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Biohybrid robotics: From the nanoscale to the macroscale

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Abstract Biohybrid robotics is a field in which biological entities are combined with artificial materials in order to obtain improved performance or features that are difficult to mimic with hand‐made materials. Three main level of integration can be envisioned depending on the complexity of the biological entity, ranging from the nanoscale to the macroscale. At the nanoscale, enzymes that catalyze biocompatible reactions can be used as power sources for self‐propelled nanoparticles of different geometries and compositions, obtaining rather interesting active matter systems that acquire importance in the biomedical field as drug delivery systems. At the microscale, single enzymes are substituted by complete cells, such as bacteria or spermatozoa, whose self‐propelling capabilities can be used to transport cargo and can also be used as drug delivery systems, for in vitro fertilization practices or for biofilm removal. Finally, at the macroscale, the combinations of millions of cells forming tissues can be used to power biorobotic devices or bioactuators by using muscle cells. Both cardiac and skeletal muscle tissue have been part of remarkable examples of untethered biorobots that can crawl or swim due to the contractions of the tissue and current developments aim at the integration of several types of tissue to obtain more realistic biomimetic devices, which could lead to the next generation of hybrid robotics. Tethered bioactuators, however, result in excellent candidates for tissue models for drug screening purposes or the study of muscle myopathies due to their three‐dimensional architecture. This article is categorized under: Therapeutic Approaches and Drug Discovery > Emerging Technologies Nanotechnology Approaches to Biology > Nanoscale Systems in Biology
Applications of enzyme‐powered micromotors. (a) SEM image of silica microparticles used to fabricate urease‐powered micromotors. Adapted with permission from Patiño, Feiner‐Gracia, et al. (2018). (b) Computer‐generated representation of the location of the heterogeneous localization of enzymes, obtained with super resolution microscopy. Adapted with permission from Patiño, Feiner‐Gracia, et al. (2018). (c) Speed of the urease‐powered micromotors depending on the amount of detected enzyme molecules on its surface. Adapted with permission from Patiño, Feiner‐Gracia, et al. (2018). (d) Average speed of biohybrid micromotors based on hollow silica microparticles depending on the enzyme used as biocatalytic engine. Inset shows the correlation of the speed with the catalytic rate of the enzyme. Adapted with permission from Arqué et al. (2019). (e) Effect of the ionic strength of NaOH in the speed of these micromotors with or without an mPEG coverage. Adapted with permission from Arqué et al. (2020). (f) 3D trajectory mapping of urease‐powered micromotors showing directionality in all directions. Adapted with permission from Arqué et al. (2020). (g) Schematic fabrication of the Janus platelet motors powered by urease. Right: Fluorescent images in Cy5‐labeled urease showing the Janus functionalization of the motors. Adapted with permission from Tang et al. (2020). (h) Enhanced diffusion of Janus and non‐Janus motors after the addition of urea. Adapted with permission from Tang et al. (2020)
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Applications of biohybrid nanomotors powered by enzymatic reactions. (a) Schematic representation of a urease‐powered silica nanomotor functionalized with antibodies for enhanced penetration in bladder cancer spheroids. Confocal fluorescence images of nanomotors incubated with spheroids at 0 and 40 mM of urea (scale bars are 50 μm). Green: targeted antigen (FGFR3); red: nanomotors. Adapted with permission from Hortelao et al. (2019). (b) Schematic representation of urease‐powered nanomotors radiolabeled with Fluorine‐18 and Iodine‐124 (attached to gold nanoparticles). Bottom images show swarming behavior of these nanomotors after the addition of urea via PET in vitro. Adapted with permission from Hortelao, Simó, et al. (2020). (c) in vivo PET‐CT images of urease nanomotors radiolabeled with Fluodine‐18 after intravesicular administration, with and without urea, showing their distribution in the bladder of mice. Adapted with permission from Hortelao, Simó, et al. (2020). (d) Schematic representation of an asymmetric polymerosome nanomotor propelled by the tandem reaction of GOx and catalase. Bottom images show characterizations of the polymerosome imaged under several types of staining targeting different polymers. Adapted with permission from Joseph et al. (2017). (e) Normalized trajectories and corresponding mean squared displacements (MSDs) of asymmetric polymerosomes under different conditions of fuels and directions. Adapted with permission from Joseph et al. (2017)
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Biohybrid nanomotors powered by enzymatic reactions. (a) Top: Schematic of the structure and working mechanism of a biocatalytic Janus mesoporous silica nanomotor. Bottom: Transmission electron microscope (TEM) image of the mesoporous silica nanoparticles that compose such motor. Adapted with permission from Ma and Sánchez (2017). (b) Top: Schematic representation of the motion of urease‐powered nanotubes depending on enzyme localization: Inside and outside (up) or only inside (bottom). Bottom: Scanning electron microscope (SEM) image of the silica nanotubes. Adapted with permission from Ma, Hortelao, et al. (2016). (c) Top: Schematic representation of the structure and working mechanism of a polymeric stomatocyte nanomotor with multiple enzymes encapsulated in its interior and working via cascade decomposition of glucose and hydrogen peroxide by GOx and catalase. Bottom: TEM image of a group of polymeric stomatocytes used to fabricate this nanomotor. Adapted with permission from Abdelmohsen et al. (2016). (d) Top: Schematic representation of lipobots with urease molecules outside or inside the lipidic layer. Bottom: Confocal laser scanning microscopy images of urease (red) in micrometer‐sized lipobots (green) with the enzyme located outside or inside. Scale bars are 2 μm. Adapted with permission from Hortelao, García‐Jimeno, et al. (2020)
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Biohybrid microrobots based on single cells. (a) Optical microscopy image of a sperm‐driven microrobot with a streamlined cap design. Adapted with permission from Striggow et al. (2020). (b) SEM image of a biohybrid microrobot based on Escherichia coli. The bacterium attaches preferentially to the metallic Fe surface of the microparticle, deposited by e‐beam. Adapted with permission from Stanton et al. (2016). (c) Fluorescent image of a swarm of bacteria‐based microswimmers moving by chemotaxis toward the upper side of the image. Inset shows a fluorescently labeled image of a microswimmer, composed of a polystyrene bead and several S. marcescens attached in random positions. Adapted with permission from Zhuang and Sitti (2016). (d) Fluorescent confocal microscopy image of several Salmonella typhimurium bacteria (green) attached to polystyrene beads (red) to form a bacteriobot. Adapted with permission from S. J. Park et al. (2013). (e) (Top) SEM image of a nonpathogenic magnetotactic bacterium Magnetosopirrillum gryphiswalense (MSR‐1), with an inset of TEM image showing the distribution of the internal magnetosome. (Bottom) SEM image of an MSR‐1 bacterium captured within a microtube, forming a biohybrid micromotor. Adapted with permission from Stanton et al. (2017)
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Status of biohybrid research in the literature, as of June, 2020. (a) Number of papers and percentage published between 2000 and June, 2020 on biohybrid robots. The analysis was performed in the Web of Science database searching for the following keywords in their title or abstract: “bio‐hybrid actuator*,” “biohybrid actuator*,” “cell‐based actuator*,” “bacteria robot*,” “muscle bioactuator*,” “muscle‐based bioactuator*,” “muscle‐based bio‐actuator*,” “bioactuator*,” “bioactuator*,” “biohybrid robot*,” “bio‐hybrid robot*,” “hybrid bio‐robot*,” “hybrid biorobot*,” “bio bot*,” “bio‐hybrid device*,” “biohybrid device*,” “bio‐hybrid system*,” “biohybrid system*.” (b) Number of publications on biohybrid robots according to their type (Note:  Several publications could have duplicate types). The search was performed using the same keywords. (c) Number of publications on biohybrid robots according to their field. The search was performed using the same keywords
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Biohybrid robots based on skeletal muscle tissue. (a) Image representing the formation of a biobot. On the bottom, comparison of the motion of a biobot with a symmetric skeleton and with an asymmetric one via finite element analysis (FEA) simulations, showing that only the asymmetric skeleton produces net motion. Adapted with permission from Cvetkovic et al. (2014) and Pagan‐Diaz et al. (2018). (b) Displacement in time of large biobots at different frequencies, compared with numerical simulations of their motion. On the bottom, a schematic of the working mechanism by friction differences due to the asymmetry. Adapted with permission from Pagan‐Diaz et al. (2018). (c) Schematic representation of the coculture of neurospheres with skeletal muscle tissue after 8 days of differentiation of the muscle, for the fabrication of a biohybrid swimmer. Normally, at day 11, neurite growth can be already observed. (d) Below, optical microscopy image of the biohybrid swimmer after release from its anchors, indicating the position of the muscle tissue and the neurospheres, which are activated via optical stimulation to induce contractions and swimming motion. Adapted with permission from Aydin et al. (2019). (d) (i) schematic representation of the spring‐based muscle‐powered swimmer and (ii) optical image of the assembly. (iii) Tracking of the biohybrid robot swimming at 1 Hz for 30 s at the air‐liquid interface. (iv) Speed of the swimmer at different frequencies and (v) hydrodynamics FEA simulations of the flow around the skeleton during a contraction, showing a heterogeneous distribution of the flow lines due to the asymmetry in the design, which leads to motion. Adapted with permission from Guix et al. (2020)
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Biohybrid actuators based on skeletal muscle tissue. (a) Image of a biohybrid actuator based on an antagonistic pair of skeletal muscle tissues. Scale bar: 5 mm. Adapted with permission from Morimoto et al. (2018). (b) Schematic representation and real images of a biohybrid actuator covered with a collagen structure for actuation in air. Perfusion tubes allow the flow of culture media to the muscle tissue. Scale bar: 2 mm. Adapted with permission from Morimoto et al. (2020). (c) (i) completely 3D‐bioprinted bioactuators composed of two PDMS posts surrounded by skeletal muscle tissue, (ii) which can be used as a force measurement platform. Iii) force increase after exercising the bioactuators with electric pulses of different frequency over a period of 4 days. Adapted with permission from Mestre, Patiño, Barceló, et al. (2019). (d) (i) Immunostaining images of young human skeletal muscle myocytes in the force measurement platform and aged‐induced with atrophic fibers after the addition of 40 ng/mL of the cytokine TNF‐α. scale bars = 80 μm. (ii) Contraction force profiles after a sustained stimulation of 75 Hz, showing the relaxing effects of a cosmetic peptide, proving the use of the bioactuators as a drug testing platform. Adapted with permission from Mestre, Garcia, et al. (2020)
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Biohybrid robots based on cardiac muscle tissue. (a) Snapshots of muscular thin films with different conformations upon contractions. Adapted with permission from Feinberg et al. (2007). (b) (i) Snapshots and motion mechanism due to friction of a biohybrid robot based on a thin film of cardiomyocytes. (ii) Plot of friction vs force of each one of the legs of the biobot (supporting and actuating), indicating that motion happens when the coefficient of static friction of the actuating leg is larger than the coefficient of kinetic friction of the supporting leg. Adapted with permission from Chan et al. (2012). (c) (i) Image of a biohybrid stingray made of a mold‐casted PDMS structure stabilized with a gold skeleton and cardiomyocytes seeded on top. Right‐hand images were immunostained for sarcomeric –actinin (red) and cell nuclei (blue), revealing its sarcomeric structures. (ii) A dense serpentine pattern of fibronectin was used to guide the attachment of cardiac cells and engineer a wave propagation pattern that simulated the deflection of a stingray's fins. (iii) Kinematic analysis of the distance traveled and speed of a biohybrid stingray upon different types of optical stimulation. Adapted with permission from S. J. Park et al. (2016)
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Nanotechnology Approaches to Biology > Nanoscale Systems in Biology
Therapeutic Approaches and Drug Discovery > Emerging Technologies

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