Biohybrid Actuators Based on Skeletal Muscle-Powered Microgrooved Ultrathin Films Consisting of Poly(styrene-block-butadiene-block-styrene).

This paper describes a biohybrid actuator consisting of a microgrooved thin film, powered by contractile, aligned skeletal muscle cells. The system was made of a thermoplastic elastomer [SBS, poly(styrene-block-butadiene-block-styrene)]. We prepared SBS thin films with different thicknesses (0.5-11.7 μm) and Young's moduli (46.7-68.6 MPa) to vary their flexural rigidity. The microgrooves on the SBS thin film resembled the microstructure of the extracellular matrix of muscle and facilitated the alignment and differentiation of skeletal muscle cells. Electrical stimulation was applied to self-standing biohybrid thin films to trigger their contraction, enabled by the low flexural rigidity of the SBS thin film. Finite element model simulations were also examined to predict their contractile behavior. We achieved the prediction of displacements, which were rather close to the actual values of the SBS thin film: the discrepancy was <5% on the X axis. These results pave the way for in silico prediction of the contractile capabilities of elastomeric thin films. This study highlights the potential of microgrooved SBS thin films as ultraflexible platforms for biohybrid machines.

[1]  Ritu Raman,et al.  Damage, Healing, and Remodeling in Optogenetic Skeletal Muscle Bioactuators , 2017, Advanced healthcare materials.

[2]  T. Fujie,et al.  Heterofunctional nanosheet controlling cell adhesion properties by collagen coating , 2012, Journal of biomaterials applications.

[3]  R. Close Dynamic properties of mammalian skeletal muscles. , 1972, Physiological reviews.

[4]  Ritu Raman,et al.  Three-dimensionally printed biological machines powered by skeletal muscle , 2014, Proceedings of the National Academy of Sciences.

[5]  M. N. Hamdan,et al.  Parametric Study of Dynamic Wrinkling in a Thin Sheet on Elastic Foundation , 2012 .

[6]  Megan L. McCain,et al.  A tissue-engineered jellyfish with biomimetic propulsion , 2012, Nature Biotechnology.

[7]  R. Duffy,et al.  Optimizing the structure and contractility of engineered skeletal muscle thin films. , 2013, Acta biomaterialia.

[8]  Barbara Mazzolai,et al.  Robotics: Generation soft , 2016, Nature.

[9]  Adam W Feinberg,et al.  Engineered skeletal muscle tissue for soft robotics: fabrication strategies, current applications, and future challenges. , 2014, Wiley interdisciplinary reviews. Nanomedicine and nanobiotechnology.

[10]  Shuichi Takayama,et al.  Large‐Scale, Ultrapliable, and Free‐Standing Nanomembranes , 2013, Advanced materials.

[11]  T. Fujie,et al.  Large‐Scale Fabrication of Porous Polymer Nanosheets for Engineering Hierarchical Cellular Organization , 2016 .

[12]  Satoshi Arai,et al.  Gold Nanoshell-Mediated Remote Myotube Activation. , 2017, ACS nano.

[13]  Xiaochen Wu,et al.  Activation of Actuating Hydrogels with WS2 Nanosheets for Biomimetic Cellular Structures and Steerable Prompt Deformation. , 2017, ACS applied materials & interfaces.

[14]  Ali Khademhosseini,et al.  Engineered nanomembranes for directing cellular organization toward flexible biodevices. , 2013, Nano letters.

[15]  R. Bashir,et al.  Creating Living Cellular Machines , 2013, Annals of Biomedical Engineering.

[16]  Ian D. Walker,et al.  Soft robotics: Biological inspiration, state of the art, and future research , 2008 .

[17]  Jeong-Woo Choi,et al.  Phototactic guidance of a tissue-engineered soft-robotic ray , 2016, Science.

[18]  Jinchao Xu,et al.  A scalable consistent second-order SPH solver for unsteady low Reynolds number flows , 2015 .

[19]  G. Whitesides,et al.  Muscular Thin Films for Building Actuators and Powering Devices , 2007, Science.

[20]  Ali Khademhosseini,et al.  Interdigitated array of Pt electrodes for electrical stimulation and engineering of aligned muscle tissue. , 2012, Lab on a chip.

[21]  Ali Khademhosseini,et al.  Directed 3D cell alignment and elongation in microengineered hydrogels. , 2010, Biomaterials.

[22]  L. Ricotti,et al.  Thin polymeric films for building biohybrid microrobots , 2017, Bioinspiration & biomimetics.

[23]  Paolo Dario,et al.  Biohybrid actuators for robotics: A review of devices actuated by living cells , 2017, Science Robotics.

[24]  Dogan Gidon,et al.  Photocrosslinking of styrene-butadiene-styrene (SBS) networks formed by thiol-ene reactions and their influence on cell survival , 2015, Biomedical materials.

[25]  Anna Grosberg,et al.  Simulating muscular thin films using thermal contraction capabilities in finite element analysis tools. , 2016, Journal of the mechanical behavior of biomedical materials.

[26]  P. Dario,et al.  Self-assembly of polydimethylsiloxane structures from 2D to 3D for bio-hybrid actuation , 2015, Bioinspiration & biomimetics.

[27]  D. Bodas,et al.  Hydrophilization and hydrophobic recovery of PDMS by oxygen plasma and chemical treatment—An SEM investigation , 2007 .

[28]  J. Hickman,et al.  Correlation of embryonic skeletal muscle myotube physical characteristics with contractile force generation on an atomic force microscope-based bio-microelectromechanical systems device. , 2013, Applied physics letters.

[29]  R. Xiao,et al.  Bio‐Origami Hydrogel Scaffolds Composed of Photocrosslinked PEG Bilayers , 2013, Advanced healthcare materials.

[30]  Toshia Fujisato,et al.  Control of myotube contraction using electrical pulse stimulation for bio-actuator , 2009, Journal of Artificial Organs.

[31]  Ritu Raman,et al.  Optogenetic skeletal muscle-powered adaptive biological machines , 2016, Proceedings of the National Academy of Sciences.

[32]  A. Khademhosseini,et al.  Aligned Carbon Nanotube–Based Flexible Gel Substrates for Engineering Biohybrid Tissue Actuators , 2015, Advanced functional materials.

[33]  M. Shikida,et al.  Assembly of skeletal muscle cells on a Si-MEMS device and their generative force measurement , 2010, Biomedical microdevices.

[34]  Mattia Gazzola,et al.  Simulation and Fabrication of Stronger, Larger, and Faster Walking Biohybrid Machines , 2018, Advanced Functional Materials.