cell self-renewal10.1186/s13619-022-00137-4 ↗
31. Remote magnetic microengineering and alignment of spheroids into 3D cellular fibers10.1002/adfm.202204850 ↗
32. Mechanical loading stimulates hypertrophy in tissue‐engineered skeletal muscle: molecular and phenotypic responses10.1002/jcp.28923 ↗
33. A novel bioreactor for the generation of highly aligned 3D skeletal muscle-like constructs through orientation of fibrin via application of static strain10.1016/j.actbio.2015.06.033 ↗
34. Three-dimensional cell and tissue patterning in a strained fibrin gel system10.1371/journal.pone.0001211 ↗
35. Cyclic mechanical stimulation favors myosin heavy chain accumulation in engineered skeletal muscle constructs10.1177/228080001000800202 ↗
36. A 3D magnetic tissue stretcher for remote mechanical control of embryonic stem cell differentiation10.1038/s41467-017-00543-2 ↗
37. Evolution of a confluent gut epithelium under on-chip cyclic stretching10.1103/PhysRevResearch.4.023032 ↗
38. The potential of magnetic hyperthermia for triggering the differentiation of cancer cells10.1039/C8NR05946B ↗
39. Photothermia at the nanoscale induces ferroptosis via nanoparticle degradation10.1038/s41467-023-40258-1 ↗
40. Combination of magnetic hyperthermia and immunomodulators to drive complete tumor regression of poorly immunogenic melanoma10.1007/s00262-022-03345-8 ↗
41. Parallelized manipulation of adherent living cells by magnetic nanoparticles-mediated forces10.3390/ijms21186560 ↗
42. Cell patterning using magnetite nanoparticles and magnetic force10.1002/bit.21322 ↗
43. Scaffold-free, label-free and nozzle-free biofabrication technology using magnetic levitational assembly10.1088/1758-5090/aac900 ↗
44. Rapid construction and enhanced vascularization of microtissue using a magnetic control method10.1088/1758-5090/abe4c2 ↗
45. Novel methodology for fabrication of tissue-engineered tubular constructs using magnetite nanoparticles and magnetic force10.1089/ten.2005.11.1553 ↗
46. Magnetically bioprinted human myometrial 3D cell rings as a model for uterine contractility10.3390/ijms18040683 ↗
47. Remote magnetic nanoparticle manipulation enables the dynamic patterning of cardiac tissues10.1002/adma.201904598 ↗
48. Magnetic bioprinting of stem cell-based tissues10.1016/j.bprint.2023.e00265 ↗
49. Magnetic levitational bioassembly of 3D tissue construct in space10.1126/sciadv.aba4174 ↗
50. Magnetic activation of TREK1 triggers stress signalling and regulates neuronal branching in SH-SY5Y cells10.3389/fmedt.2022.981421 ↗
51. High‐throughput differentiation of embryonic stem cells into cardiomyocytes with a microfabricated magnetic pattern and cyclic stimulation10.1002/adfm.202002541 ↗
52. Magnetic bioprinting and actuation of stretchable muscle tissue10.1002/adhm.202503035 ↗
53. Magnetic microtweezers: a tool for high‐throughput bioseparation in sub‐nanoliter droplets10.1002/admt.202200747 ↗
54. How cellular processing of superparamagnetic nanoparticles affects their magnetic behavior and NMR relaxivity10.1002/cmmi.504 ↗
55. The influence of matrix integrity on stress-fiber remodeling in 3D10.1016/j.biomaterials.2012.06.103 ↗
56. Role of boundary conditions in determining cell alignment in response to stretch10.1073/pnas.1715059115 ↗
57. Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding10.1016/j.actbio.2011.05.034 ↗
58. Two characteristic regimes in frequency-dependent dynamic reorientation of fibroblasts on cyclically stretched substrates10.1529/biophysj.107.128611 ↗
59. Combining dynamic stretch and tunable stiffness to probe cell mechanobiology in vitro10.1371/journal.pone.0023272 ↗
60. Cell orientation under stretch: a review of experimental findings and mathematical modelling10.1016/j.jtbi.2023.111564 ↗
61. Magnetically driven formation of 3D freestanding soft bioscaffolds10.1126/sciadv.adl1549 ↗
62. A review on four-dimensional (4D) bioprinting in pursuit of advanced tissue engineering applications10.1016/j.bprint.2022.e00203 ↗
63. Actomyosin controls planarity and folding of epithelia in response to compression10.1038/s41563-019-0461-x ↗
64. Active viscoelastic models for cell and tissue mechanics10.1098/rsos.231074 ↗
65. Mechanical instabilities of biological tubes10.1103/PhysRevLett.109.018101 ↗
66. Computational models for mechanics of morphogenesis10.1002/bdrc.21013 ↗
67. Reciprocal cell-ECM dynamics generate supracellular fluidity underlying spontaneous follicle patterning10.1016/j.cell.2022.04.023 ↗
68. 3D bioprinting of hepatocytes: core–shell structured co-cultures with fibroblasts for enhanced functionality10.1038/s41598-021-84384-6 ↗
69. Fracture in living tissues10.1016/j.tcb.2022.01.005 ↗
70. Rupture strength of living cell monolayers10.1038/s41563-024-02027-3 ↗
71. Characterizing the mechanics of cultured cell monolayers10.1073/pnas.1213301109 ↗
72. Transversely isotropic tensile material properties of skeletal muscle tissue10.1016/j.jmbbm.2009.03.004 ↗
73. Experimental characterization of post rigor mortis human muscle subjected to small tensile strains and application of a simple hyper-viscoelastic model10.1177/0954411914555422 ↗
74. Effect of strain rates on the mechanical response of whole muscle bundle10.1007/s10867-023-09630-6 ↗
75. Detachment and fracture of cellular aggregates10.1039/c2sm26648b ↗
76. Squeezing and detachment of living cells10.1016/j.bpj.2010.10.008 ↗
77. Energy landscapes of receptor–ligand bonds explored with dynamic force spectroscopy10.1038/16219 ↗
78. Interplay of damage and repair in the control of epithelial tissue integrity in response to cyclic loading10.1016/j.ceb.2025.102511 ↗
79. Adherens junction length during tissue contraction is controlled by the mechanosensitive activity of actomyosin and junctional recycling10.1016/j.devcel.2018.10.025 ↗
80. A review of experimental and theoretical research on the deformation and failure behavior of rocks subjected to cyclic loading10.1016/j.jrmge.2021.03.012 ↗
81. Numerical investigation on the effect of thickness and stress level on fatigue crack growth in notched specimens10.1016/j.tafmec.2021.103138 ↗
82. Surface tension and neuronal sorting in magnetically engineered brain‐like tissue10.1002/advs.202302411 ↗
83. Managing magnetic nanoparticle aggregation and cellular uptake: a precondition for efficient stem‐cell differentiation and MRI tracking10.1002/adhm.201200294 ↗